Behavioral Ecology and Sociobiology

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Lifespan for the different selection regimes in both sexes either isolated or in mixed-sex groups. Light grey line: FLX regime, dark grey line: CFM regime, and black line Cwt regime. a Female lifespan when isolated. We did not find any significant difference in lifespan between the three regimes when kept isolated. b Female lifespan in mixed-sex groups. We did find a significant difference in lifespan between the three regimes when the females were continuously exposed to males (p = 0.030). c Male lifespan when isolated. We found a significant difference in lifespan between the three regimes when the males were kept isolated (p = 6.765e⁻⁰⁵). d Male lifespan in mixed-sex groups. There were no significant different in lifespan between the three regimes, when the males could continuously mate with females
Article
  • Katrine K. Lund-HansenKatrine K. Lund-Hansen
  • Megan A. M. KutzerMegan A. M. Kutzer
  • Sophie A. O. ArmitageSophie A. O. Armitage
  • [...]
  • Jessica K. AbbottJessica K. Abbott
Sexual dimorphism in somatic investment may be shaped by two distinct forms of sexual conflict; under intralocus sexual conflict (IASC), males and females have different optimal levels of somatic investment but are constrained from reaching their respective optima by their shared genome, while under interlocus sexual conflict (IRSC), males and females have different optimal sexual strategies, which could have direct or indirect effects on levels of somatic investment. We investigated effects of IASC and IRSC on two aspects of somatic investment, immune defence strategies and longevity, using previously established female-limited experimental evolution lines in Drosophila melanogaster. We found little evidence for any effect of either type of sexual conflict on investment in the immune defence resistance or tolerance. Nor did we find convincing evidence that longevity is subject to IASC in this species. However, we did find evidence that increased female control over mating rate had important and opposite effects on longevity between the sexes. Specifically, females that had adapted to high levels of female control over mating had a longer lifespan when kept in mixed-sex groups, while males had shorter longevity, perhaps due to increased investment in post-copulatory sexual selection. These novel results show that female control over mating rates may have important and unexpected effects on patterns of somatic investment. Significance statement Sexual conflict occurs between the two sexes over numerous life history traits, and it is complex to disentangle how these traits interact and affect each other. Here we use a long-term evolution experiment to investigate sexual dimorphism in somatic maintenance. We found no effect of feminising the X chromosome on female immune defence. However, we did find that increased female control over mating rate resulted in longer female lifespan, but reduced male lifespan, and that these effects were dependent on social context (isolated or in mixed-sex groups). Unlike previous studies on the effect of sexual conflict on longevity, our experiment did not manipulate environmental conditions nor the adult sex ratio, which is likely to reduce both pre- and post-copulatory sexual selection.
 
Article
The widespread occurrence of extra-pair paternity (EPP) in birds adds rich complexity to our understanding of sexual selection and mating system evolution. Extra-pair matings are typically cryptic so for most species, we lack the detailed behavioral observations needed to fully determine whether both sexes benefit from EPP and when trait correlations with EPP are found, whether they reflect female choice or male intrasexual competition. Here we examine behavioral and morphological correlates of EPP in the lark bunting (Calamospiza melanocorys), a grassland songbird where EPP-seeking behaviors of males are unusually overt and conspicuous. Males sought EPP by closely following receptive pairs, often in groups. Virtually all observed extra-pair copulation attempts involved male aggression, were resisted by females, and larger females had a lower rate of extra-pair paternity in their nests. Male plumage traits predicted both male effort in seeking EPP (number of mating groups joined) and fitness gained through EPP; these same male traits have previously been linked to male-male competition but were not linked to consistent mate choice in lark buntings. There was no trade-off between investment in seeking EPP and fitness at a male’s own nest, indicating that fitness from EPP is likely a potent driver of sexual selection in lark buntings, one that may not entirely be driven by female fitness interests.
 
Female mountain katydids performing their displays at various intensities (A) score of zero, no stripes showing, (B) score of two (C), three red stripes, a maximum intensity score. Image credits: Michael R Whitehead
Observed display intensity of female (a) and male (b) katydids across the 10 attack replicates in an arena without plants (grey) and in an arena with plants (green), repeated across three consecutive trials. Predicted probability of each display score intensity for females (c) and males (d) according to the model. In all panels, plant presence is in green and absence in grey
Escape probability of female (a) and male (b) katydids across the 10 attack replicates in an arena without plants (grey) and in an arena with plants (green), repeated across three consecutive trials
Repeatability estimates for display intensity in 75 individual katydids, across five trials (a) original-scale repeatability estimations and (b) link-scale repeatability estimations
Article
How and when deimatic behaviours are performed can change during encounters between predators and prey. Some predators attack repeatedly, investigating and manipulating prey, and in response, an individual’s deimatic behaviour may intensify or may diminish in favour of escaping. The presence of a resource can further force a trade-off between displaying and escaping. Here, we examined the intensity of the katydid’s deimatic behaviour, a visual display, the propensity of their escape response under repeated simulated attacks, and how these responses change in the presence of foraging resources. We found that display intensity increased with repeated simulated attacks and that females displayed at a greater intensity than males. The presence of their preferred food plant had no significant effect on display intensity, but reduced escape probability in both sexes. Some katydids were predictable in their display intensity and at the population level we found that strong display intensity is moderately repeatable. Overall, our results suggest that 1) display intensity increases with repeated attacks and might indicate a cost in performing at maximum intensity upon first attack, 2) deploying a deimatic display while feeding can reduce the need to flee a rich foraging patch and 3) some individuals are consistent in their display intensities. Future experiments that aim to determine causal mechanisms such as limitations to perception of predators, sensitisation to stimuli and physiological constraints to display intensity will provide necessary insight into how deimatic displays function. Significance statement Though often regarded as success or failure, interactions between predators and prey during the attack phase of a predation event are complex, especially when predators make repeated investigative attacks in quick succession. Our study shows that in mountain katydids, intensity of deimatic behaviour increases with repeated attacks, perhaps indicating that prey sensitise or that maximal displays during initial attacks carry high costs such as conspicuousness. The intensity of the display does not change with the introduction of a valuable food resource, but the probability of fleeing decreased, suggesting that displaying may reduce the opportunity costs of leaving a patch. We also show that individuals vary in the repeatability of their display, suggesting that deimatic display may be highly adaptable, nuanced and targeted.
 
Timeline of Chinese imperial dynasties from 221 BC to 1911 AD. The gray-colored are the dynasties that lasted more than 100 years, which were included in this study
Imperial family structure and its managerial system depicted for the Qing dynasty. Harem was the main part of the Forbidden City which is a penalty zone for other fertile men except emperor and his sons. Lower-rank persons can not into upper strata of regions who live can only be carried out in specified areas
Article
Sexual selection echoed by the sex ratio is a critical issue in evolution and reproductive biology studies, and the second sex ratio (sex ratio at birth, SRB) is an important evaluation indicator for sex regulation. However, broad debates on sex ratio at birth exist due to the lack of a clear spatiotemporal genealogical database. This study explicitly tests the Trivers and Willard’s hypothesis stating that parents with good social conditions tend to show a male-biased SRB. Using a database of Chinese imperial families from 211BC to 1912 (2142 years) which avoids the spatiotemporal confusion of data thanks to its clear boundaries and long timespan, we found that a proportion of males at birth was 0.54. In particular, the results indicate that the empresses generated a significantly higher male-biased SRB than the concubines within the imperial harems (0.61 vs 0.53), while the SRB of concubines was not higher than ordinary people (0.53 vs 0.52). A significant difference of SRB before and after empress coronation (0.48 vs 0.65) was detected, indicating that the change to a higher social status is the leading cause of a biased SRB. These findings suggest that mothers with privileged instant social conditions tend to generate more boys than girls. In other words, a higher maternal social rank during the conception period, instead of rich resources, forms the primary mechanism regulating the SRB. Significance statement Adaptive sex ratio has been a debatable topic difficult to clearly verify since the publication of Trivers and Willard Hypothesis in 1973, which proposes that parents who have good conditions should produce more male offspring. The one reason is that the validity and sample size of the databases used contained unavoidable confounding noise, both genealogically and genetically. To overcome these issues, we specifically compiled a historical database of Chinese imperial families, which are characterized by a confined mating harem and unique eunuch system, guaranteeing biological and genetic purity with precise genealogical relationships and genetic linkages between the parents and the offspring. Thus, this is an extraordinary effort to clarify the hypotheses proposed by TWH and other hypotheses.
 
Colonies but not social phenotypes differ in gut bacterial diversity and composition. A and B Diversity and C and D composition of gut bacterial communities among every individual colored according to colonies and social phenotype. The ordinations in (C and D) depict the first two coordinate axes of a PCoA of weighted UniFrac distance among every individual sample in the cross-sectional study. Panels E and F depict the relative abundance of bacterial phyla and families within the Bacteroidetes and Firmicutes across colonies (E) and phenotypes (F). Colors refer to colony in panels A, C, and E and phenotype in panels B, D, and F
The gut bacteria of newly paired individuals do not resemble one another over time. Gut bacterial diversity (A) of paired individuals and the difference in diversity between paired animals (B) over the course of isolation. Shapes in panel A refer to sex. (C) The ordination depicts the first two coordinate axes of a PCoA of weighted UniFrac distance among every individual sample in the longitudinal study. Colors refer to unique animals pairs, shape refers to timepoint, and outline refers to sex. The inset panel in C illustrates the within-pair compositional dissimilarity among pairs across the time course
Experimental factors affecting the abundance of the naked mole-rat core gut bacterial community. The phylum assignment of each ASV represented in the phylogenetic tree is shown in the first column of panel A. Columns 1–6 show the effects of different factors within the cross-sectional study on the abundance of individual ASVs (column numbers refer to the factors listed on the x-axis in panel B). Columns 7–9 show the effects of different factors within the longitudinal study. We used a consensus approach using three differential abundance analysis methods (see “Materials and methods”). Cells colored yellow, blue, or purple represent significant effects of experimental factors on taxon abundance found with one, two, or all three methods, respectively (false discovery rate adjusted P values < 0.05). We summarize the consensus distribution among all ASVs for each experimental factor in panel B. Full differential abundance results can be found in Supplemental Dataset S1
The A diversity and B composition of gut bacteria across host species and sex. The ordination in (B) depicts the first two coordinate axes of a PCoA of weighted UniFrac distance among every individual sample in the dataset. The compositional differences between the gut bacteria of H. glaber and M. musculus are largely driven by C shifts in the relative abundance of the two major bacterial phyla colonizing mammalian guts, Firmicutes and Bacteroidetes. D A number of abundant families in addition to Prevotellaceae and Lactobacillaceae exhibit differential abundance between H. glaber and M. musculus (note results from the DESeq2 analysis are shown but all three methods used to analyze differential abundance yield qualitatively identical results; Supplemental Dataset S1)
Article
Group living occurs across the animal kingdom and can shape fundamental aspects of individual biology, including the microbes inhabiting the animal gut. The naked mole-rat, Heterocephalus glaber, exhibits extreme cooperative breeding (eusociality) and presents an ideal opportunity to study the effects of social structure on the mammalian gut microbiota. Within colonies reproduction is limited to few animals, while the remaining members are non-reproductive, form linear dominance hierarchies, and show evidence of task specialization with stable yet plastic behavioral phenotypes. Here, we sequenced the gut bacteria of naked mole-rats across 6 replicate captive colonies and longitudinally during a colony removal experiment. Colony had much larger effects than social phenotype or status on the diversity and composition of gut bacteria. Our longitudinal experiment revealed that over the course of 2 months, the gut bacteria of previously unfamiliar, newly paired animals did not become more similar. In comparison to mice housed in the same facility, the naked mole-rat gut microbiome exhibited substantial compositional differences including the near absence of Lactobacillaceae and the enrichment of Prevotellaceae. Our study provides new insight into the factors shaping gut bacterial communities in social animals and indicates a prominent role of social group membership but not social phenotype. Significance statement The social groups to which animals belong can be strong determinants of the composition of their associated gut microbial communities (i.e., gut microbiome). However, less is known about the link between social status within animal groups and the gut microbiome. We studied this relationship in the naked mole-rat, Heterocephalus glaber, which exhibits extreme cooperative breeding (eusociality). Animals within naked mole-rat colonies show clear social hierarchies and evidence of social phenotypes. Across replicate colonies, we found that colony but not social phenotype or status had large effects on the diversity and composition of gut bacteria. During a colony removal experiment, the gut bacteria of newly paired but previously unfamiliar animals did not become more similar over the course of 2 months. Our results show that when decoupled from differences in diet or exposure to microbes, within colony social roles and their accompanying unique physiology and social experience may have little effect on gut microbiota. In contrast, gut bacterial diversity and composition was strongly shaped by colony membership despite being exposed to identical environmental conditions.
 
A schematic of the test arena for the tradeoff task. The task was recorded using a camera suspended above the tank. Experiments were conducted in the dark with red night vision lights for recording. The safe and predator areas of the tank were not physically separated, and frogs could swim between both areas. The safe side contained a PVC pipe “hide,” and the predator side contained a food (for both absence and presence of the predator groups). The hide and the food were located 12.7 cm from the ends of the safe and predator sides, respectively. The predator apparatus was located 47 cm from the bottom of the tank and the recording camera was located 58 cm from the bottom of the tank. Figure created by Wendy Beth Jackelow Medical and Scientific Illustration
Timeline of the tradeoff task. Animals were first isolated from the group housing 48 h before the testing began. The animals were moved to the test arena for 24 h prior to the test for acclimation. We recorded three simultaneous time periods on the test day: time period A (no stimulus, 10 min), time period B (absence/presence of predator and food, 30 min), and time period C (new food, no predator, 10 min). After time period C frogs were anesthetized, euthanized, and tissue was collected for RNA extraction
Differences in forelimb sweeps (A), entrances into the predator side (B), total time swimming (C), and time inactive (D) in adult male X. laevis in the absence or presence of a predator across all three test periods. Asterisk indicates a statistically significant difference between predator and non-predator condition at that time point. Bars represent the mean ± S.E.M. of 9–10 animals per group. Asterisk indicates predator-exposed group is significantly different from control group, p < 0.05
Differences in transcript abundance of A corticotropin releasing factor (crf), B dopamine D1 receptor (drd1), C dopamine D2 receptor (drd2), and D serotonin 1a receptor (htr1a) relative to the reference gene, ribosomal protein L8 (rpl8) in the optic tecta of control and predator-exposed X. laevis. Data are represented as mean ± S.E.M. of n = 6–7 animals
Article
Animals often halt foraging in the presence of predator cues, an ecological phenomenon known as the foraging/predator avoidance tradeoff. Although some have proposed that anxiety may exist in animals exposed to predator cues, few studies have examined whether such interactions lead to anxiety-like behavior in animals other than laboratory rodents and zebrafish. In this experiment, a foraging/predator avoidance tradeoff task was modified using adult male African clawed frogs (Xenopus laevis) and a looming visual predator stimulus to determine if (1) visual predator cues reduce appetitive behavior, (2) visual predator cues lead to predator avoidance behavior, and (3) if visual predator cues alter the abundance of transcripts in the optic tectum known to be modulated in other brain areas during anxiety. Frogs exposed to the predator stimulus did not reduce their food intake, although sweeping, a foraging behavior, was significantly reduced by the predator stimulus. Predator-exposed animals spent significantly more time stationary and entered the predator zone less compared controls. There were no statistically significant changes in relative transcript abundance of anxiety-related peptides between the groups in the optic tectum. Collectively, this tradeoff task was able to induce discrete avoidance and appetitive behaviors that are similar to anxiety-like behaviors observed in other predator avoidance models; however, the effects of visual threats on feeding and anxiety-related transcript abundance requires further study. Significance statement Halting foraging activities to increase vigilance and engage avoidance behaviors has been proposed to play an adaptive role in survival of predator encounters in a number of animal species. Some have proposed that anxiety evolved as a state associated with the engagement of avoidance and antipredator behavior. However, few studies have examined whether such foraging/predator avoidance tradeoffs result in anxiety-like behavior in animals other than rodents. We developed a foraging/predator avoidance tradeoff task in an aquatic frog species to determine if the sight of a looming visual threat interferes with feeding and causes anxiety-like behavior in an amphibian. Our data suggest that some, but not other (feeding, for example), behavioral aspects of foraging/predator avoidance tradeoffs mimic anxiety-like behavior when a visual threat is present. These data contribute to a growing body of literature indicating that anxiety may be an adaptive response to predator threats in non-mammalian species.
 
