Evolutionary Ecology

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(Left) Phylogenetic overview of larval life history across the insect order Diptera. Circles indicate whether a clade contains mostly or exclusively aquatic species (white), peripherally aquatic or a mixture of aquatic and terrestrial species (grey), or mostly terrestrial species (black). Clades marked with a black star are viviparous and bear live offspring, while clades marked with an asterisk (*) are addressed in this review. Cladogram modified from Dobson (2013). (Right) Overview of the major groups of dipteran disease vectors of focus in this review. Information regarding each group’s adult life history, primary vectored pathogens, and associations with non-pathogenic microbes is provided. Groups marked with both a droplet and flower icon contain hematophagous and non-biting species, while groups marked with only a droplet or flower contain only obligately hematophagous or non-biting species, respectively. Icons with horizontal arrows indicate groups for which microbiota are known to be acquired horizontally from the environment, while icons with vertical arrows indicate groups with highly specific associations with bacterial endosymbionts that are vertically transmitted from mother to offspring. Icons containing letters indicate groups with known functions for microbiota in host physiology (N = nutrition; I = immunity; R = reproduction; D = growth and development; V = vector competence). Question marks indicate groups for which microbiota function is poorly elucidated. All groups contain species that are known to be naturally infected by the intracellular bacterium Wolbachia. Figure created with BioRender.com
Vector-borne diseases constitute a major global public health threat. The most significant arthropod disease vectors are predominantly comprised of members of the insect order Diptera (true flies), which have long been the focus of research into host–pathogen dynamics. Recent studies have revealed the underappreciated diversity and function of dipteran-associated gut microbial communities, with important implications for dipteran physiology, ecology, and pathogen transmission. However, the effective parameterization of these aspects into epidemiological models will require a comprehensive study of microbe-dipteran interactions across vectors and related species. Here, we synthesize recent research into microbial communities associated with major families of dipteran vectors and highlight the importance of development and expansion of experimentally tractable models across Diptera towards understanding the functional roles of the gut microbiota in modulating disease transmission. We then posit why further study of these and other dipteran insects is not only essential to a comprehensive understanding of how to integrate vector-microbiota interactions into existing epidemiological frameworks, but our understanding of the ecology and evolution of animal-microbe symbiosis more broadly.
Map of southeast Norway showing the extent of the study area and the positions of the 42 localities (filled circles) where the 77 boreal owl treatment nests occurred
The probability that a boreal owl nest was predated as a function of time elapsed from nest box relocation to start of egg laying, with the curve describing the logistic regression model, separately for the box in the original nest tree (grey columns, solid hatched curve, thin hatched lines for 95% CI) and a box in a new nest tree for the season (white columns, solid curve, thin lines for 95% CI), for the average distance from the new nest tree to the original one (177 m). Time since nest box relocation ranged 10–229 days, and is grouped in 50 days units. The parameter estimates are reported in Table 2
Distribution of boreal owl nests that were predated (filled circles) and nests that escaped predation (open circles) in relation to time elapsed from nest box relocation to start of egg laying and to distance between the two boxes in a dyad, for boxes in the original nest tree (upper panel) and boxes in the new nest tree for the season (lower panel)
The probability that a boreal owl nest in the box in the original nest tree was predated as a function of the number of years elapsed since the successful nesting in this tree, with the solid curve describing the logistic regression model, and the thin curves the 95% CI. The bars denote the distribution of cases in which the nest was predated (lower row) or escaped predation (upper row), and the dotted horizontal line shows the probability of nest predation in the box in the new tree
A fundamental problem for any animal is how to weigh the benefits of making a rapid decision against the costs of making a poor decision, because time for detecting and evaluating all options is often restricted. For nest-site selection in birds, an important cost of a speedy decision would be nest predation, which is a major factor lowering reproductive success. I tested whether shorter time available for assessment of nest sites would lead to a decision with higher probability of nest predation. Where boreal owls (Aegolius funereus) had nested successfully in a box in the previous season, I manipulated nest box availability by offering a dyad of nest boxes. One box (kept or exchanged) was in the original nest tree and one box (new or taken from the original tree) was in a new tree for the season, each box containing either “post-nesting residue” from the successful nesting or new wood shavings. Hence, the owls could assess the risk of nest predation at a familiar site relative to that at a new site. The timing of nest box installation and relocation was such that time for assessment varied among localities, from the whole non-breeding season to just a few days prior to laying in spring. Owls that had had longer time in which to make their assessment and selection were less likely to have their nest predated by pine martens (Martes martes). Boreal owls are non-migratory and probably gained information on the relative safety of the two options by a Bayesian-like updating process in the days, weeks or months before the decision had to be made. A migratory cavity-nester exposed to the same landscape of nest predation would be more time-constrained and forced to rely on the win-stay loose-shift tactic, which underperforms relative to Bayesian-like updating.