Article
In traditional definitions of endurance rivalry, individuals compete to remain reproductively active longer than their rivals, but these time periods are typically brief, such as a single breeding season. Here, we explored endurance rivalry among adult males in a long-lived species that breeds year-round, the spotted hyena (Crocuta crocuta). We found that most dispersing males navigated the adaptive challenges of remaining in their new clans (“enduring”) for over 2 years before siring their first cub. Additionally, sires remained in their new clans at least 4 years, whereas males that never sired any cubs typically disappeared by their fourth year of tenure. This suggests that males might incorporate their initial reproductive success in the clan into their decisions regarding whether to “endure” by remaining in the current clan or to disperse again to another clan. Finally, we used Bayesian mixed modeling to explore variation in annual male reproductive success, which we found to have a positive linear relationship with tenure and a quadratic relationship with age. A male’s rate of social associations with adult females, but not aggressive interactions with those females, was predictive of his annual reproductive success. We also found substantial individual variation in annual reproductive success across males. Our results support the notion that male spotted hyenas compete via an extended endurance rivalry; tenure unequivocally improves male reproductive success, but advanced age does not, and questions remain regarding other traits that might be salient to the rivalry or to female mate choice in this species. Significance statement Some animals compete indirectly for mates by trying to outlast their competitors during a finite breeding season; individuals that can endure the longest in this “marathon” reap the reproductive rewards. Male spotted hyenas face a different challenge because females breed year-round, so the competition to remain viable as mates is seemingly endless. Here, we show that male spotted hyenas seem to make decisions about whether to stay in a clan based on their initial reproductive success in that clan. For males with early success, the longer they stay and the more time they spend with females, the more cubs they sire each year. Our findings suggest that male spotted hyenas compete for mating opportunities via an “ultramarathon” in which they must remain in a single social group at the bottom of the hierarchy for many years to demonstrate to females their ability to endure.
 
The predicted association between group composition (no. of helper males − no. of helper females provisioning the brood) and the proportion of sons in M. elegans broods under the local resource competition hypothesis (Table 1). Negative values represent groups that are female-biased, whereas positive values represent groups that are male-biased. We predict that the effect of local competition will be stronger for female-biased groups, thus the slope of a > slope of b. The horizontal grey dashed line indicates equal offspring sex ratio
The mean (± SE) proportion of sons in M. elegans broods in relation to whether females lived in groups or pairs. The grey dashed line indicates 50/50 offspring sex ratio. Numbers in the bottom of the plot indicate the number of broods
The mean (± SE) proportion of sons in M. elegans broods in relation to group composition (no. of helper males − no. of helper females provisioning the brood) for breeding females living in groups. The solid red trendline represents the significant between-female effect of the ‘group composition’ predictor according to the top model in Table 3, and the dashed blue trendline represents the non-significant within-female effect of the ‘group composition’ predictor according to model 3 in Table 3. The grey dashed line indicates 50/50 offspring sex ratio and the numbers in the bottom represent the number of broods
Article
Females should facultatively bias offspring sex ratio when fitness returns vary among sexes. In cooperative breeders, where individuals help raise others’ young, overproducing the philopatric sex will be adaptive when helpers are absent, whereas overproducing the dispersive sex may be adaptive to reduce intrasexual competition. Thus, fitness returns are expected to vary with the social environment. However, any offspring sex-ratio biases may also result from consistent among-female differences (e.g. quality) and/or environmental variables (e.g. food availability). Yet, few studies have disentangled facultative from persistent biases. We investigated offspring sex-ratio biases in relation to the social environment in cooperatively breeding red-winged fairy-wrens ( Malurus elegans ). Repeated observations of the same females over nine years allowed for disentanglement of facultative from persistent biases. Females without help did not overproduce daughters, despite female helpers being associated with higher fledgling survival (resource enhancement hypothesis). Instead, females without helpers facultatively overproduced sons —the slower dispersing sex— thereby ensuring long-term helper availability. Furthermore, offspring sex ratio was not biased towards the rarer sex of helpers present in the group or population (resource competition hypothesis). However, females with sex-biased helping produced similarly skewed offspring sex ratios. This among-female association may not be surprising, because helpers are previous seasons’ offspring. Thus, in addition to facultative responses to prevailing social conditions, we found evidence for persistent biases among females. This could potentially explain previous evidence for resource competition/enhancement that have typically been interpreted as facultative responses, highlighting the need for a within-female approach to better understand the adaptiveness of sex-ratio biases. Significance statement Under certain conditions, females may benefit from producing a biased offspring sex ratio, but evidence for such effects in vertebrates is weak and inconsistent. Here, using observations of the same females under different social conditions, we show that cooperatively breeding red-winged fairy-wrens facultatively biased offspring sex ratio towards sons when living in pairs, thereby ensuring the availability of a workforce to assist in raising future offspring. However, biased offspring sex ratio patterns may also be the result of consistent differences among females. Indeed, we also found evidence for such patterns and suggest that this could be an explanation for previous findings which are often interpreted as facultative responses.
 
Relationship between the number of Egyptian vulture immatures and number of adults censused in roosting sites (n = 5) throughout five wintering seasons (2014–2019). Black dots represent the raw data points. The shaded area represents the 95% confidence interval
Differences between migrant and resident birds in percentage of time spent daily in flapping flight (as a proxy of energy expenditure) among migrant and resident birds during non-winter (in yellow) and wintering (in light blue) seasons. Shaded areas represent 95% confidence intervals
Predicted values of the significant variables included in the best models of breeding. A The ratio between breeding years and tracking years for each migratory type throughout the study period. B Differences between migrant and resident birds on successful/Breeding years ratio. The bars represent 95% confidence intervals
Survival analysis results for different migratory behaviours and Age class (A), migratory behaviour (B) and Age class (C) by using cox regression method for GPS-tracked individuals (n = 33) during the study period. The plots show survival probability throughout one year (in days) since the first tracking day. Each step in the lines represents the death of an individual in each case. The shaded area represents 95% confidence interval
Article
Partial migration is one of the most widespread migratory strategies among taxa. Investigating the trade-off between environmental/social factors — fitness and energetic consequences — is essential to understand the coexistence of migratory and resident behaviours. Here, we compiled field monitoring data of wintering population size and telemetry data of 25 migrant and 14 resident Egyptian Vultures Neophron percnopterus to analyse how environmental and social factors modulate overwintering immature population size, compare energetic consequences between migratory and resident individuals across wintering and non-wintering seasons and evaluate fitness components (i.e. survival and reproduction) between the two migratory forms. We observed that social attraction may influence the number of overwintering immature individuals, which increased linearly with adult birds surveyed. Residents spent more energy but exhibited higher survival probabilities and lower breeding activity. On the contrary, migratory birds showed lower energy expenditure during winter but also lower survival and more breeding attempts. These results suggest that social attraction may modulate population dynamics and promote residency in immature birds. Resident individuals benefit from enhancing their survival at the expense of higher energy expenditure during winter. Migrant birds, on the contrary, may compensate for the higher costs in terms of survival by a reduction in the energy cost, which may benefit more frequent breeding. Our results offer new insights to understand how species benefit from one strategy or another and that the coexistence of both migratory forms is context-dependent. Significance statement Animal populations exhibiting partial migration are composed of migrant and resident individuals who share the same breeding areas but different overwintering quarters. Deciphering the causes and consequences that affect each migratory behaviour is essential to understand the balance and persistence of the two strategies. Here, we investigate the environmental and social factors affecting number of immatures during winter and evaluate both migratory strategies in terms of energy expenditure, reproduction and survival. We found that social attraction modulates wintering population size of immature individuals and that the residency is energetically more costly but beneficial in terms of survival but not for breeding. By contrast, migration lessens the energy costs, increases the breeding activity, but also reduces survival probability.
 
Article
Inadvertent social information (ISI) use, i.e., the exploitation of social cues including the presence and behaviour of others, has been predicted to mediate population-level processes even in the absence of cohesive grouping. However, we know little about how such effects may arise when the prey population lacks social structure beyond the spatiotemporal autocorrelation originating from the random movement of individuals. In this study, we built an individual-based model where predator avoidance behaviour could spread among randomly moving prey through the network of nearby observers. We qualitatively assessed how ISI use may affect prey population size when cue detection was associated with different probabilities and fitness costs, and characterised the structural properties of the emerging detection networks that would provide pathways for information spread in prey. We found that ISI use was among the most influential model parameters affecting prey abundance and increased equilibrium population sizes in most examined scenarios. Moreover, it could substantially contribute to population survival under high predation pressure, but this effect strongly depended on the level of predator detection ability. When prey exploited social cues in the presence of high predation risk, the observed detection networks consisted of a large number of connected components with small sizes and small ego networks; this resulted in efficient information spread among connected individuals in the detection networks. Our study provides hypothetical mechanisms about how temporary local densities may allow information diffusion about predation threats among conspecifics and facilitate population stability and persistence in non-grouping animals. Significance statement The exploitation of inadvertently produced social cues may not only modify individual behaviour but also fundamentally influence population dynamics and species interactions. Using an individual-based model, we investigated how the detection and spread of adaptive antipredator behaviour may cascade to changes in the demographic performance of randomly moving (i.e., non-grouping) prey. We found that social information use contributed to population stability and persistence by reducing predation-related per capita mortality and raising equilibrium population sizes when predator detection ability reached a sufficient level. We also showed that temporary detection networks had structural properties that allowed efficient information spread among prey under high predation pressure. Our work represents a general modelling approach that could be adapted to specific predator-prey systems and scrutinise how temporary local densities allow dynamic information diffusion about predation threats and facilitate population stability in non-grouping animals.
 
Effects of light conditions (control vs. artificial light at night, ALAN) and temperature conditions (control vs. simulated heat wave) during early adulthood on pre-mating traits in female Gryllus lineaticeps: a body mass, b reproductive investment, c food intake, d body mass conversion efficiency, and e ovary mass conversion efficiency. Sample sizes are included atop each column. Values are displayed as estimated marginal mean ± s.e.m. for a–c because initial body mass was included in analyses, and as mean ± s.e.m. for d and e See text for further details
Effects of light conditions (control vs. artificial light at night, ALAN) and temperature conditions (control vs. simulated heat wave) during early adulthood on mating success in Gryllus lineaticeps. Sample sizes are included atop each column. Values are displayed as estimated marginal mean ± s.e.m. because mating partner body mass was included as a covariate in the analysis. See text for further details
Effects of light conditions (control vs. artificial light at night, ALAN) and temperature conditions (control vs. simulated heat wave) during early adulthood on 24-h oviposition in Gryllus lineaticeps: a total number of eggs laid, and b oviposition specialization (coefficient of variation across three available oviposition sites). Sample sizes are included atop each column. Values are displayed as estimated marginal mean ± s.e.m. because maternal body mass was included as a covariate in analyses. See text for further details
Article
Animals are increasingly exposed to both artificial light at night (ALAN; a.k.a., ecological light pollution) and heat waves. Traditionally, the effects of ALAN and heat waves have been investigated in isolation, and results indicate mixed support for their costs to important decisions made at specific stages of reproduction (i.e., before, during, and after mating). Therefore, we used a factorial design to manipulate temperature and light conditions during adulthood in female variable field crickets (Gryllus lineaticeps) to determine (1) whether ALAN has stage-specific effects on reproductive decisions and (2) if ALAN effects on reproduction interact with a simulated heat wave. We found that ALAN simulating bright urban lighting promoted mating success, and a simulated heat wave resulted in even greater benefits to reproduction, including increased reproductive investment (ovary mass prior to mating), the efficiency by which food was converted into reproductive tissue, and reproductive output (number of eggs laid). Heat wave and ALAN did not modulate the effect of one another because we found no evidence of interactive (e.g., synergistic or antagonistic) effects of temperature and light treatments on any reproductive trait. Our study is the first to examine the combined effects of ALAN and heat waves across reproductive stages, and we found that these two increasingly common environmental factors may generally benefit reproduction in an insect. Significance statement Animals are increasingly exposed to artificial light at night (a.k.a., ecological light pollution) and heat waves, but the combined effects of these two potential stressors are unknown. Therefore, we manipulated temperature and light conditions during adulthood in female variable field crickets (Gryllus lineaticeps) to examine effects across three important reproductive stages—before, during, and after mating. We found that ALAN simulating bright urban lighting promoted mating success, and a simulated heat wave resulted in even greater benefits to reproduction, including increased reproductive investment (ovary mass prior to mating) and reproductive output (number of eggs laid after mating). Our results indicate that these two increasingly common environmental factors may generally benefit reproduction in an insect.
 
A Frequency and B temporal distribution of repeated conglobation tests conducted on 23 American giant millipedes (Narceus americanus). In B, successive tests made on a given individual are connected by a grey line, showing how different individuals were repeatedly sampled throughout the summer. Multiple individuals were caught and subsequently tested on each day such that many observations overlap in B (darker lines and dots indicate more individuals)
Among- and within-individual variation in A conglobation latency, B conglobation duration, and C chemical secretion of 12 American giant millipedes (Narceus americanus). In each panel, individuals are ordered on the x-axis according to their individual mean values, represented by solid black dots. Conglobation measurements are in seconds, log10-transformed. Repeatability ± SE estimates are also presented (see Table 2)
A–D Conglobation latency, E–H conglobation duration, and I–L chemical secretion as functions of test sequence, body length, air temperature, and time of day in 23 American giant millipedes (Narceus americanus). Conditional effects for conglobation latency and duration (in SD units) are from the bivariate model (allowing residual correlation), whereas effects for chemical secretion (modelled as a Bernoulli binary trait) are from the trivariate model (which does not allow residual correlations). Shaded regions and error bars represent 95% credible intervals at each fitted value. Solid black lines indicate significant effects. See Table 1 for effect size estimates
Conglobation duration as function of conglobation latency in 23 American giant millipedes (Narceus americanus). The among-individual correlation is displayed by the thick black line regressed through raw individual means (solid dots), whereas the within-individual correlation is displayed by the thin grey lines regressed through observations made on each individual separately (open grey circles)
Among-individual correlation between chemical secretion and A latency to conglobate and B duration of conglobation in 23 American giant millipedes (Narceus americanus). Individual estimates and their 95% credible intervals (CI) were extracted as best linear unbiased predictors from the trivariate mixed model. Axes are in standard deviation units from the population mean
Article
The trait compensation and cospecialization hypotheses make contrasting predictions on how boldness is co-adapted with antipredator defences. If trait compensation occurs, then bold individuals should be equipped with better antipredator defences to compensate for their increased risk exposure. By contrast, if trait co-specialization occurs, shy individuals should be equipped with better antipredator defences to enhance overall protection from predation. Here, we test the two alternative hypotheses by evaluating the among- and within-individual relationships between boldness and chemical defences in the American giant millipede (Narceus americanus; order Spirobolida). After controlling for test sequence, body length, air temperature, and time of day, latency to conglobate (i.e. “curl up”) upon disturbance and duration of conglobation were both found to be repeatable (R = 0.28 and 0.35). Moreover, the latency and duration of conglobation were negatively correlated at both the among- and within-individual levels (r = − 0.46 and − 0.32). Hence, individuals displayed consistent differences in risk-taking along a “shy-bold” axis. Millipedes also displayed—albeit weaker—individual differences in their probability to secrete chemical defences (R = 0.12), but no significant relationship was found with conglobation latency or duration. Overall, these results suggest that chemical defences evolved separately from the shy-bold axis (as measured with conglobation behaviour) as two independent antipredator strategies in millipedes. Significance statement Many species assume a defensive pose when threatened to protect themselves from predators, which makes them conducive to boldness measurements in a way that is directly relevant to antipredator strategies. The question arises as to whether boldness is co-adapted with other antipredator defences. Here, we demonstrate the existence of a shy-bold axis in American giant millipedes, which both conglobate into a defensive position and secrete a defensive fluid when threatened. We also found consistent individual differences in the propensity to secrete chemical defences, but with no relationship to boldness. While many studies have looked at the relationship between boldness and morphological defences (e.g. size of a protective shell), this is the first study to have partitioned the among- and within-individual correlations between boldness and chemical defences. Despite their importance as predator deterrents, chemical defences seem to have evolved independently from boldness in this species.
 
Seasonal variation in pairing in A. angulosus: percent shrimp collected in pairs. A Percent shrimp in pairs across collection dates (open circles = reproductive season, n = 42; filled circles = nonreproductive season, n = 14). Note that reproductive and nonreproductive seasons are operationally defined by the percentage of shrimp reproducing, and so the timing of these seasons may vary slightly between years. B Percent shrimp collected in pairs is greater in the reproductive than nonreproductive season
Assortative pairing by body size (A) and claw size (B) in the reproductive (open circles) and nonreproductive (filled circles) seasons. Dashed line = 1:1. Body sizes are highly correlated in both reproductive and nonreproductive seasons; the correlation is stronger in the reproductive season. Claw sizes are also highly correlated in both seasons, with no difference between seasons
Seasonal variation in within-pair relative body size (male size–female size). A Within-pair relative body size across months (mean ± SE; open circles = reproductive season, n = 42 collections; filled circles = nonreproductive season, n = 14 collections); B relative within-pair body size (male–female) is greater in nonreproductive season than in the reproductive season. In the reproductive season, within-pair size differences are less than 0 (males smaller than females); in the nonreproductive season, within-pair size differences are greater than or equal to 0. Box plot as in Fig. 1
Article
Size-assortative pairing is common across a wide range of taxa. In many cases, both sexes would benefit from pairing with a mate larger than themselves. As males and females cannot simultaneously be larger than their pair mate, size differences within pairs reflect which sex is able to obtain this benefit. Snapping shrimp can be found in pairs year-round, and both males and females would benefit from pairing with larger individuals. Larger females are more fecund; males, then, are likely to benefit from pairing with larger females primarily in the reproductive season. Larger individuals are more successful competitors and females benefit more from shared burrow defense than males; for females, then, benefits of pairing with larger males are likely to accrue year-round. In this study, we use field data to test whether within-pair size differences in snapping shrimp correspond more to male or female interests, and whether this outcome differs between seasons. We find that size-assortative pairing varies seasonally: although body sizes of paired males and females are highly correlated year-round, the within-pair size difference is greater during the reproductive season than the nonreproductive season. Furthermore, within pairs, females are larger than males during the reproductive season, while pairs are size-matched or male-biased during the nonreproductive season. These changes in within-pair size relationships suggest seasonal differences in which sex has greater control over pair formation, and highlight nonreproductive benefits associated with monogamous pairing. In addition, these results underscore the importance of considering temporal variation in studies of size-assortative pairing. Significance statement In many taxa, it is advantageous for both males and females to mate with larger individuals. As both sexes cannot simultaneously mate with larger individuals, size relationships within pairs reflect the outcome of this sexual conflict. In snapping shrimp, pairs cooperate in defending their burrows from invading conspecifics, and larger individuals are better competitors; larger females are also more fecund. Thus, males obtain a reproductive advantage from mating with larger females, while for females, mating with larger males provides social (territorial defense) benefits. Here, we find seasonal differences in within-pair size relationships, such that females are larger than males during the reproductive season, but pairs in the nonreproductive season are size-matched or male-biased. These results suggest seasonal variation in the outcome of conflict over body size within pairs, and highlights the need to consider temporal variation in size-assortative pairing.
 
Article
For human-audible vocalizations (below 20 kHz) of rodents, subterranean lifestyle results in low-frequency calls coupled with low-frequency hearing. For ultrasonic vocalizations (above 20 kHz), the effect of subterranean lifestyle on the acoustics is unknown. This study fills this gap of knowledge, by comparing vocalizations of two closely related species, the surface-dwelling Brandt’s vole Lasiopodomys brandtii (17 pups, 19 adults) and the subterranean mandarin vole L. mandarinus (15 pups, 16 adults). As predicted, the audible calls (AUDs) were substantially higher-frequency in L. brandtii than in L. mandarinus, in either pups or adults. In contrast to AUDs, the ultrasonic calls (USVs) did not differ in frequency variables between species, in either pups or adults. Interspecies differences were found in duration: AUDs were shorter in adult L. brandtii than in adult L. mandarinus, USVs were longer in pup L. brandtii than in pup L. mandarinus, and the low-frequency USVs of adult L. brandtii were longer than low-frequency USVs of adult L. mandarinus. We advance a hypothesis that shift towards higher-frequency AUDs in L. brandtii compared to L. mandarinus was triggered by the evolutionary emergence of the high-frequency audible alarm call, which is only present in L. brandtii but absent in L. mandarinus. We discuss that USVs may be resistant to these selection pressures as close-distant social signals. Significance statement Relationship between ecological specialization, such as subterranean or surface-dwelling lifestyle, and the acoustic traits of communicative signals in rodents evoke interest for over than 30 years. So far, the relationship between vocalization and subterranean life (low-frequency calls and low-frequency hearing) was only reported for calls produced by rodents in human-audible range of frequencies. No data was available for ecological adaptations of ultrasonic calls; moreover, even the existence of ultrasonic calls in subterranean rodents was unknown to recent time. Comparative studies of closely related subterranean and surface-dwelling rodent species might highlight the evolution of acoustic traits related to these ecological specializations.
 
Evolutionary fate of populations is subject to novel interactions with humans. Each species has a unique history of domestication, feralization, and gene flow. Despite this, broad characterizations can be made of the steps leading to human-adapted animals across a continuum: pests, managed game, domesticates, and HIREC-adapted wild animals. If populations fail both to produce appropriate plastic responses and adapt in response to selection, human-induced changes to the environment may lead to extinction or extirpation. Animals that survive or thrive under HIREC without human control over reproduction and feeding are considered HIREC-adapted wild animals. Despite the dichotomy shown in the figure, there is a continuum of human control over these activities ranging from loosely managed game populations and pests, through free-ranging domestics like backyard turkeys, to tightly controlled domestics like thoroughbred horses. Feral populations routinely arise from domestic ones and may subsequently face the same selection pressures as managed, pest, or wild lineages
Five of Diamond’s (2002) six criteria for domesticability (see the Domesticability and adaptation to HIREC section) are also useful for understanding what makes some wild species successful under HIREC. The sixth (not shown) is not relevant to discussion about wild animals and HIREC: social dominance hierarchies used to control groups. 1. Adapts to human-provided diet (a) Successful domesticates thrive on a wide variety of human-provided food. Cat eating a flour tortilla (photo credit: Amanda Beckman). (b) Under HIREC, many wild animals are expanding what is considered their “natural” diet to include resources provided directly or indirectly by humans. Leptonycteris spp. feeding at nectar feeder (photo credit: Simon Tye). 2. Fast growth rate and short birth spacing (a) An extreme of short birth spacing is observed in domestic poultry as evidenced by the high frequency of egg-laying outside the historic breeding season. Five chicks pictured behind metal bars. (b) Some non-cavity nesting birds are drawn to nest in human structures. Mourning dove (Zenaida macroura) sitting on a nest on top of a green box with a brick wall in the background (photo credit: Chris Jarvis). 3. Not threatening to humans (a) Secondary rounds of domestication are currently happening for several species to retain juvenile traits and be more suited for indoor life. A small breed of pig (Sus domesticus) standing indoors on a rug (photo credit: Vjeran Pavic). (b) Animals that humans are willing to feed in public are not considered to be dangerous or aggressive, and typically are not pest species. A grey squirrel (Sciurus carolinensis) places its paw in a human’s hand that contains food while looking at the person. 4. Breeds in human-altered environments (a) One extreme of breeding in human environments, dairy calves are quickly separated from their mother after birth in many cases. A black and white photo shows approximately five cattle per small, fenced pen, for dozens of pens. (b) While many wild birds will nest on human-created structures, getting wild birds to breed in captivity remains a major obstacle in ornithology research, though some researchers have recently had success. A fledgling dark-eyed junco (Junco hyemalis) with an orange band on its leg that was hatched from captive-reared parents in a research population is pictured in an enclosure made of wire mesh with branches, moss, and leaves on the ground (photo credit: Ketterson Lab & Sarah Wanamaker). 5. Tendency not to panic in enclosures (a) Donkeys (Equus asinus) and mules (Equus asinus × Equus caballus) still perform their duties as pack animals, the reason they were first domesticated, despite the changes to the landscape and infrastructure around them. A mule carrying several sacks on its back and wearing a halter crosses a bridge in front of a stone wall (photo credit: Gil Rosenthal). (b) An Italian wall lizard (Podarcis siculus), climbs up a brick wall that has crumbled in places to create small crevices. Many animals are drawn to anthropogenic structures because they mimic natural caverns. (photo credit: John Hutchinson)
Article
With nearly all life on earth experiencing direct or indirect effects of human activity, there is an urgent need to understand how organisms do or do not adapt to human-induced environmental change. Domestication was an early crash into the Anthropocene for some species, and the response of animal populations to domestication selection gives us insights on how plastic responses and evolutionary changes interact to determine the fate of wild vertebrates responding to a human-altered world. We consider intentional breeding, managed hunting, and extermination as part of a continuum of anthropogenic agents of ecological selection and highlight shared targets of selection between domestication and human-induced selection pressures more broadly. Many of the traits that predict successful domestication also predict adaptation of wild animals to human-dominated environments. Domestic animals are also a source for feral lineages and for genetic exchange with wild populations. Shared ecological constraints and gene flow thus contribute to convergent or congruent changes across a spectrum of responses to human influence. Evaluating domestication as another source of anthropogenic selection yields insights for conservation and a promising way to understand mechanisms of behavioral adaptation. Significance statement In this review, we draw insights for conservation from domestication—the oldest and most intense evolutionary interaction between animals and humans. Domestication is a special case of organisms successfully responding to an abrupt shift towards human-altered environments, and success in those environments depends on the same factors that make some animals easier to domesticate than others. Domestication has the potential to simultaneously inform us how behavior and genetics contribute to the process of human adaptation in animals and provide a window into the processes required for animals to become human-adjacent. Understanding how animals adapt in our presence yields clues as to how contemporary species react to decreasing habitat and increasing contact with humans.
 
Color morph differences in flight initiation distance FID (A), distance to nearest refuge DNR (B), and distance to chosen refuge DR (C). Boxes indicate the inter quantile range (IQR), with the central line depicting the median and the whiskers extending to 1.5*IQR. Different symbols indicate significant mean differences in log-transformed FID, DNR, and DR behaviors between groups (alpha < 0.05). Note that datapoints presented in the Fig. are the raw data and not log-transformed
Proportion of chosen refugia by color morph at each field site. At both Moni and Damarionas, orange morphs used vegetation as a refuge more often than white and yellow morphs. Asterisks indicate significant differences between morphs in their use of vegetation as a refuge (alpha < 0.05)
Article
Variation in color morph behavior is an important factor in the maintenance of color polymorphism. Alternative anti-predator behaviors are often associated with morphological traits such as coloration, possibly because predator-mediated viability selection favors certain combinations of anti-predator behavior and color. The Aegean wall lizard, Podarcis erhardii , is color polymorphic and populations can have up to three monochromatic morphs: orange, yellow, and white. We investigated whether escape behaviors differ among coexisting color morphs, and if morph behaviors are repeatable across different populations with the same predator species. Specifically, we assessed color morph flight initiation distance (FID), distance to the nearest refuge (DNR), and distance to chosen refuge (DR) in two populations of Aegean wall lizards from Naxos island. We also analyzed the type of refugia color morphs selected and their re-emergence behavior following a standardized approach. We found that orange morphs have different escape behaviors from white and yellow morphs, and these differences are consistent in both populations we sampled. Orange morphs have shorter FIDs, DNRs, and DRs; select different refuge types; and re-emerge less often after being approached compared to white and yellow morphs. Observed differences in color morph escape behaviors support the idea that morphs have evolved alternative behavioral strategies that may play a role in population-level morph maintenance and loss. Significance statement Color polymorphic species often differ in behaviors related to reproduction, but differences in other behaviors are relatively underexplored. In this study, we use an experimental approach in two natural populations of color populations of color polymorphic lizards to determine that color morphs have diverged in their escape behaviors. By conducting our experiments in two different populations with similar predator regimes, we show for the first time that behavioral differences among intra-specific color morphs are repeatable across populations, suggesting that alternative behavioral strategies have evolved in this species. Using this experimental approach, we demonstrate that the brightest orange morph stays closer to refuge than other morphs, uses a different refuge type (vegetation) more often than other morphs (wall crevices), and take much longer to emerge from refuge after a simulated predation event than other morphs. Thus, selective pressures from visual predators may differ between morphs and play a role in the evolution and maintenance of color polymorphisms in these types of systems. Our study species, Podarcis erhardii , belongs to a highly color polymorphic genus (19/23 spp. are color polymorphic) that contains the same three color morphs, thus we believe our results may be relevant to more than just P . erhardii .
 
a Percent reflectance relative to PFTE diffuse reflectance standard for blue and white (blue and gray lines respectively) stimuli and plywood background (brown line). b Location of blue and white stimuli in the color vision space of Bombus impatiens. c Diagram to scale of setup with bumblebee colonies connected via a clear plastic tube to plywood foraging arenas. d Experimental design for floral choice assay where bees were given experience with either blue or white flowers and then foraged in a mixed array of blue and white flowers where we recorded their behavior. The same nectar chemistry treatment was applied to all the flowers in the array. Bumblebee illustration by Damond Kyllo
Experimental design for the social behavior assay. Bees were given experience with either a blue or b white and then released to forage in an array of flowers of the color they had experience with half of which were occupied by pinned demonstrator (model) bees. The same nectar chemistry treatment was applied to all the flowers in the array
Bee experience with color interacts with nectar chemistry for behavior. a Chittka’s Index of floral constancy ranges from 1 (constant) to − 1 (inconstant) with 0 as random foraging. Blue bars are means and standard errors of bees with previous experience with blue, and gray bars are means and standard errors of bees with previous experience with white. Asterisks indicate significant (p < 0.05) differences from 0 (random foraging). Different letters indicate significant differences between treatments according to Tukey-corrected post hoc tests. b Jacobs’ Index of floral preference ranges from 1 (preference for white) to − 1 (preference for blue). Blue bars are means and standard errors of bees with previous experience with blue, and gray bars are means and standard errors of bees with previous experience with white. Asterisks indicate significant (p < 0.05) differences from 0 (no preference). Different letters indicate significant differences between treatments according to Tukey-corrected post hoc tests. c Proportion of visits made by bees to occupied flowers in each nectar chemistry and flower color treatment. Asterisks indicate significant (p < 0.05) differences from 0.5 (no preference), and the cross indicates a marginal difference (p = 0.051). Different letters indicate significant differences between treatments according to Tukey-corrected post hoc tests
Article
Caffeine and ethanol are naturally occurring compounds in floral nectar. We examined how these compounds influenced pollinator behaviors including floral preference, floral constancy, and social behavior using bumblebees, Bombus impatiens, which were given prior experience foraging on either human blue or human white (hereafter blue and white) artificial flowers. Because flower color influenced bee behavior, with strong preferences for blue, we focused on the interaction between nectar chemistry and flower color. Bees that had experience with blue flowers preferred blue regardless of nectar chemistry. In contrast, for bees that had prior experience with white flowers, only the control treatment preferred white, while bees exposed to caffeine and ethanol showed no preference. The effects of nectar compounds may therefore only occur when bees are already foraging on a less-preferred color. We also examined the impact of nectar chemistry on the social behavior of joining other bees at flowers. In the same treatments for which bees showed a preference for previously experienced flower colors (all of the blue treatments and only the white control), bees also preferentially visited unoccupied flowers. In the treatments where bees showed no color preference, however (the white caffeine and ethanol treatments), bees showed no preference for unoccupied flowers. We show that the impacts of field-realistic levels of caffeine and ethanol in nectar on pollinator behavior depend on flower color, highlighting that the potential costs and benefits of nectar chemistry to plants are likely to be dependent on bee behavioral biases for other floral traits. Significance statement Flower nectar often contains toxic compounds hypothesized to impact pollination, but little research has shown their effects on the behavioral decisions of free-flying bees. Caffeine and alcohol occur in the nectar of some flowers. We found that bee response to these nectar compounds depends on the flower color. Bees preferentially visited blue flowers regardless of nectar chemistry, but the presence of caffeine or alcohol reduced bee color preference when bees had experience foraging on white flowers. The bumblebee’s social behavior of joining other bees at flowers showed related effects; in treatments where bees showed a preference for flower type, they also preferred to forage alone. This research highlights that bees make decisions based on the interaction between multimodal cues including nectar chemistry, and therefore the strength of selection on nectar chemistry is dependent on bee behavioral biases for other floral traits.
 
The relationship of aggression scores (A) and song rates (B) with habitat and noise treatment. The boxes indicate interquartile ranges, the middle line indicates median, and the whiskers indicate 95% confidence intervals. Dots connected by dotted lines represent data from individual subjects
Proportion of first trials where the resident male used visual signals, grouped by habitat and noise treatment. The numbers at the bottom of each bar indicate the total number of subjects for each combination
Article
Anthropogenic noise may disrupt signals used to mediate aggressive interactions, leading to more physical aggression between opponents. One solution to this problem is to switch signaling effort to a less noisy modality (e.g., the visual modality). In the present study, we investigate aggressive behaviors and signaling in urban and rural male European robins (Erithacus rubecula) in response to simulated intrusions with or without experimental noise. First, we predicted that urban birds, living in noisier habitats, would be generally more aggressive than rural birds. We also predicted that during simulated intrusions with experimental noise, robins would increase their physical aggression and show a multi-modal shift, i.e., respond with more visual threat displays and sing fewer songs. Finally, we expected the multi-modal shift in response to noise to be stronger in urban birds compared to rural birds. The results showed that urban birds were more aggressive than rural robins, but an increase in aggression with experimental noise was seen only in the rural birds. Urban but not rural birds decreased their song rate in response to noise. Contrary to the multi-modal shift hypothesis, however, there was no evidence of a concurrent increase in visual signals. These results point to a complex role of immediate plasticity and longer-term processes in affecting communication during aggressive interactions under anthropogenic noise. Significance statement Human activity has an enormous effect on wildlife, including on their social behavior. Animals living in urban areas often tend to be more aggressive than those living in rural areas, which may be due to urban acoustic noise making communication between individuals more difficult. In a study with a common songbird, the European robin, we investigated the role of urban acoustic noise in aggression and territorial communication. Urban robins were more aggressive than rural robins, and additional noise in the territory increased aggression in rural but not urban robins. While urban robins decreased their singing effort with additional noise, they did not increase visual signals concurrently. These results suggest that noise can indeed make animals behave more aggressively although the effect may depend on how noisy it is already. These results further our understanding of how human-made noise changes animal communication and social behavior.
 