Allometry—the study of proportional growth of body parts, and the relationship of body size to an organism’s morphology, physiology and behaviour—is a fundamental influencer of ecological and evolutionary diversity. Allometric studies can focus on scaling across an individual's development (ontogenetic allometry), among individuals at the same developmental stage (static allometry), and among species (evolutionary allometry). The key assumption in allometry is that an organism’s body size is a critical factor in shaping its biology, so biological scaling underpins biological diversity. This commentary accompanies a special issue that collates original research papers on the wide-ranging ecological and evolutionary implications of biological scaling. We discuss the common themes uniting each contribution, such as how ontogenetic allometry facilitates evolutionary allometry, how size influences feeding performance and trophic niche, methodology in allometry and size estimation, and allometry in sexual selection. In doing so we highlight areas of particular need for future studies to better understand the role of allometry in evolutionary ecology.
Distribution map of Phrynosomatidae, with county sampling localities of specimens included in this study indicated by circled. Range data are from Roll et al. (2017)
Diagrams of measurements taken on different bones including the length of the dental row of the maxilla (LDR); length of the dental row of the dentary bone (LDR); the greatest length (GL), smallest width (SW), and posterior width (PW) of the frontal bone; the greatest width between the ventrolateral crests (GW) and greatest length of the table (GL) on the parietal bone; the greatest height of the quadrate bone (GH); the greatest width of the occipital condyle on the occipital complex (WC); the width of the retro-articular process of the articular bone (WR); the height of the glenoid cavity of the scapulocoracoid (HG); the greatest length of the femur (GL); the greatest length of the humerus (GL); the height of the acetabular fossa of the pelvis (HA); and the greatest length of the ilium crest (GL)
Framework through which cross-validation tests for the accuracy of each body-size estimation equation was assessed. The numbers correspond to the following body-size estimation questions we sought to address: (1) Can allometries from a species accurately estimate body size within that species? (2) Can allometries from a species accurately estimate body size within that genus? (3) Can allometries from a species accurately estimate body size within that family? (4) Can allometries from a genus accurately estimate body size within a species? (5) Can allometries from a genus accurately estimate body size within that genus? (6) Can allometries from a genus accurately estimate body size within that family? (7) Can allometries from a subfamily accurately estimate body size within that subfamily? (8) Can allometries from a subfamily accurately estimate body size within that family? (9) Can allometries from a family accurately estimate body size within a species? (10) Can allometries from a family accurately estimate body size within a genus? (11) Can allometries from a family accurately estimate body size within that family?
Absolute differences from actual SVL for each genus resulting from cross-validation predictions for datasets six (non-S. occidentalis phrynosomatids) and seven (non-Sceloporus phrynosomatids)
Allometric relationships in the traditional sense among different phrynosomatid genera for each measurement
Body size is an important life history trait that for fossils can be reconstructed by utilizing scaling relationships between body size and measurements on isolated bones from extant taxa. Allometry, which describes the scaling relationship between such a measurement and body size, has traditionally been thought of as constrained, meaning that evolutionary allometries should follow the same trajectories as ontogenetic and static allometries. However, if allometries are evolving it may be difficult to accurately estimate body size for extinct taxa or fossils that cannot be identified to low taxonomic levels. Knowing the degree to which the allometric relationships of features are evolutionarily constrained therefore has implications for studying the fossil record and can also provide insight into morphological evolution. We use phrynosomatid lizards as a case study for investigating scaling relationships at different taxonomic levels. We examined scaling relationships between body size, represented as snout-vent length (SVL), and 15 skeletal measurements taken from 188 phrynosomatid lizards with 30 species represented. For each measurement, we developed species-level, genus-level, subfamily-level, and family-level linear models. We used these models to predict SVL in cross-validation tests and determine which models and measurements produced the most accurate body size predictions. Generally, predictions from congeneric species accurately reconstructed body size, but some measurements also exhibited conserved scaling relationships across phrynosomatids and appear to serve as good family-wide predictors for body size. We found that static allometries are more similar to evolutionary allometries at the genus-level than to family-level evolutionary allometries. Differences between evolutionary allometries at the genus and family-level appear to be driven by Phrynosoma, as measurements on several cranioskeletal elements are highly divergent. Our work sets a foundation for understanding allometric relationships across Phrynosomatidae and provides a framework for examining trends in body size based on evidence from the fossil record.
Landscape structures drive biogeographic patterns and population connectivity of animals distributed across diverse biotopes. Here, we provide a fresh insight on the impact of five landscape types in East Asia on the phylogeography and acoustic variability of the widespread Mongolian Toad, Strauchbufo raddei. For the first time, we reconstructed the biogeography of S. raddei over the species’ entire range throughout East Asia (N = 293; assembled up to 2,613 bp of concatenated CR-COI-12S rRNA-16S rRNA) using fossil-based molecular dating and genetic connectivity assessments. In addition, we addressed past population dynamics in relation to landscape types, and geographic variations in release calls for the clades occurring in the steppes of northern Mongolia and the Amur River basin (N = 147). Our results recovered two separate ancestors of S. raddei in East Asia, supporting a basal split between the northeastern and southern lineages in the Middle Miocene, c. 9.48 – 13.77 Mya. Ancestral range estimates suggested a Late Miocene radiation within the northeastern lineage, likely due to aridity-induced vicariance and dispersal from the central Asian steppes, c. 7.89 (5.25 – 11.50) Mya. The southern lineage emerged subsequently from glacial refugia, c. 6.84 (3.48 – 2.63) Mya, expanding northward and crossing the Gobi Desert and current-day Mongolia, c. 2.60 (1.15 – 3.72) Mya. At the exception of the pre-Tibetan Plateau clade, our reconstruction of migration trajectories highlighted the presence of effective gene flow across other landscapes, notably among the central and northeastern Chinese clades in the habitats defined as steppe, river basin and canyon. Significant variation in release calls between the clades in northern Mongolia and the Amur River Basin reflected the isolation between the two clades, and supported the presence of a northern refugium and post-glacial expansion of the southern lineage into northwestern Mongolia. In contrast with prior studies, our finding indicates that release calls can reflect phylogeographic patterns.
Framework in which we discuss the potential role of infection risk on the evolution of migration allopatry between juvenile and adults. Grey arrows comprise the four main drivers of migration. The disease arrow is expanded to detail the four disease mechanisms thought to play a role in shaping migration strategies of which migration allopatry is one. The four main variants of migration allopatry, or instances wherein juveniles and adults have differing migration strategies, are presented. This includes oversummering as the most extreme case of migration allopatry, where juvenile birds forego migration. To also showcase alternative explanations to disease risk as an ultimate explanation for age-differential migration allopatry, we present other proximate explanations for oversummering. Avian silhouettes generated by M. Wille
Juvenile animals are generally more prone to parasite infection than adults, which may have driven the evolution of different types of age-dependent migration strategies. We distinguish four different types of such “migration allopatry” strategies. Image of Wood Thrush was photographed by, and shared with permission from Mike Melton, Ruddy Turnstone and Sharp-tailed Sandpiper were photographed by, and shared with permission from Kerry Vickers, Honey Buzzard was photographed by and shared with permission from Magnus Hellström, Short-toed Snake Eagle was photographed by Lehava Kiryat Shmona Pikiwiki Israel and distributed under a CC BY 2.5 licence, Eleonora’s Falcon was distributed by Conselleria de Medi Ambient i Mobilitat, Govern des Illes Balears under a CC-BY-SA 3.0 licence, Greater Yellow-legs was photographed by Alan D. Wilson and distributed under a CC BY-SA 2.5, Red Knot was photographed by, and is shared with permission from Sandy Horne
Seasonal long-distance migratory behaviour of trillions of animals may in part have evolved to reduce parasite infection risk, and the fitness costs that may come with these infections. This may apply to a diversity of vertebrate migration strategies that can sometimes be observed within species and may often be age-dependent. Herein we review some common age-related variations in migration strategy, discussing why in some animal species juveniles preferentially forego or otherwise rearrange their migrations as compared to adults, potentially as an either immediate (proximate) or anticipatory (ultimate) response to infection risk and disease. We notably focus on the phenomenon of “oversummering”, where juveniles abstain from migration to the breeding grounds. This strategy is particularly prevalent amongst migratory shorebirds and has thus far received little attention as a strategy to reduce parasite infection rate, while comparative intra-specific research approaches have strong potential to elucidate the drivers of differential behavioural strategies.