(a) Diagram of the experimental design and (b) apparatus used for the behavioural testing
Variation in (a) latency to emerge from the refuge zone and (b) proportion of time spent in the refuge zone in relation to the composition of the shoal. In the boxplots, edges represent the upper and lower quartiles, internal lines represent the median, whiskers represent maximum and minimum, and points represent outliers
Shoal cohesion in relation to the composition of the shoal. Increasing values of the indexes indicated increasing shoal cohesion. In the boxplots, edges represent the upper and lower quartiles, internal lines represent the median, whiskers represent maximum and minimum, and points represent outliers
Article
Research on several social fishes has revealed that shoals constituted by familiar individuals behave remarkably differently compared to shoals formed by unfamiliar individuals. However, whether these behavioural changes may arise also in shoals composed by a mixture of familiar and unfamiliar individuals, a situation that may commonly occur in nature, is not clear. Here, we observed the behaviour of Mediterranean killifish ( Aphanius fasciatus ) shoals that were composed by both familiar and unfamiliar individuals (i.e. individuals were familiar to each other in pairs) and compared it with shoals entirely made by either unfamiliar or familiar individuals. Shoals formed by familiar individuals took longer to emerge from a refuge and swam more cohesively compared to shoals formed by unfamiliar fish. Shoals formed by a mixture of familiar and unfamiliar individuals behaved as shoals formed by unfamiliar individuals. Moreover, mixed shoals did not segregate in pairs according to their familiarity. This study suggests that mixed shoals do not show the behavioural effects of familiarity. Significance statement Laboratory studies have compared the behaviour of shoals formed by familiar fish versus shoals formed by unfamiliar fish, finding notable advantages in the former ones, such as improved antipredator and foraging behaviour. However, comparing these two opposite shoal types may not provide information on the natural situation, because in nature, shoals often change composition. We investigated how shoals formed by a mixture of familiar and unfamiliar fish behaved. We analysed shoals’ preference for open environment versus covers and shoals’ swimming cohesion. Results showed that shoals formed by both familiar and unfamiliar individuals mostly behave like shoals entirely formed by unfamiliar individuals. This suggests that the advantages of social groups formed by familiar fish might be hardly seen in nature for species in which shoal composition changes frequently.
 
Mating and reproduction along social status and relative 1 status between couples. Age at first marriage was plotted using all cases while the mating as well as the reproductive outcome was plotted using only cases with age ≥ 40. The upper panels indicate that higher status men are less likely to be unmarried, going through marriage disruption or childless while the patterns are the opposite for women. For the lower three panels, decile 1 would indicate the respondent had an extremely lower status compared with their partner while decile 10 extremely higher status compared with their partner. Deciles 5–6 would indicate homogamy in terms of education level. Men who are relatively higher status compared with their spouse married at a younger age and had younger wives. The patterns are the opposite for women. Both hypergamy and homogamy are effective reproductive strategies
Article
Evolutionary psychological theories posit that higher social status is conducive to men’s reproductive success. Extant research from historical records, small scale societies, as well as industrialized societies, support this hypothesis. However, the relationship between status difference between spouses and reproductive success has been investigated less. Moreover, even fewer studies have directly compared the effect of status and status difference between spouses on reproductive success in men and women. Using data from the Chinese General Social Survey (CGSS) conducted between 2010 and 2017 ( N = 55,875; 28,931 women) and operationalizing social status as standardized income and educational level (compared with same-sex peers), we examined how social status and relative status between spouses impact men’s and women’s mating and reproductive success. We found that (1) men with higher social status were more likely to have long-term mating (being in a marriage and/or not going through marriage disruption) and reproductive success, mainly through having a lower risk of childlessness; (2) women with higher social status were less likely to have mating and reproductive success; and (3) relative status between spouses had an impact on the couple’s reproductive success so that couples, where the husband had higher status compared to the wife, had higher reproductive success. Thus, social status positively impacted men’s reproductive success, but relative status between spouses also affected mating and impacted childbearing decisions. Significance statement In terms of standardized educational level and income among peers, social status positively predicts men’s mating and reproductive success in contemporary China. However, while a higher social status increases the probability of having at least one child, it does not predict a greater number of children for men. A status difference between spouses, on the other hand, consistently predicts having children. Thus, the higher the husband’s status relative to his wife, the greater the likelihood of having the first, second, and third children. The current results suggest that when examining the effect of status on mating and reproduction, social status and status within a family should be considered. We also stress the importance of exploring the potential proximate mechanisms by which a status difference influences childbearing decisions.
 
Effect of male and female age at first reproduction on the number of offspring produced by Euoniticellus intermedius dung beetles. Bars represent means and 95% CI
a Linear and b quadratic effects of female survival on the number of emerged offspring in Euoniticellus intermedius females mated young and mature
Effect of age at first reproduction on a male and b female survival, depending on self and mate’s age in Euoniticellus intermedius dung beetles. A dotted line is shown at day 30, when mature individuals were first mated
a Effect of parental mating age on male offspring body size (mean ± 95% CI). b Trade-off between offspring number and female body size in Euoniticellus intermedius dung beetles
Article
Mating young can cause early death due to resulting energetic depletion, physical damage, or sexually transmitted disease, whereas waiting too long to mate has the risks of suffering reproductive senescence or death before finding a mate. The ideal age for reproducing also depends on the mate’s age, as young partners may be more aggressive or less fertile and experienced than mature partners. Therefore, longevity and lifetime reproductive success depend on the combination rather than the individual effects of self- and the mate’s mating age, but this idea has not been formally explored. Here I evaluated lifetime reproductive success and longevity in males and females mated at different ages (i.e., young or mature) with mates of the same or a different age. As a study system, I used the horned dung beetle Euoniticellus intermedius, a classic study subject with intense sexual selection for male horn size, which is a reliable indicator of male strength and condition. For both males and females, mating young severely reduced lifespan, independent of the mate’s age, body, or male horn size. Due to reduced survival, females, but not males, had fewer offspring, with a stronger fitness effect suffered by mature than by young females. Regarding reproductive success, mature males and females had 3.4 and 1.6 times more offspring, respectively, when mated with mature than when mated with young partners, independently of their own body and horn sizes. Reproductive success of young males or females was not sensitive to the mate’s age. These results indicate that the optimal onset of reproduction and the ideal reproductive investment are highly dependent on the combination of self- and the mate’s age. Significance statement A very important decision in life is when to mate for the first time. Whereas mating too young can be risky or suboptimal, waiting too long increases the chance of dying before finding a mate. Here I show that in dung beetles, it can be equally important to choose the correct mate’s age in order to maximize lifetime reproduction. The most dramatic decision is for individuals (mainly males) that take a long time to mate, whose fitness get reduced by up to three times when mated with young rather than mature couples. This idea had never been tested in animals, and dung beetles showed that a combination of self- and the mate’s age will be determinant of how much progeny can animals have and how deadly it can be to take maladaptive decisions.
 
A–H The prevalence of polyandry (PA) in amphibian and reptile breeding populations across taxonomic groups and maps of sampling locations (excludes cases with fewer samples than five). Jittered points in graphs are the PA for individual cases within each taxonomic group, with values summarised above as a box plot (central lines in boxes are median values, numbers are the number of cases, boxes correspond to the first and third quartiles and whiskers extend to 1.5 times of the inter-quartile range). Sampling locations are plotted in maps, with the bubble size reflecting the degree of PA and colour corresponding to the colour used in the associated graph. Single-case taxonomic groups (excluded from summary graphs) are plotted on the map with a black bubble and numbered: (1) Gymnophiona (Boulengerula taitanus), (2) Rhynchocephalia (Sphenodon punctatus), (3) Centrolenidae (Hyalinobatrachium valerioi), (4) Dendrobatidae (Ranitomeya imitator), (5) Leptodactylidae (Thoropa taophora), (6) Megophryidae (Leptobrachium boringii), (7) Phrynosomatidae (Uta stansburiana), (8) Crotaphytidae (Crotaphytus collaris), (9) Chamaeleonidae (Bradypodion pumilum), (10) Diplodactylidae (Oedura reticulata), (11) Pythonidae (Liasis fuscus), (12) Chelidae (Elseya albagula) and (13) Cheloniidae (Natator depressus)
Forest plot of effect sizes, and summary effect sizes estimated by phylogenetically controlled meta-analysis (random-effects maximum likelihood method) of the relationship between the number of offspring and the number of sires. The star indicates the outlying influential case (see text). Within taxonomic subgroups, cases are organised by the effect size (Zr) and labelled with the reference of the study. Point sizes are proportional to the precision of the estimates, and whiskers, 95% confidence intervals (CI). An effect size is considered significantly different from zero if its 95% confidence interval is either larger than or smaller than zero. Positive values indicate that there are larger numbers of offspring in groups of siblings and half-siblings with more sires, whereas negative values indicate the opposite. ‘PA %’ is the estimated prevalence of polyandry in the population with sample size ‘N’. The black diamond polygon below each subgroup is the estimated summary effect size including the 95% confidence interval, labelled by the taxonomic name of the subgroup. The grey diamond polygon is the summary effect size excluding the outlying influential case. Summary effect sizes for the whole dataset are represented by diamond polygons at the bottom of the graph. The black polygon represents the estimate for all cases (36 cases, labelled ‘Full dataset’), the grey polygon represents the estimate for cases without the outlier (35 cases, labelled ‘Without outlier’) and the white polygon represents the estimate based on a mixed-effects model that included average expected heterozygosity as a moderator (27 cases, labelled ‘With moderator’). The latter excluded the outlying influential case, and cases that were missing data for average expected heterozygosity (see also Fig. 3)
Forest plot of a cumulative meta-analysis for relationships between the number of offspring and the number of sires, cumulated according to the average expected heterozygosity estimated for the population. Points are cumulative effect sizes (Zr) with 95% confidence intervals (CI) and labelled with the reference of the study (see Fig. 2 for species names). The data for each study is cumulated progressing from top to bottom (each addition symbolized with ‘ + ’). The plot excludes cases that lack data for average expected heterozygosity. Diamond polygons at the bottom show summary effect sizes including the 95% confidence interval that are predicted for various values of average expected heterozygosity (minimum, mean and maximum of the dataset), for a mixed-effects model fitted with average expected heterozygosity specified as the moderator. This model also controlled for time-lag bias and small study effect and included random factors. The predicted effect size based on the mean value of average expected heterozygosity is also displayed as a white polygon in Fig. 2. Stars mark cases that, when left out of the dataset, result in non-significant results in tests of average expected heterozygosity as a moderator
Article
In general, males mate with multiple females to increase individual reproductive success. Whether or not, and under what circumstances, females benefit from multiple mating has been less clear. Our review of 154 studies covering 184 populations of amphibians and reptiles showed that polyandry was widespread and variable among and within taxonomic groups. We investigated whether amphibian and reptile females had greater reproductive output as the number of sires for offspring increased. Meta-analysis revealed significant heterogeneity in the dataset of all taxa. Expected heterozygosity was a significant moderator (covariate) of positive relationships between female reproductive output and the number of sires, but a sensitivity test showed the result was tenuous. Significant heterogeneity remained despite controlling for expected heterozygosity and other variables but was resolved for most taxonomic groups with subgroup meta-analyses. Subgroup meta-analyses showed that only female salamanders (Caudata) had significantly greater reproductive output with an increased number of sires. For many species of Caudata, males cannot coerce females into accepting spermatophores. We therefore suggest that if females control the number of matings, they can use polyandry to increase their fitness. Caudata offers ideal models with which to test this hypothesis and to explore factors enabling and maintaining the evolution of female choice. Outstanding problems may be addressed by expanding taxonomic coverage and data collection and improving data reporting. Significance Statement Many factors and combinations of factors drive polyandry. Whether or not females benefit from mating with more than one male remains equivocal. Focusing on amphibians and reptiles, our analyses demonstrate that female salamanders produced more offspring when mated with multiple males, whereas this was not the case for reptiles. Unlike many other species in our dataset, the polyandrous female salamanders fully control sperm intake and have chosen to mate multiple times. We further highlight problems and key directions for future research in the field.
 
a Display arena of spotted bowerbird with pile of sun-bleached snail shells in the foreground and avenue-shaped bower in the background. Males arrange various decorations within the avenue walls and at the bower entrances. b A visitor positioning itself parallel to the bower walls while watching a displaying male. c Schematic depiction of a typical display sequence. Display bouts are defined here as courtship sequences separated by less than 10 s (top). We differentiate between different display segments depending on the position of the receiver during a display bout (middle). See text for definitions. During a display bout, males perform a repertoire of up to 19 stereotyped display elements (Supplementary Table S1) separated by intervals of variable length (bottom)
Six visual display elements exhibited by male spotted bowerbirds during courtship. a Leap. b Crest presentation. c Wing flick, in the two-wings variant (left) and single-wing variant (right). d Rising. e Nodding. f ‘Wings drooping’ strut. Other visual display elements are depicted in Warham (1962) and Frith and Frith (2004)
Comparisons between males with different ownership status (white = subordinate males; grey = bower owners) and in different display segments. a Comparison between the proportions of peripheral, central static and central dynamic display elements calculate for each male in different display segments; N = 66 observation, 22 birds. b Comparison between the durations of intervals calculated for each male in different display segments; N = 27,705 observations, 22 birds. c Comparison between proportions of display elements performed with a decoration held in the beak by each male; N = 138 observations, 22 birds. Box plots show median (black horizontal line), 25% and 75% quartiles, upper and lower values within 1.5 inter-quartile range (whiskers), and extreme values above 1.5 inter-quartile range (outliers); stars on top of horizontal bars depict significance levels: ***p < 0.001)
Proportions of attendance of bower owners, subordinate males and unbanded birds as a function of date. Proportions of attendance are total proportions of time per total video recording time per bower, calculated for each category of bird per day. Data are shown separately for 2018 and 2019. Regression lines are shown with 95% confidence intervals (grey shading). N = 3120 observations, 1226 days-bower
Effect of subordinate attendance on number of marauding events (left; N = 28 bowers-year) and on the number of copulations per bower (right; N = 14 bowers-year). Red lines depict the fitted model and grey areas depict 95% confidence intervals. Camera recording time is controlled for in both models by including this variable as an offset term (see ‘Methods’)
Article
Despite strong selective pressures inherent in competition for mates, in species with non-resource-based mating systems males commonly engage in non-agonistic interactions with same-sex visitors at display arenas. Bowerbirds perform courtship dances on elaborate display structures — known as bowers — that are built and defended by one resident male. Several reports have suggested that bower owners tolerate the presence of specific male visitors at their display arenas, referred to here as ‘subordinates’. Subordinate males may learn the skills required for successful sexual signalling via prolonged social interactions at adults’ arenas, but little is known about whether courtship proficiency changes with experience and/or whether subordinates actively contribute to enhancing the resident male’s mating success. In this study, we investigated male-male associations in wild spotted bowerbirds (Ptilonorhynchus maculatus). We first sought to determine whether courtship behaviour differs based on bower ownership status. We then examined whether social interactions between bower owners and subordinate males may qualify as courtship coalitions. Our analysis of courtship postural components did not reveal differences in timing or relative occurrence of postural components between subordinate males and bower owners, whereas we found evidence that male-male associations in spotted bowerbirds may provide an example of rudimentary courtship coalitions. In particular, higher subordinate attendance is associated with lower destruction rates by neighbouring rivals and with overall higher mating success, and male pairs are stable in subsequent years. This study provides novel information about social dynamics among male bowerbirds, and further insights into the evolution of coalitionary behaviour in male displays. Significance statement Same-sex associations between established males and subordinate visitors on display arenas are common in birds, yet poorly understood. Using video recordings from a population of wild spotted bowerbirds, Ptilonorhynchus maculatus, we performed a quantitative analysis on motor courtship components across males, and on their social interactions on display arenas to investigate the nature of male–male partnerships. Our results showed that motor courtship performance in subordinate visitors is not suggestive of an early ontogenetic stage, as previously speculated. Moreover, though bower ‘owners’ and subordinate males do not coordinate their behaviour during courtship or bower building, male–male partnerships may qualify as a rudimentary or incipient form of courtship coalitions. Subordinate males are tolerated at bowers, the magnitude of subordinate attendance correlates with owner males’ mating success, and repeated interactions between individuals reveal consistent partner associations.
 
A peek under the pillbug bonnet: photographs of two representative individuals showing genital features. Left is a female and right a male. Photos credit to PAB
Predicted latency to emerge for 100 individual pillbugs measured a repeatedly over time and b across unexposed and exposed (bare half of tank) contexts. Each black line represents the model predicted individual trendline (reaction norm); the red lines indicate the mean level temporal and contextual trendline, respectively
Raw data plots illustrating the longitudinal sampling of behaviour. Shown are four individual pillbugs with mean latencies that span some of the shortest (bold) and longest (shy) latencies observed. Note the two samples taken each day, 4 days per week, across a total of 3 weeks (where each 4 days per ‘week’ is referred to as a burst of sampling). Data are plotted on a log10 scale, which is the transformation used in our analyses
Among-individual relationships between latency to unroll and a mean mass and b short-term growth in mass. Dots represent model predicted mean values and error bars the SE of those estimates
Article
In recent years, many studies have investigated the potential state dependence of individual differences in behaviour, with the aim to understand the proximate and ultimate causes and consequences of animal personality. Among the potential state variables that could affect behavioural expression is size and mass, but few studies have found associations at the among-individual levels. Insufficient sampling and incorrect analysis of data are cited as impediments to detecting correlations, if they exist. Here, we conducted a study using 100 pillbugs (Armadillidium vulgare) and assayed their defensive behaviour 24 times each over time and across familiarity contexts, to test the asset protection hypothesis that predicts a negative correlation between boldness and mass, and with increases in mass over time. Multivariate mixed models revealed that despite mostly consistent individual behavioural differences over time (modest slope variance) and across contexts (near-parallel reaction norms), and 18-fold range in starting mass, there was no correlation between individual mean mass and boldness. However, individuals that gained more mass over time may have been more ‘shy’ compared to those gaining less mass, but the correlation was weak and observed variation in mass gain was small. There was also a mean level trend of increasing shyness over time that was coincident with mean level mass increases over time. Together, our study provides weak evidence for the asset protection hypothesis, whereby individuals that accumulate more resources are thought to protect them through risk averse behaviour. Significance statement Individual variation in ‘state’, such as mass or energy reserves, is thought to be a predictor of individual differences in behaviour that are consistent over time. However, few studies reveal such links, and several studies suggest insufficient sampling may explain null results in most studies. We studied 100 animals sampled 24 times each in a controlled setting to reveal stable individual differences in mean behaviour over time and across contexts; however, individual behaviour was unrelated to large differences in individual mass but weakly related to increases in mass through time whereby individuals became more shy and those growing faster were somewhat more shy. Our results provide little evidence for the asset protection hypothesis.
 
Picture of the territorial defense trial, presenting the speaker and a male on top of the perimeter
Schematic (a) and picture (b) of the Novel Environment Test. The cooler box measured 50 × 25 × 29 cm, with a 10 cm PVC tube attached on one side of the box. A sliding door separated the shelter from the box. Two LED tubes and a Hero Black 5 Go pro camera were attached to the lid of the box. Three solid PVC tubes (10 cm height, 5 cm diameter) were placed inside the box as visual obstacles at randomized positions every day. A grid was drawn on the floor of the cooler box to help randomize the position of the obstacles. A mesh net was placed in the cooler box at 20 cm height to prevent the frog from jumping on a wall outside of the camera range
Path diagrams of the best structure equation models (SEMs) (based on difference in Akaike’s information criterion (AIC) values) explaining the covariance structure among four behaviors assessed during an aggressivity test (a), and five behaviors assessed during a Novel Environment Test (b). “HBO” refers to the latency until the first head-body orientation. Squares represent the variances of the different behaviors explained by the SEM structure (R²). Numbers associated with arrows are standardized factor loadings which represent how behavioral responses are predicted to change based on changes to the latent variable. Number in brackets represent variances of residuals or error variances (e) associated to each behavior. All simulated models can be found in the Supplementary material (Supplementary Fig. 1, 2)
Range of variation in the three behaviors that best represented the latent variables of aggression, exploration and boldness. The latency until the first jump (a), the time spent in the shelter (b), and the distance travelled in the Novel Environment Test (c) are presented for individual males. All variables have been transformed using a log (a) or constant (b and c) transformation. Boxes indicate the inter quartile range, with the central line depicting the median and the whiskers extending to 1.5*IQR. Dots represent the results of each trial. Males are ordered by their median (represented as a horizontal bold line)
Maps showing the spatial distribution of individual performance of male frogs on the island in the behavioral essays. The maps use the Voronoi territories of 7 March 2019 when the most individuals were present at the same time on the island. The maps show the mean value, calculated over all respective trials of (a) the individuals’ latency to jump in the territorial defense trial, (b) the time spent in the shelter during the Novel Environment Test (NET), and (c) the distance travelled in the NET. All color ramps have 20 equal intervals across the full range of the respective value; darker colors represent shorter latency in (a), shorter time spent in the shelter in (b), and longer distances in (c). Black squares indicate the 14 artificial pools that were in place on the island since 2018; thin gray lines show 50 cm elevation isoclines; the blue area shows the river Arataye. The territories of two males that were not tested in the behavioral assays are shown with a hatched white pattern
Article
An animal’s behavioral phenotype comprises several traits, which are hierarchically structured in functional units. This is manifested in measured behaviors often being correlated, partly reflecting the need of a coordinated functional response. Unfortunately, we still have limited understanding whether consistent differences in animal behaviors are due to underlying physiological constraints or a result of plastic adaptation to their current environment. Therefore, characterizing the spatial distribution of behaviors can provide important insights into causes and consequences of behavioral variation. In the present study, we quantified behaviors in a wild, free-ranging population of the Neotropical frog Allobates femoralis . We investigated how these behaviors were linked to the frogs’ natural and social environment and quantified the extent to which these behaviors consistently differed among individuals (i.e., animal personality). We assessed levels of aggressiveness, exploration, and boldness by measuring several underlying behaviors expressed in a set of experimental assays, and found evidence for consistent among-individual differences along these axes. Contrary to our expectation, there was no relationship between individual behaviors and their natural environment, but we found a plastic response of males to changes in female density, which might reflect how individuals cope with their socio-ecological environment. Significance statement How are behavioral phenotypes distributed across space? Here, we studied an entire free-ranging population of poison frogs, and investigated if the personality traits aggressiveness, exploration, and boldness are linked to the frogs’ natural or social environment. We found that behavioral traits were non-randomly distributed across the population, suggesting that the spatial arrangement of behavioral traits reflects how individuals cope with their complex natural and social environment.
 
Phylogenetic distribution of parental cooperation in (a) pre-hatching care and (b) post-hatching care (Bayesian maximum credibility tree of 100 phylogenies using 1065 and 991 bird species, respectively). Red = egalitarian biparental care, yellow = uniparental care. (c) The relationship between pre-hatching and post-hatching parental cooperation in five speciose of birds. Each line connecting the degrees of pre- and post-hatching cooperation represents one species. For each avian family, the black points represent the mean levels of pre- and post-hatching parental cooperation. The phylogenetic tree was plotted in R (3.4.2) using the “phytools” package (Revell 2012)
Association of parental cooperation before and after hatching with (a) coloniality and (b) chick development mode. The rectangle of the small box plots inside the violin plots represents the two central quartiles; the horizontal line indicates the median level of parental cooperation, and the far ends of the upper and lower whiskers show the highest and lowest levels of parental cooperation, respectively. The kernel density plot of each violin plot shows the distribution of parental care and its probability density. The extent of parental cooperation is centered at the mean (see Methods), and the number of species n is shown for each plot
Article
In animals, species differ remarkably in parental care strategies. For instance, male-only care is prevalent in teleost fishes, while biparental care predominates in birds and female-only care is widespread in mammals. Understanding the origin and maintenance of diversified parental care systems is a key challenge in evolutionary ecology. It has been suggested that ecological factors and life-history traits play important roles in the evolution of parental care, but the generality of these predictions has not been investigated across a broad range of taxa. Using phylogenetic comparative analyses and detailed parental care data from 1101 avian species that represent 119 families of 26 orders, here we investigate whether parental strategies are associated with ecological variables (i.e., food type, nest structure, and coloniality) and life-history characteristics (i.e., chick development mode and body size). We show that parental care strategies are in relation to coloniality (solitary, semi-colonial, colonial) and chick development mode (altricial vs. precocial). Colonial and altricial species provide more biparental care than solitary and precocial species, respectively. In contrast, food type (plant, invertebrate, vertebrate), nest structure (open vs. closed), and body size do not covary systematically with parental care patterns in birds. Taken together, our results suggest that living in groups and/or having high-demand offspring are strongly associated with biparental care. Towards the end, we discuss future research directions for the study of parental care evolution. Significance statement Animal species differ remarkably in the amount of care parents provide to their offspring and in the distribution of care tasks over the parents. In birds, for example, the young of some species are quite independent from the start, while the young of other species are helpless after hatching, requiring a lot of care. Moreover, either the female or the male does most of the caring in some species, while the parental tasks are shared equally in still other species. To understand the diversified parental care patterns, we applied advanced comparative methods to a large data set comprising over 1000 bird species. The analysis reveals that the parents tend to share their care duties equally when they live in groups and/or have offspring that are born helpless, and that parental care patterns are not associated with diet, nest type or body size. Hence, living in groups and having high-demand offspring seem to play important roles in the evolution of parental care.
 
Map of the seven field sites in Sabah, Malaysia, from which gibbon duet recordings were collected. The map was made using ArcGIS (ESRI) v. 10.5.1 (www.esri.com)
Representative spectrograms of a portion of the North gray gibbon (Hylobates funereus) duet. The male coda follows the female great call. The three features used in this study—coda timing, coda duration, and great call duration—are shown
Boxplots of the two acoustic features estimated from spectrograms of male gibbon codas—coda timing relative to the female (seconds) and coda duration (seconds)—by individual male. Color denotes the site at which the gibbon pair was recorded. The central line represents the median while the box represents the interquartile range (25% and 75% quartiles are the min and max of each box), and the bars represent values within 1.5 times the interquartile range. Dots represent values greater than 1.5 times the interquartile range
Posterior densities of intra-class correlation coefficients for coda duration and coda timing for 777 codas from 50 adult North Gray gibbon pairs (Hylobates funereus). The y-axis represents density and is not labeled because densities are only comparable within each parameter and relative densities between each level (inter-site, inter-pair, and inter-observation) are important
Scatterplots showing the relationship between female great call duration and male coda timing (A), female great call duration and male coda timing coefficient of variation (B), female great call duration and male coda duration (C), and female great call duration and male coda duration coefficient of variation (D). For plots A and C, each point represents the female great call and subsequent male coda. For plots B and D, each point represents the coefficient of variation of all female great calls and male codas from a duetting pair (N = 50 pairs). The points are colored by the site where they were recorded
Article
Social animals use complex communication to maintain social bonds. For pair-bonded animals in particular, acoustic communication is vital to reinforcing bonds and coordinating various behaviors within the bonded pair. Pair consistency in duets can be influenced by the time since pairing and may serve multiple functions; two of note are pair-bond reinforcement and advertisement of the relationship to conspecifics. Here, we assess the potential for pair consistency and plasticity in timing of vocalizations in 50 wild Northern gray gibbons (Hylobates funereus) from seven sites in Sabah, Malaysia. Specifically, we looked at the timing of the female gibbon’s great call and the subsequent male coda, the male duet contribution that follows the female great call (coda timing), and the duration of the male coda (coda duration). We found that for coda timing, pair-level variance was the most important source of variance, as opposed to intra-individual or inter-site variance. In contrast, for coda duration, individual-level variance was the most important source of variance. We also found that variability in the duration of female calls was not correlated with the timing or duration of male codas. Our results are consistent with previous work showing pair consistency in other paired, duetting species and contribute to the growing body of literature indicating that primate vocalizations—rather than being inflexible and innate—have a high degree of plasticity. Future work should aim to understand both how gibbons coordinate their duets and what impact this coordination may have on quality of the pair’s bond. Significance statement Duetting is seen across a diverse range of taxa, but in only a few nonhuman primates including indris, tarsiers, titi monkeys, and gibbons. Duetting in primates co-occurs with a suite of behavioral traits that include territoriality and pair bonding. Although the functions of primate duets remain a topic of debate, it is clear that duets provide information to neighboring conspecifics about the calling animal(s). Our results indicate that gibbon duets may contain information about pair identity. Investigating how duration of the pair bond influences either pair-level signatures or consistency of male timing will be an important next step in understanding the proximate influences that shape gibbon duet structure.
 
a Timeline of the playback experimental design. We broadcast the neighbour stimulus (‘NS’) for 5 min per trial (number in each box corresponds to the trial number), for a total of three trials per day with approximately 1 h between trials. This procedure was repeated for three consecutive days. On the third day, immediately following the final neighbour playback (NS 9), we broadcast a different song from a different location (‘SS’: stranger stimulus, a test of stimulus specificity, in other words that males that had reduced their response to the neighbour retain the capability of an aggressive response towards strangers). In 2017, the entire procedure was repeated with different stimuli after a period of 10 days to test the repeatability of dear enemy behaviour. (b) Exemplar playback stimulus. The spectrogram shows a single great tit song that was used to build one of the playback stimuli. (c) A second exemplar stimulus, taken from a different bird, illustrating the acoustic variation in great tit songs. An example playback experiment could use the song in (b) for the neighbour stimulus and that in (c) for the stranger stimulus. Note that the spectrograms do not illustrate the equalization of playback amplitude that was used for the trials
Response across trials. a The proportion (± SE) of individuals (N = 51 for all trials except N = 50 for N1; see ‘Methods’) that responded by either singing or approaching the playback speaker in each of the nine neighbour playback trials (labelled N1–N9) and on the stranger playback trial. Colours correspond to the day that the playback was performed (red = day 1, green = day 2, blue = day 3). b The closest approach, in categories of 10 m (note that in the statistical analyses we used categories of 5 m, but for ease of visualization we use broader categories here). None corresponds to trials in which the bird did not move at all towards the playback speaker. c The number of songs produced by males during the playback trial. Dots represent an individual’s response to that trial (points have been jittered along the x-axis and rendered partially transparent for ease of interpretation). Horizontal lines represent mean values
Relationship between whether the individual met the standard criterion (see ‘Methods’) for exhibiting the dear enemy effect (‘dear enemy’) or not (‘no dear enemy’) and different measures of reproductive success. Each dot represents the value for an individual nest (points jittered along the x-axis and rendered partially transparent); red horizontal line represents the median. a Clutch size, b number of within-pair offspring successfully fledged, c average mass of within-pair offspring at day 15 post hatch (not including nests for which no offspring survived to day 15). N = 47 individuals in each graph, except for c where N = 30
Article
Territorial animals often respond less aggressively to neighbours than strangers. This ‘dear enemy’ effect is hypothesized to be adaptive by reducing unnecessary aggressive interactions with non-threatening individuals. A key prediction of this hypothesis, that individual fitness will be affected by variation in the speed and the extent to which individuals reduce their aggression towards neighbours relative to strangers, has never been tested. We used a series of song playbacks to measure the change in response of male great tits to a simulated establishment of a neighbour on an adjacent territory during early stages of breeding, as an assay of individuals’ tendencies to form dear enemy relationships. Males reduced their approach to the speaker and sang fewer songs on later playback repetitions. However, only some males exhibited dear enemy behaviour by responding more strongly to a subsequent stranger playback, and when the playback procedure was repeated on a subset of males, there was some indication for consistent differences among individuals in the expression of dear enemy behaviour. We monitored nests and analysed offspring paternity to determine male reproductive success. Individuals that exhibited dear enemy behaviour towards the simulated neighbour did not suffer any costs associated with loss of paternity, but there was also no evidence of reproductive benefits, and no net effect on reproductive fitness. The general ability to discriminate between neighbours and strangers is likely adaptive, but benefits are probably difficult to detect because of the indirect link between individual variation in dear enemy behaviour and reproductive fitness and because of the complex range of mechanisms affecting relations with territorial neighbours. Significance statement The dear enemy effect, in which animals respond less aggressively to familiar neighbours compared to strangers, is probably beneficial because it reduces aggressive interactions with non-threatening individuals. However, no study has ever tested whether there actually are fitness benefits for individuals with a greater tendency to form dear enemy relationships. Our study used experimental playbacks to simulate neighbours and strangers, and we found no relationship between dear enemy behaviour and reproductive success in a songbird. However, our approach to test adaptive hypotheses of this widespread territorial behaviour and our longitudinal playback design to examine the development of familiarity towards a neighbour and discrimination of neighbours and strangers are likely to be important tools to advance our understanding of territorial behaviour and individual recognition.
 