a Panel a depicts a two-dimensional trait space. The dark area in the center represents the centroid of the community distribution; the colored dots represent the position of populations of different species in the community in the two-dimensional space: Green dots represent resident species in the community, with the size reflecting relative abundance; grey dots represent introduced species that failed to establish; blue dots represent species that are introduced and become naturalized; purple dots represent species that are introduced and become invasive. The relative size of the dots indicates the population size. b Panel b depicts the phylogenetic relatedness and position along the two-dimensional trait axes for introduced species across a range of different potential outcomes: naturalized, invasive and failed to establish along with the hypothesized phylogenetic relatedness of the species. For example, failed species (those that did not establish into the community) are outside the current EoTS of the community trait distribution and are more distantly related. c Panel c depicts how mating between distinct populations following their introduction into a community can create a population with distinct trait profiles that, following subsequent selection, reside at the EoTS. The left most panel: blue and red dots signify geographically distinct populations introduced into the new range and their position in the two-dimensional trait space; the middle panel represents the admixture of the two distinct populations in the introduced range (purple dots); the right-most panel: admixed individuals with traits at the EoTS in the introduced range are, according to this model, destined to become invasive.
The ecological and evolutionary processes that allow alien species to establish and dominate native communities (i.e., become invasive) have been a rich area of research. Past areas of inquiry have included identifying the traits necessary to invade a community and/or determining how phylogenetic relatedness of the introduced species with the resident community can promote invasive success. Yet despite decades of research, little consensus exists about why particular species successfully invade native communities while others do not. Here we develop a conceptual framework for why only certain introduced species become invasive: optimal differentiation to the edge of trait space (EoTS). We posit that optimal differentiation leading to successful invasion into a community requires that the multi-dimensional trait space of the introduced species exists at the edge of the multi-dimensional trait space of the native community. Species that possess traits that are too different cannot enter the community because of environmental filtering, while species that are too similar will either become integrated into the community but not take over or alternatively never establish. We apply this conceptual framework to species functional traits and discuss how both genetic processes and phylogenetic processes may also result in optimal differentiation to EoTS.
An example of ancestral character reconstruction of the presence/absence of forked tails in swallows and martins (Aves: Hirundininae) using the functions ‘plotTree’ in the R package ‘phytools’ (Revell 2012). Black and white circles in tips indicate birds with forked tails and forkless tails (i.e., square tails), respectively. Likewise, the proportions of black and white in nodes indicate the probability of an ancestral state with and without forked tails, respectively. Species names in grey (black) correspond to species with sexual plumage monomorphism (dimorphism)
The most likely evolutionary transition A between prey size and social foraging and B between the index of extrapair mating opportunities and social foraging in the subfamily Hirundininae. Prey size and social foraging evolved in a dependent manner. Model-averaged transition rates, which are reflected by arrow size, are depicted
The most likely evolutionary transition between the presence and absence of forked tails in relation to sexual plumage dimorphism (see text) in the subfamily Hirundininae. Model-averaged transition rates, which are reflected by arrow size, are depicted
The most likely evolutionary transition between the presence and absence of forked tails in relation to the index of extrapair mating opportunities (see text) in the subfamily Hirundininae. Model-averaged transition rates, which are reflected by arrow size, are depicted