a Territory distribution of dominant males and females of Neolamprologus meeli in the study area (20 × 10 m). The subordinate number is indicated in or near the territory of dominant females. Examples of territories of dominant males (blue line), dominant females (red lines), subordinates (green lines), and outsiders (orange lines) of the b monogamous and c polygynous groups. The arrows indicate the locations of b and c in a. Nest areas are shown in gray. One of the outsiders did not interact with any dominant female. Examples of home range distribution of group members in nests clipped from videos observed in another study. d A dominant male (Dm), a dominant female (Df), and four subordinates (S) stay in their nest; e both dominants and one subordinate stay in their nest; and one outsider (O) stays near the nest. Blue, red, green, orange, and black lines show territories of dominant males, dominant females, subordinates, outsiders, and nest areas, respectively
Body size (standard length (SL), mm) distribution of dominant males (n = 32), dominant females (n = 53), subordinates (males = 6, females = 12, unsexed = 7), outsiders (males = 9, females = 21, unsexed = 11), independents (males = 6, females = 9, unsexed = 4), and juveniles (n = 35) in Neolamprologus meeli. The box plots show the medians (thick horizontal lines) and 25% and 75% percentiles; the whiskers indicate the values within 1.5 times the interquartile range. Blue, red, and gray points indicate the males, females, and unsexed individuals, respectively
Mean relatedness of a dominant males (Dm), b dominant females (Df), c subordinates (S), d outsiders (O), and e juveniles (J) to members of the same subgroup (white circle), members of different subgroups within the same group (gray circle), and fish of the outgroup (black circle). See “Definition of social status and group and subgroup members” in the “Materials and methods” section for the definition of group and subgroup. Different letters denote statistically significant differences by LMMs with sequential Bonferroni correction (P < 0.05). Plots represent the mean ± SE. Sample sizes are presented above the error bars
Relationship between the body size (SL, mm) and genetic relatedness of subordinates, outsiders, and juveniles to the dominant females in the same subgroup (white circles and a thick regression line) and the dominant males in the same group (black circles and a thin regression line). Bar plots represent the mean ± SE. Sample sizes are shown above the error bars
Kinship of subgroup members with the dominant breeders in Neolamprologus meeli. Green, blue, red, and gray bars indicate individuals related to both dominant breeders, related to a male breeder but not to a female breeder, related to a female breeder but not to a male breeder, and unrelated to both dominant breeders, respectively. The number of individuals and percentages in parentheses are shown in bars
Article
Cooperative breeding systems, where individuals other than parents assist in raising offspring, have been documented in insects, fish, birds, and mammals. Still, the factors driving the evolution of such complex systems are not fully understood. Here, we report a new example of cooperative breeding in the obligate shell-brooding cichlid fish Neolamprologus meeli from Lake Tanganyika. Field observations revealed that dominant males were either monogamous or polygynous, with each mating with one to four dominant females. Dominant females maintain nests containing one to ten empty gastropod shells used as breeding substrates and shelters. Up to four immature subordinates of either sex lived in these nests. They assisted with territory defense and nest maintenance, the frequency of which was not different from that of the dominants. Parentage analyses showed that most subordinates were the offspring of at least one of the breeders, suggesting that juveniles delay dispersal and help in raising their relatives. The relatedness of subordinates to the breeders declined with increasing body size and was significantly higher to female than to male breeders. These patterns could be caused by extra-pair paternity, between-group dispersal of helpers, or sex differences in breeder turnover. Male helpers were larger than female helpers, and six out of eight dispersed individuals were females, suggesting female-biased dispersal. Because N. meeli is phylogenetically distinct from other cooperatively breeding cichlids, these results contribute to a better understanding of cooperative breeding in fishes and to understanding of the evolution of complex social systems in general. Significance statement Cooperatively breeding cichlid fishes of Lake Tanganyika are an excellent model for studying the evolution of social complexity because cooperative breeding evolved at least 5–6 times independently in a small phylogenetic group. Here, we provide a new example of cooperative breeding in the cichlid Neolamprologus meeli. Field observations revealed that these fish were either monogamous or polygynous. Subordinates remained in the breeders’ nests and helped with territory defense and nest maintenance. Subordinates of both sexes were unlikely to participate in reproduction because of their immature gonads. Parentage analyses showed that most helpers and juveniles were offspring of the dominant breeders, suggesting that N. meeli has a kin-structured cooperative breeding system. As N. meeli is phylogenetically distinct from all other cooperatively breeding cichlids, these results pose a hitherto undescribed independent evolutionary event, leading to a highly complex social system.
 
Observed residency and dispersal of subordinate immigrant males (with the size of the dots representing sample size) and the predicted relationship between the likelihood of subordinate male secondary dispersal during a particular month (with shaded areas or error bars representing the 95% confidence interval) and (A) siring offspring during the past year; (B) adult female:immigrant male ratio; (C) male age; and (D) number of years until the alpha male’s oldest daughter becomes adult, with the y-axis being square root transformed
Observed patterns of subordinate immigrant males siring offspring (with the size of the dots representing sample size) and the predicted relationship between the likelihood of a subordinate immigrant male siring offspring during a particular year (with shaded areas or error bars representing the 95% confidence interval) and (A) number of genotyped infants born that year; (B) adult female:immigrant male ratio; (C) male age category; and (D) presence of alpha’s mature daughters, with the y-axis being square root transformed
Observed number of offspring produced by immigrant males (with the size of the dots representing sample size) and the predicted relationship between the total number of infants sired (with shaded areas or error bars representing the 95% confidence interval) and (A) male position and (B) number of adult females in the group, with the y-axis being square root transformed
Each bar represents an immigrant male with the solid part of the bar showing the number of offspring produced during his tenure in the position as follows: (1) a subordinate male in a group in which the alpha male did not have mature daughters; (2) a subordinate male with alpha’s mature daughters; (3) an alpha via queuing and (4) an alpha who gained his position immediately or shortly after entering the group and the white part of the bar showing the total number of infants produced in the group during his tenure
Article
Although males often disperse to increase their immediate access to mates, it is unclear whether they also consider potential future reproductive opportunities. We investigated whether immediate or delayed reproductive opportunities predicted dispersal decisions and reproductive success of subordinate immigrant male white-faced capuchins in the Sector Santa Rosa, the Área de Conservación Guanacaste, Costa Rica. We collected genetic, behavioral, and demographic data from four social groups across 20 years. We genotyped individuals at up to 20 short tandem repeat loci to determine paternity. Having previously sired offspring in a group did not predict the subordinate immigrant male’s likelihood of staying or dispersing. Instead, a male was more likely to remain in the group if he was younger and likely to benefit from queuing for future reproductive opportunities. Subordinate immigrant males were more likely to sire offspring if they resided with a long-term alpha male and his mature daughters, who avoid inbreeding. Reproductive output was similar among three categories of males: those that became alpha immediately after immigration, those that became alpha after queuing, and subordinate males that resided with a long-term alpha male and his mature daughters. These three categories of males had higher reproductive success than subordinates who did not reside with mature daughters of the alpha male. Waiting for reproductive opportunities can lead to high reproductive success and could be important in maintaining tolerant or cooperative male-male relationships in species with high reproductive skew, long alpha male tenures, and intense between-group mating competition requiring cooperative male group defense. Significance statement We used 20 years of data from white-faced capuchins to assess whether male dispersal decisions were predicted by actual reproduction, perceived reproductive opportunities, or future reproductive opportunities and whether male reproduction was predicted by demographic factors and the male’s social position. Immigrant subordinate males were less likely to disperse from the group if they were younger and likely to benefit from queuing for future reproductive opportunities. Subordinate males residing in groups with a long-term alpha male and his mature daughters produced a similar number of offspring as did alpha males. Queuing for reproductive opportunities may maintain cooperative male-male relationships in populations with high reproductive skew and long alpha male tenures. Because these patterns only become apparent over time, our study highlights the importance of taking longitudinal paternity patterns into account to understand the evolution of dispersal and cooperation in long-lived species.
 
The social landscape of infection in Asian elephants highlighting no significant variation in infection, as estimated by faecal egg counts (FEC, in eggs per gram of faeces, epg) with differences in (a) solitary behaviour, (b) working group size, and (c) working group sex ratio. In total, 130 measures were collected from 71 individual elephants. Red points correspond to raw FECs, black points and error bars to mean and standard error FEC values, and black diamonds correspond to median FEC values. For (c), lines show predicted FECs, calculated in R using ggpredict (Lüdecke 2018), and shaded areas correspond to 95% confidence intervals. Plotted data is limited to FECs of 1000 epg, excluding one individual data point (2720epg)
Article
Frequent social interactions, proximity to conspecifics, and group density are main drivers of infections and parasite transmissions. However, recent theoretical and empirical studies suggest that the health benefits of sociality and group living can outweigh the costs of infection and help social individuals fight infections or increase their infection-related tolerance level. Here, we combine the advantage of studying artificially created social work groups with different demographic compositions with free-range feeding and social behaviours in semi-captive Asian elephants (Elephas maximus), employed in timber logging in Myanmar. We examine the link between gastro-intestinal nematode load (strongyles and Strongyloides spp.), estimated by faecal egg counts, and three different aspects of an elephant’s social world: individual solitary behaviour, work group size, and work group sex ratio. Controlling for sex, age, origin, time since last deworming treatment, year, human sampler bias, and individual identity, we found that infection by nematodes ranged from 0 to 2720 eggs/g between and within 26 male and 45 female elephants over the 4-year study period. However, such variation was not linked to any investigated measures of sociality in either males or females. Our findings highlight the need for finer-scale studies, establishing how sociality is limited by, mitigates, or protects against infection in different ecological contexts, to fully understand the mechanisms underlying these pathways. Significance statement Being social involves not only benefits, such as improved health, but also costs, including increased risk of parasitism and infectious disease. We studied the relationship between and three different sociality measures—solitary behaviour, group size, and the proportion of females to males within a group—and infection by gut nematodes (roundworms), using a unique study system of semi-captive working Asian elephants. Our system allows for observing how infection is linked to sociality measures across different social frameworks. We found that none of our social measures was associated with nematode infection in the studied elephants. Our results therefore suggest that here infection is not a large cost to group living, that it can be alleviated by the benefits of increased sociality, or that there are weak infection–sociality associations present which could not be captured and thus require finer-scale measures than those studied here. Overall, more studies are needed from a diverse range of systems that investigate specific aspects of social infection dynamics.
 
Article
The function of holding territories is primarily to have access to resources like food and mates. However, it is costly in terms of energy and time investment. Solitary-living, territorial species are known to reduce these costs by being more aggressive towards unfamiliar strangers and less aggressive towards neighbors. However, in social, territorial species, neighbors can impose a greater threat than strangers. We tested whether the highly social Asiatic wild dogs/dholes (Cuon alpinus) exhibit the “nasty neighbor” or the “dear enemy” phenomena in Tadoba Andhari Tiger Reserve (TATR), Maharashtra, India. We conducted scat translocation experiments where we presented fresh scats collected from unique donor groups to a resident dhole group and tested the type and the intensity of behavioral response (duration) to the stimulus. Dholes responded differentially to the two treatments suggesting they exhibit neighbor-stranger discrimination. Overall, strangers elicited a stronger response with longer duration and larger packs were less likely to respond to the stimulus than smaller packs. Differences found between categories of dhole scent marks establish the importance of olfactory communication, especially “counter-marking” in the species. Within recipient packs, individual status affected the response to trials wherein the alpha pair reacted more intensively to strangers than others. Our study provides experimental evidence to demonstrate that dholes exhibit the “dear enemy” phenomenon. Significance statement Animals defend territories from other members of their own species, but intrusions are commonplace in the wild. Different intruders may pose different levels of threats, and hence, intruders are treated differentially to minimize the energetic costs of territorial defense. In some animals, neighbors with well-established territories may become less aggressive towards each other. This is known as the dear enemy effect. By contrast, at times neighbors may represent a greater threat than strangers which is known as the “nasty neighbor” effect. We experimentally show that dholes exhibit the dear enemy phenomenon by responding more intensively to strangers than familiar neighbors. We show how response varied based on hierarchy in a pack as well as the pack sizes. Furthermore, we found that, both in core as well as buffer areas of their own territory, this relationship was consistent.
 
Relationship between the number of foraging workers in a group and the total number of offspring produced in nests with worker-queens and foundress-queens. 95% confidence intervals are indicated by dashed lines and fitted relationships by solid lines. Note that the x-axis scale is different for the two graphs
Relationship between the number of trips per brood and the number of foraging workers for each treatment. Trips per brood were calculated as foraging trips per day divided by offspring per day of foraging. 95% confidence intervals are indicated by dashed lines and fitted relationships by solid lines. Note that the x-axis scale is different for the two graphs
Relationship between total foraging time and the number of workers for each treatment. 95% confidence intervals are indicated by dashed lines and fitted relationships by solid lines. Note that the x-axis scale is different for the two graphs
Relationship between the number of trips per worker and the number of workers for each treatment. Trips per worker were calculated as total days of foraging multiplied by foraging trips per day divided by number of workers. 95% confidence intervals are indicated by dashed lines and fitted relationships by solid lines. Note that the x-axis scale is different for the two graphs
Article
Plasticity is a key trait when an individual’s role in the social environment, and hence its optimum phenotype, fluctuates unpredictably. Plasticity is especially important in primitively eusocial insects where small colony sizes and little morphological caste differentiation mean that individuals may find themselves switching from non-reproductive to reproductive roles. To understand the scope of this plasticity, workers of the primitively eusocial sweat bee Lasioglossum malachurum were experimentally promoted to the reproductive role (worker-queens) and their performance compared with foundress-queens. We focussed on how their developmental trajectory as workers influenced three key traits: group productivity, monopolisation of reproduction, and social control of foraging nest-mates. No significant difference was found between the number of offspring produced by worker-queens and foundress-queens. Genotyping of larvae showed that worker-queens monopolised reproduction in their nests to the same extent as foundress queens. However, non-reproductives foraged less and produced a smaller total offspring biomass when the reproductive was a promoted worker: offspring of worker-queens were all males, which are the cheaper sex to produce. Greater investment in each offspring as the number of foragers increased suggests a limit to both worker-queen and foundress-queen offspring production when a greater quantity of pollen arrives at the nest. The data presented here suggest a remarkable level of plasticity and represent one of the first quantitative studies of worker reproductive plasticity in a non-model primitively eusocial species. Significance statement The ability of workers to take on a reproductive role and produce offspring is expected to relate strongly to the size of their colony. Workers in species with smaller colony sizes should have greater reproductive potential to insure against the death of the queen. We quantified the reproductive plasticity of workers in small colonies of sweat bees by removing the queen and allowing the workers to control the reproductive output of the nest. A single worker then took on the reproductive role and hence prevented her fellow workers from producing offspring of their own. These worker-queens produced as many offspring as control queens, demonstrating remarkable worker plasticity in a primitively eusocial species.
 
Relationship between age and number of offspring produced for both males and females. Points are raw data. Lines and 95% credible intervals are based off of predicted values from males and females located down valley. Females were considered of average mass (scaled mass = 0). Males are in turquoise and females in red
The (a) additive genetic and (b) year cross-sex variance matrices of annual reproductive success. Points in each graph are the posterior mode of the best linear unbiased predictors (BLUPs) from the bivariate models. Points in yellow are males, in black are females and purple are years. Bold ellipses represent the posterior mode of the variance matrices, while grey ellipses are from 300 randomly selected estimates from the posterior distribution. Grey ellipses offer a sense of uncertainty around the estimate
Article
Owing to sex-specific reproductive strategies, the mean and variance in annual offspring production may differ between the sexes. In addition, there may be sex-specific changes in reproductive performance with age (e.g. senescence). We used 20 and 50 years of longitudinal data on male and female yellow-bellied marmots, respectively, to investigate sex-specific age effects and genetic variance in annual reproductive success. In both sexes, annual offspring production increased linearly with age until a peak was reached at 7 years. This was followed by a decline in annual offspring production in both sexes, indicative of reproductive senescence. However, the initial increase and the subsequent decline (senescence) in reproductive success were both faster in males compared to females. Genetic variance in annual offspring production was higher in males than in females, but heritability was low for both sexes. Additionally, we found no cross-sex genetic correlation in the number of offspring produced, possibly reflecting sex-specific selection related to the inter-sexual differences in reproductive strategies. There was an effect of year on annual offspring production in both sexes, with a high yearly correlation between the sexes emphasizing the importance of environmental variation in determining fitness. Overall, these results demonstrate the impact of sex-specific reproductive strategies on annual offspring production and suggest that male and female marmots may be evolving to separate phenotypic optima. This study further demonstrates the value and limitations of long-term studies investigating sex-based patterns of ageing in the wild. Significance This study on yellow-bellied marmots demonstrates the key constraints surrounding the research of age-related changes in reproduction in wild populations, which is especially challenging in males. Among these challenges are high immigration rates which prevent the estimation of exact age and maternal identity. Genetic analysis—the only reliable way to estimate paternity—has only been a recent development, limiting the number of father-son relationships available for analysis. The dataset used in this study is long term (20 years of data on males and 50 on females), partially overcoming these obstacles. Results show that reproductive success declines with age in both sexes, with a faster rate of decline in males compared to females, and is influenced by the environment. Genetically, male and female reproductive success is not correlated, revealing that both sexes may be following separate evolutionary trajectories.
 