Evolutionary drivers of the gain and loss of ornamentation are often unclear even for classic ornamentation such as swallows’ tails, because macroevolutionary analysis, which is needed to clarify the factors responsible for the transition, is rarely conducted. Some behavioural experiments support the hypothesis that sexual selection is responsible for the evolution of “forked” tails, while others support the hypothesis that foraging on large prey favours the evolution of forked tails. However, empirical tests of these hypotheses used already-ornamented species and macroevolutionary studies of forked/forkless tails, which is critical for inferring the evolutionary forces driving the transition between the presence and absence of ornamentation, are still lacking. Here, using a clade of swallows and martins (Aves: Hirundininae), we examined the evolutionary transition between forkless and forked tails in relation to measures of foraging mode and sexual selection. We found replicated evolution of forkless tails from forked tails, all in clades with sexually monomorphic plumage. Furthermore, we detected correlated evolution of tail shape (i.e., forkless/forked) and extrapair mating opportunity, measured as incubation type which is tightly linked to extrapair paternity both within and among species. A transition from forked to forkless tails was less likely to occur than the reverse transition when extrapair mating opportunities were readily available, but not when extrapair mating opportunities were limited. In contrast, the tail shape was more likely to evolve independently with prey size (i.e., small/large) and social foraging behaviour (i.e., social/solitary foraging). These findings indicate that the intensity of sexual selection, rather than foraging mode, explains the evolutionary transition between the presence and absence of tail ornamentation, questioning the widespread perspective that capturing large prey is an evolutionary force driving and maintaining forked tails.
Hypothetical predictions for morphological divergence under different scenarios. Three hypothetical scenarios expected under extreme parallel ecological selection, extremely parallel character displacement in response to reinforcement selection, and introgression to an extent that populations converge. These are only three of many possible patterns of divergence (see Supplementary Material 1). Bars represent mean values of morphological traits, with one population being represented by each bar. While the white areas of the graph depict allopatric populations, the grey area includes co-existing populations. ‘N. allo.’ stands for northern allopatry, ‘Symp.’ stands for sympatry and ‘S. allo.’ stands for southern allopatry. Two hypothetical transects are depicted side by side. A: Scenario 1, parallel ecological selection between host races. This scenario would be expected e.g. for ecologically important traits where natural selection imposed by the environment provided by the host differ. B: Scenario 2, parallel reproductive character displacement. This pattern could arise e.g. if a character under sexual selection would be reinforced by maladaptive hybridization in a parallel manner in both transects. C: Scenario 3, hybridization in sympatric areas is causing introgression resulting in reduced divergence in these areas. Whereas these explanations are not the only possible explanations, they were chosen as we expect some degree of parallelism to result from the adaptation to a similar environment and potentially some gene flow in the sympatric regions. Alternative explanations to the pattern in C would be clinal host plant independent variation, for instance
Methods A: Map showing distribution of the T. conura host races, with the distribution of CH-flies infesting Cirsium heterophyllum depicted in purple and that of CO-flies infesting Cirsium oleraceum depicted in green. Sampling locations are indicated by red circles. B: Dorsal photograph of a T. conura wing annotated with 15 landmarks used to analyze wing shape. C: Cirsium heterophyllum. D: Cirsium oleraceum. Principal component analyses are used for illustrating how the host races of T. conura differ in morphology using an unguided approach. Both morphological traits including including body length, ovipositor length, wing length, wing width and melanisation ratio as well as wing shape traits in form of six relative warps were included. E: For female flies, where the ovipositor also was included in the analysis. F: For male flies
A subset of trait measurements of female T. conura divided by host race, co-existence and geographic setting. Host race is illustrated by color, with purple corresponding to CH-flies infesting the purple melancholy thistle and green to CO-flies infesting the white cabbage thistle. The grey shaded area in the center denotes sympatric populations (triangular mean markers). X axis labels represent which state of co-existence the fly population is in. ‘N.allo.’ stands for Northern allopatric, ‘Symp.’ stands for sympatric and ‘S. allo.’ stands for Southern allopatric. West and East headers represent from which side of the Baltic Sea the populations are sampled. A: Mean values of female T. conura body length per population. B: Mean values of female T. conura ovipositor length per population. C: Mean values of female T. conura wing length per population. D: Mean values of female T. conura wing width per population. All plots portray mean trait values with 95% confidence interval bars of the mean. The traits depicted in the figure were chosen to illustrate the broad range of different divergence scenarios. All other traits and data on male divergence are available in the supplementary material (Females: Fig. S6; Males: Fig. S7-S10)