The relationship between the size of fledged broods and productivity. Productivity at each brood size was calculated as the number of fledglings multiplied by the per capita recruitment probability, estimated from a GLMM that had brood size, presence of helpers, sex, and fledge date as fixed effects and year (1994–2018, excluding 2000) and nest ID (n = 238 nests) as random effects
The probability that a nest is helped as a function of a the number of nestlings, b the age of nestlings (in days), c the number of other helpers at the nest, and d distance from the helper’s breeding attempt. Lines are predictions from GLMMs, controlling for other fixed effects and helper ID, and the shaded area denotes the standard error. Boxplots show values for helped and non-helped nests. Central lines represent median values, outer lines of the box represent the first and third quartiles, and horizontal lines represent approximately 2 SD around the interquartile range. Points are raw data
The probability that a nest is helped as a function of the indirect fitness payoff that a helper stands to receive from caring for the brood. The line is predicted from a GLMM, controlling for distance from the helper’s breeding attempt and helper ID, and the shaded area denotes the standard error. Boxplots show values for helped and non-helped nests. Central lines represent median values, outer lines of the box represent the first and third quartiles, and horizontal lines represent approximately 2 SD around the interquartile range. Points are raw data
Article
Cooperative breeding sometimes occurs when adult breeders form groups following natal dispersal and mating. In such cases, individuals typically face a choice of social partner with whom to cooperate. Selecting appropriate social partners is crucial to maximising the fitness payoffs from cooperation, but our understanding of the criteria guiding partner choice is limited. Here, we analyse helping decisions by long-tailed tits (Aegithalos caudatus), which may redirect their care to assist breeders in raising offspring following the failure of their own nests. In this species, helpers prefer to help relatives at nearby nests, but it is unclear whether other criteria that may affect helper fitness also influence helping decisions. When choosing among broods of equivalent kinship, we found that helpers did not prefer those broods that offered the greatest indirect fitness returns. Further analyses revealed that helpers did not choose nests on the basis of brood size or age, but were more likely to help broods that were closer to their own failed nests and that were already being cared for by other helpers. Both effects likely reflect the limited choice available to helpers: although individuals breed close to relatives within kin neighbourhoods, a high rate of nest predation constrains helpers’ choice of broods. In other species where cooperatively breeding groups form after natal dispersal, a greater range of options may be available and here detailed analysis of group formation will be helpful for determining the decision rules that underpin partner choice and permit stable cooperation in the face of alternative options. Significance statement Cooperative breeding occurs most frequently when offspring delay dispersal from their natal site and help to care for their younger siblings. In some species, however, individuals first disperse and then come together as adults to cooperate in rearing young. In the latter case, multiple social partners may be available — what then determines which partner is helped? We studied partner choice in long-tailed tits, which may help to feed other broods if their own brood fails. When multiple related broods were available, individuals were more likely to help those close by but showed no preference for broods offering the greatest indirect fitness returns. One explanation for this result is that helping options for most individuals are limited by high levels of nest predation, favouring a simpler decision-making process based on identifying close relatives breeding in close proximity.
 
Schematic representation of the design main assay. Experimental subsets were generated from stock populations following one generation of standardization (common garden rearing). Experimental males were generated in the following manner: CO (i.e. control) subset was used to generate CO experimental males and CCO males (phenocopied controls, these were generated by growing larvae at a density of 240 per 3 ml of standard food) and ACO (i.e. evolved) males were generated from ACO stock. Oregon R females were generated separately under standard conditions as common female for all three regime males. On assay day, the whole set-up was divided into two male-exposure condition, i.e. single exposure (where males and females are allowed to mate once) and continuous exposure (where males and females were housed together after first mating). Trait assays were then carried out for 20 days where female mortality was recorded every day, and fecundity and courtship frequency were noted at every 5-day interval. All vials were flipped into fresh food vial at every alternate day
Effect of exposure to treatment males (ACO/CCO/CO) on female mortality and fecundity. (a) Proportion of females died by the end of the 20-day assay period (cumulative female mortality), under the two male-exposure conditions — single exposure and continuous exposure. The vertical bars indicate the mean across all replicate populations. Error bars represent the standard errors of means (SEM); (b) average per capita fecundity of experimental Oregon R females exposed to treatment males across all five age classes, under the two male exposure conditions — single exposure and continuous exposure. Means were calculated over five replicate populations. Only relevant multiple comparisons, which were done using Tukey’s HSD, are shown. Significant differences are marked with horizontal line and an asterisk. The X-axis for both the panels represents male exposure conditions
Results of the courtship behaviour assays. (a) Courtship frequency (bouts of courtship per observation) was measured for the 20-day assay period on days 2, 6, 11, 16 and 20 in the continuous exposure vials of the main assay. (b) Frequency of the five components (proportional contribution of a courtship component) of courtship ritual was measured in a separate assay, where evolved (ACO) and control (CO) males were held with Oregon R females. The vertical bars indicate the mean across all five replicate populations. Error bars represent the standard errors of means (SEM). Only relevant multiple comparisons are shown in the figure. Significant differences are marked with horizontal line and an asterisk
Article
Detrimental effect of males on female, often termed mate harm, is a hallmark of sexual conflict. Allowed to evolve unchecked, mate harming traits are predicted to bring down average fitness of a population, unless mitigated by the evolution of resistance in females. In addition, life history may also modulate sexual conflict, but the mechanism is not clearly understood. Here we investigated the evolution of mate harm in a set of experimentally evolved laboratory populations of Drosophila melanogaster, wherein a faster aging has evolved in response to > 1000 generations of selection for faster development and early reproduction. We quantified mortality and fecundity of Oregon R females held with evolved and ancestral males to show that the evolved males are significantly less detrimental to their mates. We compared our results from the evolved males with that from a phenocopied version of the ancestral regime males to show that only part of the observed difference in mate harm can be attributed to the evolved difference in body size. We further show that the reduction in mate harming ability evolved despite an increase in courtship activity, especially early in life. We discuss the causative role of an evolved reproductive schedule and altered breeding ecology. Significance statement Sexually antagonistic male effects can significantly bring down female fitness. Along with female counter evolution of resistance traits, life history has been conjectured to impose constrains on the evolution of such harming ability in males. Here, we report the evolution of mate harming ability in males of a set of five replicate Drosophila melanogaster populations that evolved smaller size and faster aging as a result of > 1000 generations of experimental evolution for faster development and early reproduction. We show that in spite of ample scope of sexual selection, the faster aging males have evolved reduced mate harming ability despite being more active in courting their mates. To the best of our knowledge, this is one of the first clear evidences demonstrating the causal relationship between evolution of life history and reduction in sexual antagonism in a population.
 
The relationship between prey size and number of jerks towards the prey in a within-individual (N = 30 spiders) and b inter-individual comparison experiments (N = 116). The line in (b) shows the predicted values from linear regression, and the shadowed area shows 95% confidence intervals
The relationship between spider size and the number of jerks in a intraspecific (N = 29) and b interspecific comparison experiments. In (a), three different prey (from the smallest pinhead crickets to the largest worker termite) were used. Lines show the predicted values from linear regressions for each prey type. Shadowed areas show 95% confidence intervals. In (b), similar-sized dipteran prey were given to three different co-occurring species of the Cyclosa genus. sede: C. sedeculata (the smallest), arge: C. argenteoalba (medium), octo: C. octotuberculata (the largest). Bars and error bars show the mean and standard error of the mean, respectively
The results of the prey escape experiment showed the difference in the proportion of successfully escaped prey under spider-present and absent conditions
a Comparison of the additional number of spiral threads entangled around the prey (1) due to prey struggling under spider-absent condition (PS −), (2) due to prey struggling under spider-present condition (PS +), (3) due to spider jerks (JS +). Each boxplot shows the median, first, and third quartiles. Dots show outliers. b Relationship between prey size and jerk efficiency (the number of additional spiral threads that became entangled around the prey per jerk) (N = 48; one outlier removed). The line shows the predicted values from linear regression, and the shadowed area shows 95% confidence intervals
The relationship between prey size and approaching time (defined as the time from the spider responding to prey and prey capture) (N = 119). Lines show the predicted values from linear regression, and the shadowed area shows 95% confidence intervals
Article
Orb-weaving spiders often use their legs to briefly jerk the radii of the web, generating intense vibrations throughout the web. Several functions have been proposed for this behaviour, but there is a lack of empirical evidence. In this study, we conducted a series of experiments on Cyclosa argenteoalba to examine the function and adaptive significance of spider jerks in the context of interactions with prey. First, we used within-individual, inter-individual, and interspecific comparisons (in three co-occurring Cyclosa sp.) to test whether the relation between prey and spider size predict the frequency of jerks that the spider performs. Second, we examined whether jerks prevent prey from escaping the web, whether jerks entangled more spiral threads around the prey, and how prey size affected this result. We found that spiders jerked more as the prey size increased and as spider size decreased. Jerking behaviour reduced the probability of prey escaping from the web and increased the number of spiral threads contacting the prey. The jerk efficiency (the number of additional spiral threads contacted per jerk) was lower in larger prey, which potentially explains why spiders jerk more towards larger prey. Collectively, our results highlight size dependency in the performance of jerks and their role in prey capture. Significance statements Many orb-weaving spiders show a behaviour that pulls the radii of the web intensively using their legs towards their prey, called jerks. Though this behaviour is common and has been recognised for many decades, the function and their adaptive significance have been surprisingly understudied. Using a series of experiments, we demonstrate that jerks help spiders prevent prey escape and subdue prey by entangling additional spiral (sticky) threads around the prey. We further show that the performance of jerks is size-dependent: spiders jerk more (1) as their size decreases and (2) as prey size increases. Further in-depth analysis suggests that the observed size-dependent jerks seem to be related to spiders’ cautiousness and/or reduced jerk efficiency towards larger prey.
 
Critical thermal maximum (°C) values for foragers of different sizes (mm) belonging to the ant species M. barbarus (red), M. bouvieri (black), and M. capitatus (blue) at the three study locations: (a) Castellbell i el Vilar, (b) Collserola Park, and (c) UAB. The fitted lines come from the GLMMs. n, number of foragers
Daily foraging activity (number of ants entering a colony during a 2-min interval) for the ant species M. barbarus (red), M. bouvieri (black), and M. capitatus (blue) across the hours of the day (a, b) and at different soil surface temperatures (c, d) during the two sampling seasons (summer: a, c and autumn: b, d)
Mean (± SE) percentage of colonies actively foraging during each sampling period and season (summer in red and autumn in blue) for the ant species M. barbarus, M. bouvieri, and M. capitatus. *** = P < 0.0001; ns, not significant
Distributions of M. barbarus forager size during the early foraging period (low temperatures, in gray) and the late foraging period (high temperatures, in orange). The temperature difference between the two periods was at least 10 °C
Article
Physiological thermal limits can mediate species coexistence at local scales. However, it is challenging to untangle the role they play when coexisting species are also highly related, given that phylogeny may inform physiology. However, if species exploit similar trophic resources, there must be a degree of niche differentiation that precludes competitive exclusion. Physiological traits frequently correlate with body size. Furthermore, they often vary within and among animal populations, allowing organisms to optimize their foraging dynamics under different thermal conditions. Here, we analyzed interactions among critical thermal maxima (CTmax), foraging patterns, and forager size in three congeneric, sympatric, and polymorphic harvester ant species (Messor barbarus, M. bouvieri, and M. capitatus). We characterized CTmax for different-sized foragers sampled from co-occurring colonies of the three species and analyzed the colonies’ daily and seasonal foraging patterns. We also performed a baiting experiment using M. barbarus to explore the relationship between forager size and foraging temperature. In general, the species displayed different CTmax values. For similar-sized foragers, the less polymorphic M. bouvieri had higher CTmax values than did the highly polymorphic M. barbarus and M. capitatus. There was a strong positive relationship between worker size and CTmax within colonies, but the results of the baiting experiment found that foraging temperature did not influence forager size distributions. While interspecific differences in foraging patterns were influenced by environmental temperatures, these dynamics were not fully attributable to species physiology. Competition may be playing an important role as well, in the form of other factors. Significance statement Congeneric, sympatric, and polymorphic species that occupy similar trophic niches can display different physiological thermal limits and foraging patterns. However, physiological differences alone do not explain species coexistence. Competition might be at work as well, operating in forms other than thermal physiology. Indeed, coexistence may occur because competition acts through behavioral patterns, such as temporal segregation in foraging. Here, although larger workers had higher critical thermal maxima, Messor barbarus did not appear to send out larger foragers when temperatures were higher. The absence of such a response could potentially hobble species persistence under future conditions of climate change. To understand how global changes will affect the world’s terrestrial ecosystems, we need research that examines species physiology and biotic interactions in tandem.
 
Dorsal (a) and ventral (b–d) views of male striped lava lizard (Tropidurus semitaeniatus) showing body regions in which we measured coloration. Dorsal (a) numbering refers to locations of the dorsal head stripe (I), dorsal stripe (II), and dorsal side stripe (III). Ventral (b–d) numbering refers to locations of the throat (I), chest (II), ventral patch (III), femoral patch (IV), and ventral tail base (V). Male striped lava lizards express two color morphs when reaching reproductive age. By a human visual system (mainly trichromatic), morphs are differentiable in their ventral-colored patches (III, IV). The pictures were taken from live individuals and the hand of the researcher covers the lizards in part (b, c). Thus, their silhouettes are delimited by white dotted lines
Scheme of tanks from birds-eye perspective of visual female choice experiments between male color morphs of the striped lava lizard (Tropidurus semitaeniatus). Males’ compartments (above in blue, A and B) are separated from the female’s compartment (below, in pink and white colors) by a transparent plexiglass (dashed line). A solid opaque wall separates the males’ compartments (A from B) and female’s Left and Right counting areas (in pink). A female positioned at the Left area (pink) can visualize uniquely the male in compartment A. A female positioned in the Right area can only visually assess the male in compartment B. Whereas a female located in Neutral area (in white) is able to visually assess both males
Article
Sexual selection is a driver of morphological and behavioral diversity. It may also play a role in the maintenance of behavioral and morphological polymorphisms. Adaptive theory predicts that males advertise individual quality through one or more signal paths and that females choose better quality mates based on those signals. Here, we use mate choice experiments in two different signaling modes (chemical and visual), to test whether females of a color cryptic-polymorphic lizard have a preference between two co-occurring male morphs (black and yellow) with alternative behavioral types. We test whether females use visual (males’ coloration) and/or chemical cues to choose male morphs. Furthermore, we assess whether continuous costly color expression influences female choice and whether male conspicuousness in their natural background predicts female mate choice. We show that females prefer the aggressive black-morph males based on chemical cues. Females prefer more conspicuous males as mates, and coloration at polymorphic ventral part of the body also contributes to higher conspicuousness of these males. Our study adds to the knowledge of intersexual selection for multi-component signals and opens possibilities for future research to explore the roles of complementary signal modes. Significance statement Sexual selection can drive the evolution of a great diversity of behavioral and morphological features and has puzzled naturalists ever since Darwin. We studied sexual selection in the striped lava lizard (Tropidurus semitaeniatus), a species endemic to Northeast Brazil. This species is known to have two different “types” of males (yellow or black). In our study, we conducted mate choice experiments to test whether females prefer males based on chemical and/or visual cues. Black males tend to be more aggressive and dominant, and we showed that females prefer these males based on their scent. We show that females prefer males that are more conspicuous within their natural habitat, and that ventral polymorphic coloration is related to female preference. Our study highlights the complexity of animal signals and contributes to our understanding of sexual selection and the role of complementary signal modes.
 
The effects of a, b interaction between carcass size (15 g versus 25 g) and parental sex (male versus female), c, d carcass preparation (non-prepared versus prepared) on the amount and duration of parental care, e carcass size, and f interaction between carcass preparation and parental sex on weight change of burying beetle parents in the first breeding. Boxplots show median, interquartile range, and minimum/maximum range. Black points on each box are mean values. Numbers above error bars are sample sizes. For statistical analyses, see Tables 1 and 2. Asterisks, significant (P < 0.05); n.s., not significant
The carry-over effects of a, b interaction between carcass size (15 g versus 25 g) and parental sex (male versus female), c, d interaction between carcass preparation (non-prepared versus prepared) and parental sex on the amount and duration of parental care, e carcass size, and f carcass preparation on weight change of burying beetle parents in the second breeding. Boxplots show median, interquartile range, and minimum/maximum range. Black points on each box are mean values. Numbers above error bars are sample sizes. For statistical analyses, see Tables 3 and 4. Asterisks, significant (P < 0.05); n.s., not significant
Article
Life-history theory predicts trade-offs between investment in current versus future reproduction. However, many studies find no or even positive correlations among these traits. The absence of the trade-off may result from resource availability, as it influences resource allocation to different traits. In addition, since large amounts of resources require additional effort in processing, resource maintenance may affect the detection of reproductive trade-offs. Here, we carried out two breeding attempts to assess the effects of resource availability and maintenance on reproductive trade-offs for both sexes in the burying beetle ( Nicrophorus vespilloides ). In the first breeding attempt, we simultaneously manipulated carcass size (small versus large) and carcass preparation (non-prepared versus prepared). In the second breeding attempt, we provided parents with same-sized, non-prepared carcasses. For both breeding attempts, we monitored the main and interactive effects of carcass size and carcass preparation on parental effort and reproductive outcome. In the first breeding attempt, males gained more weight and provided more care as carcass size increased, whereas females gained more weight but did not change their care. In addition, when breeding on non-prepared versus prepared carcasses, both parents provided more care and gained more weight. In the second breeding attempt, with increased investment for the first breeding, parents did not show decreased investment for the second brood, vice versa. In contrast, males breeding on large or non-prepared carcasses gained more weight during the first breeding attempt, then provided more care in subsequent reproduction. There were no differences in subsequent female care among different treatments. Significance statement Resource availability and resource maintenance may affect the detection of reproductive trade-offs. Here, we simultaneously manipulated carcass size and carcass preparation to assess these effects. This is the first time that the effects of resource availability and resource maintenance on reproductive trade-offs have been separated in burying beetles. Our findings suggest that despite the increased costs of parental care and resource maintenance, parents breeding on large or non-prepared carcasses gained more benefits in terms of increased body weight by staying longer and feeding more from the carcasses. Such benefits gained during the first breeding attempt offset the costs of current reproduction to some degree and masked the reproductive trade-off between current and future reproduction in terms of parental care. These findings enhance the understanding of the effects of resource availability and maintenance on reproductive trade-offs.
 
Effects of body mass (A), leg length (B), and arm length (C) on yearly standardized randomized Elo-ratings of 198 eastern grey kangaroo male-years at Wilsons Promontory National Park (Australia), 2010–2011 and 2015–2018. Body mass was used as the sole predictor of estimated Elo-ratings in A. Models for leg (B) and arm (C) length included an interaction with body condition, as well as its additive effect. Body condition was a continuous variable, but for illustration purposes, males in poor condition (Kn < 0; N = 110) are represented by empty triangles and broken lines and males in good condition (Kn > 0; N = 88) by dots and continuous lines. Lines and associated shaded areas are model predictions ± 95% CIs
Probability of an eastern grey kangaroo male winning unescalated contests (upper row, N = 2,059; displays, displacements, and play-fights) or fights (lower row, N = 51) depending on asymmetry in body mass (A, D), leg length (B, E), and arm length (C, F) compared to its opponent at Wilsons Promontory National Park (Australia), 2010–2018. Solid lines and associated grey-shaded areas represent logistic regressions ± 95% CIs from binomial models. Dots are raw data points for probability of winning
Absolute body-mass and limb-length asymmetries of eastern grey kangaroo male pairs that were involved in fights and unescalated contests at Wilsons Promontory National Park (Australia) in 2010–2018, compared to randomly selected male pairs. Boxplots show medians, first, and third quartiles (center, lower, and upper borders, respectively). Whiskers represent the values within 1.5 times the interquartile range below and above the 25th and 75th percent percentile, respectively. Median, first, and third quartiles and whiskers of simulated fights and unescalated contests are the mean values obtained from the 50 resampling datasets
Relationship between estimated dominance ratings and reproductive success for 203 eastern grey kangaroo male-years at Wilsons Promontory National Park (Australia) in 2010–2011 and 2015–2018. Randomized Elo-ratings were standardized within each year. A) Standardized linear selection differential for yearly standardized randomized Elo-ratings on yearly relative reproductive success. The line represents the strength of selection (i = 0.582). B) Relationship between estimated randomized ratings and yearly reproductive success. The line and associated shaded areas show predicted reproductive success ± 95% CI. Dots are raw data points. Note that the scales on the Y-axes for panels A and B are different
Article
Group-living species are often organized into social dominance hierarchies, where high-ranking individuals have priority of access to resources, including estrous females. Traits associated with male dominance status should thus be correlated with reproductive success, but, with the exception of research on some primates, studies with both behavioral data to determine dominance hierarchies and a pedigree to identify male siring success are rare. For a wild population of sexually dimorphic eastern grey kangaroos Macropus giganteus, we characterized the social hierarchy over 6 non-consecutive years to investigate the relationship between male dominance and yearly reproductive success. Dominance hierarchies were steep, linear, and stable over time. Asymmetries in body mass and size between contestants were strong predictors of contest outcomes, and these morphological traits were positively correlated with dominance status. Males did not spatially avoid each other but tended to fight with individuals of similar size, suggesting that when asymmetries were large, contests were unlikely. Dominance status was under strong sexual selection, despite moderate monopolization of paternities by highly dominant males. Overall, these results suggest that body size and weapons are important determinants of dominance status and male reproductive success but that other traits play a considerable role. A clear-cut dominance hierarchy and strong selection on dominance status do not necessarily lead to monopolization of reproduction by the most dominant males in this strongly sexually dimorphic species.
 
Article
Animal species differ considerably in longevity. Among mammals, short-lived species such as shrews have a maximum lifespan of about a year, whereas long-lived species such as whales can live for more than two centuries. Because of their slow pace of life, long-lived species are typically of high conservation concern and of special scientific interest. This applies not only to large mammals such as whales, but also to small-sized bats and mole-rats. To understand the typically complex social behavior of long-lived mammals and protect their threatened populations, field studies that cover substantial parts of a species’ maximum lifespan are required. However, long-term field studies on mammals are an exception because the collection of individualized data requires considerable resources over long time periods in species where individuals can live for decades. Field studies that span decades do not fit well in the current career and funding regime in science. This is unfortunate, as the existing long-term studies on mammals yielded exciting insights into animal behavior and contributed data important for protecting their populations. Here, I present results of long-term field studies on the behavior, demography, and life history of bats, with a particular focus on my long-term studies on wild Bechstein’s bats. I show that long-term studies on individually marked populations are invaluable to understand the social system of bats, investigate the causes and consequences of their extraordinary longevity, and assess their responses to changing environments with the aim to efficiently protect these unique mammals in the face of anthropogenic global change.
 
The number of flocking or solitary species in the most frequently included avian families from a phylogenetic analysis of the ecological determinants of flocking
Estimated probabilities of flocking as a function of diet in a phylogenetic analysis of flocking across species of birds. The probabilities are shown for each diet class as a function of the first component of a PCA based on life history variables. More positive values for this component are associated with slower life histories (greater annual adult survival and smaller clutch sizes). Raw species data are shown for each species as black dots. Acronyms are the following: Invertebrate-SE, invertebrate prey obtained through searching; Invertebrate-SA, invertebrate prey obtained through sallying
Estimated probabilities of flocking as a function of foraging substrate in a phylogenetic analysis of flocking across species of birds. The probabilities are shown for each substrate as a function of the first component of a PCA based on life history variables. More positive values for this component are associated with slower life histories (greater annual adult survival and smaller clutch sizes). Raw species data are shown for each species as black dots. Acronyms are the following: Aquatic-SE, aquatic species at sea; Aquatic-SH, aquatic species at shoreline; Aquatic-F, aquatic species in freshwater; Terrestrial-G, terrestrial species foraging on the ground; Terrestrial-AG, terrestrial species foraging above ground
Article
Why birds form flocks during foraging has been long debated. Flocking like other types of group living has probably been shaped over evolutionary times by ecological factors related to food abundance and distribution and predation risk while foraging. Comparative analyses have identified several ecological correlates of group living in many taxa but have yet to be performed comprehensively in birds. Here, I conducted a phylogenetically-based comparative analysis of flocking using a large number of species (> 1000) found across the world to examine the effect of many ecological and life history variables related to food distribution and abundance and predation risk. The analysis revealed that flocking was more prevalent in species with a plant diet, in aquatic species, and in species with slow life histories. The results generally support the idea that resource abundance and distribution and perceived predation risk during foraging have shaped the evolution of flocking in birds.
 
Article
Ontogeny is expected to be a determinant factor affecting production of colour patches in lizards, while immune challenges or sudden weight loss may impair the maintenance of pigment-based coloration within a breeding season. We translocated males of the lizard Psammodromus algirus between two sampling plots that differed in distance to a road, vegetation structure, and predator abundance. We analysed variation in spectral reflectance of their colour patches the same and the following year. The change in the reflectance of the lizard colour patches within the first breeding season was explained by the interaction between plot and treatment, but not body condition. The maintenance of the breeding coloration was impaired only in those males translocated close to the road, probably reflecting that it is a poor-quality habitat for P. algirus . The following year, lizards that produced a more elaborate coloration were those that increased their body condition and controlled some parasitic infections, although suffered an increase of others. This study shows that colour patch production is plastic in P. algirus . Lizards increasing parasites or losing weight reduced pigmentation, although habitat quality can cushion these negative effects on pigmentation. However, not all parasites constrain the investment in coloration. In fact, some increased in those lizards that allocated more pigments to colour patches. In conclusion, longitudinal studies following experimental manipulation can contribute to understand pigment allocation rules in lizards. Significance statement Pigments involved in colour patches of animals are limiting resources that can be reallocated off the skin to other functions. However, longitudinal evidence of this phenomenon is scarce in reptiles. We designed a manipulative mark-recapture experiment to investigate effects of habitat and parasitic infections on colour patch maintenance (within-year variation) and production (between-year variation) in male free-ranging lizards that were reciprocally translocated between two patches of habitat that differed in quality. During the first year, lizards translocated to the habitat with more predators and worse vegetation impoverished their coloration, while lizards translocated to the more favourable habitat maintained it despite all translocated lizards loose body condition. The next year we detected different effects on the coloration of three different parasites investigated, suggesting that coloration can reflect the virulence of the infections.
 
Pairwise correlation plots for (A) male and (B) female annual fitness metrics calculated from offspring counted at birth (λan_b)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$(\lambda_{an\_b})$$\end{document}, weaning (λan_w)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$(\lambda_{an\_w})$$\end{document}, or surviving to yearling age (λan_y)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$(\lambda_{an\_y})$$\end{document}. The distribution of data is given on the diagonal. Significant Spearman’s correlation coefficients are given for ***P < 0.001
Selection on emergence date from regression of annual fitness (λan)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${(\lambda }_{\mathrm{an}})$$\end{document} on year-centered emergence dates in males (top panels) and females (bottom panels). Fitness was calculated for fecundity based on offspring counted at birth (λan_b)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${(\lambda }_{\mathrm{an}\_b})$$\end{document} (A, B), weaning (λan_w)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${(\lambda }_{an\_w})$$\end{document} (C, D), or yearling age (λan_y)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${(\lambda }_{\mathrm{an}\_\mathrm{y}})$$\end{document} (E, F). Significant regressions are indicated by black lines, and the gray ribbons represent 95% confidence intervals
Fecundity selection on emergence date from regression of relative annual reproductive success on year-centered emergence dates in males (top panels) and females (bottom panels). Fecundity was calculated from offspring counted at birth (A, B), weaning (C, D), or surviving to yearling age (E, F). Significant regressions are indicated by black lines, and gray ribbons represent 95% confidence intervals
Article
Measuring individual reproductive success in the wild is often achieved by counting the number of descendants produced by individuals. In seeking to understand how reproductive success can inform us about natural selection, however, we are faced with a conundrum. In terms of timing, what is the most relevant measure for examining selection? We might count the number of offspring born, surviving to the termination of parental care, surviving to adulthood, or only those surviving to themselves reproduce. Clearly, only the latter are passing on genes and traits to future generations, but this estimate may not always be available. So, are different estimates of fitness consistent? Do they provide us with similar inferences of selection on phenotypic traits? We examined these questions on a 29-year long-term study of individually monitored male and female Columbian ground squirrels (Urocitellus columbianus). We used the long-term data to calculate male and female fitness based on an annual measure of adult survival and the yearly production of offspring counted at the stages of birth, weaning, and yearling age. We then decomposed fitness into its constitutive elements including (1) adult survival to the next spring, and (2) the yearly production of offspring counted at the stages previously mentioned. We then compared fitness metrics to evaluate if they provided similar or contrasting information in the wild. Next, we used those fitness metrics to test for selection on the date of emergence from annual hibernation, a phenotypic trait previously shown to be highly variable, heritable, and associated with reproduction. Finally, we partitioned selection on emergence date into additive episodes of selection by looking at how selection changed from reproduction measured at birth, weaning, and when offspring reached yearling age. Overall, fitness metrics were well correlated, but correlations weakened the further offspring were counted from birth. We generally found directional selection for earlier emergence dates both in males and females. The strength of selection depended on which fitness metric was used. Most of the selection gradient on emergence date was explained by offspring born, and the selection differential was stronger in males than females. We evaluate how the choice of fitness metrics in life-history studies may nuance our inferences about natural selection. Significance statement This study explores how our inferences about natural selection acting on organismal traits vary depending on our choice of fitness metrics. Focusing on the timing of emergence from hibernation in Columbian ground squirrels, we show that directional selection for earlier emergence dates occurs, but the strength of selection depends on whether fitness is evaluated from offspring counted at birth, at weaning, or later in life. These results show that the choice of timing for fitness measurements may nuance inferences about natural selection in life-history studies.
 
Representative spectrograms of the begging calls used in the playback experiment corresponding to a) baywing, b) screaming cowbird and c) shiny cowbird fledglings (13–20 days old)
Kaplan–Meier curves for latency (in seconds) in response to the playback treatments. The curves indicate the proportion of nests in which there was no response to each call type as a function of time since the treatment began (n = 13 nests)
Box plots showing the response of adult baywings to playback of begging calls of baywing (control), screaming cowbird (mimetic) and shiny cowbird (non-mimetic) fledglings. Calls were broadcast from a loudspeaker placed near baywing nests having 9–11-day-old nestlings. Response variables were: a) duration measured as the total time spent by at least one baywing at less than 50 cm from the loudspeaker, b) frequency measured as number of times at least one baywing approached the loudspeaker and c) recruitment as number of responding adults relative to total group size. Sample size was 39 measures in13 nests for all response variables. Boxes indicate the inter quartile range (IQR), the line within each box indicates the median, and whiskers depict 1.5*IQR. Dots outside the box represent outliers
Article
Agonistic interactions between obligate avian brood parasites and their hosts can lead to the coevolution at any stage of the nesting cycle, yet adaptations and counter-adaptations at the fledgling stage are poorly known. Young of the host-specialist screaming cowbird (Molothrus rufoaxillaris) closely resemble those of its greyish baywing (Agelaioides badius) host in appearance and begging calls. This overall similarity has shown to be adaptive to escape host discrimination after leaving the nest, but the role of acoustic signals in host deception remained unclear. We examined whether baywing parents are able to distinguish between begging calls of mimetic and non-mimetic fledglings and whether screaming cowbirds can trick host parents by vocally resembling host young. We conducted a field playback experiment using fledgling calls of screaming cowbird (mimetic), shiny cowbird (M. bonariensis; non-mimetic) and baywing (conspecific control) in the absence of any visual stimuli. Baywings were significantly less responsive to non-mimetic shiny cowbird calls than to the other call types and more responsive to screaming cowbird calls than to conspecific calls. The results support the idea that baywings cue in on species-specific acoustic signals for fledgling recognition and that vocal similarity to host young in screaming cowbirds plays a role in host deception. The observed host preference for screaming cowbird over conspecific calls further suggests that vocal mimicry in brood parasites could be reinforced by the expression of acoustic features that either act as a supernormal stimulus or exploit host’s pre-existing sensory biases. Significance statement Brood-parasitic screaming cowbird juveniles closely resemble those of its primary host, the greyish baywing, in plumage appearance and vocalizations. Using a field playback experiment, we studied the ability of adult baywings to discriminate against foreign juveniles based on vocal cues, in the absence of any visual stimuli. Baywings responded differentially to own-species and non-mimetic calls, and even more, they were more attracted to screaming cowbird calls than to those of conspecific juveniles. The study supports the idea that baywings use acoustic signals to distinguish between their own and foreign fledglings, thus favouring the evolution of vocal mimicry in its specialist brood parasite. Moreover, the results suggest that screaming cowbird fledglings would be even more effective than host’s own young in attracting parental attention through their begging calls.
 
Top-cited authors
Kathryn (Kate) P Huyvaert
  • Washington State University
Jens Krause
  • Humboldt-Universität zu Berlin
Darren P Croft
  • University of Exeter
Anders Pape Moller
  • French National Centre for Scientific Research
Alexander D M Wilson
  • University of Plymouth