Linear discriminant function analyses and bootstrapped loadings. a and b: LDAs illustrating differences in how the host races group along the first two linear discriminant axes in Western (a) and Eastern (b) flies. c: The morphological traits loading on the two first discriminant axes for Eastern and Western flies. Colors illustrate how much the standard error diverges from zero based on 100 000 bootstrap replications. Loading that surpass zero are depicted in red colors whereas loadings significantly lower than zero are colored in blue. Plots and analyses are based on female fly morphology. Findings based on males are reported and illustrated in Supplementary Fig. 12
Adaptation to new ecological niches is known to spur population diversification and may lead to speciation if gene flow is ceased. While adaptation to the same ecological niche is expected to be parallel, it is more difficult to predict whether selection against maladaptive hybridization in secondary sympatry results in parallel divergence also in traits that are not directly related to the ecological niches. Such parallelisms in response to selection for reproductive isolation can be identified through estimating parallelism in reproductive character displacement across different zones of secondary contact. Here, we use a host shift in the phytophagous peacock fly Tephritis conura, with both host races represented in two geographically separate areas East and West of the Baltic Sea to investigate convergence in morphological adaptations. We asked (i) if there are consistent morphological adaptations to a host plant shift and (ii) if the response to secondary sympatry with the alternate host race is parallel across contact zones. We found surprisingly low and variable, albeit significant, divergence between host races. Only one trait, the length of the female ovipositor, which serves an important function in the interaction with the hosts, was consistently different between host races. Instead, co-existence with the other host race significantly affected the degree of morphological divergence, but the divergence was largely driven by different traits in different contact zones. Thus, local stochastic fixation or reinforcement could generate trait divergence, and additional evidence is needed to conclude whether divergence is locally adaptive.
Resistance and genotypic diversity significantly increased after recombination occurred in Hackberry Lake, but remained constant in Midland Lake. Figure 1A and C show mean resistance of isofemale lines collected at two time points: ephippial females in December 2015 (‘Parent’) and offspring hatched from those ephippia (‘Offspring’). Figure 1B and D show mean resistance of offspring hatched from ephippia produced in December 2015 (‘Offspring’) and individuals collected in Spring 2016 after the active population was refounded from the egg bank (‘Egg bank’). Phenotype comparisons are paired by experimental blocks (one block shown in A, another in B, etc.), so resistance in parents and egg bank animals cannot be directly compared. The violin plot outlines illustrate kernel probability density, i.e., the width of the shaded area represents the proportion of the data located there. Fig E and F show the observed diversity measures and bootstrapped 95% confidence intervals. The bootstrapped estimates often skew from the observed measures, and confidence intervals were centered around the observed diversity measures as recommended by Grünwald et al. 2017
Multilocus genotype 50 (i.e., MLG.50, left plot) was the most prevalent genotype in the Hackberry parent lake-group. It was also on average less resistant to infection by Metschnikowia bicuspidata compared to the majority of other, co-existing genotypes. Multilocus genotype 57 (i.e., MLG.57, right plot) was the most prevalent genotype in the Midland egg bank lake-group even though it was not detected in the fall prior. This is evidence of temporal gene flow, i.e., that resting eggs produced during earlier years help recolonize lakes in the spring. MLG.57 does not have an extremely susceptible or resistant phenotype compared to other, coexisting genotypes
Both populations showed moderate heritability of resistance (h²); the Hackberry Lake population (orange) had an h² of approximately 0.52, while the Midland Lake population (green) had h² of approximately 0.33. Midland scored lower due to low variance (i.e., high similarity) in resistance for both parents and offspring of the population. Narrow-sense heritability for both lake populations was found by doubling the slope of the linear regression of parent vs. offspring resistance
Infectious disease can threaten host populations. Hosts can rapidly evolve resistance during epidemics, with this evolution often modulated by fitness trade-offs (e.g., between resistance and fecundity). However, many organisms switch between asexual and sexual reproduction, and this shift in reproductive strategy can also alter how resistance in host populations persists through time. Recombination can shuffle alleles selected for during an asexual phase, uncoupling the combinations of alleles that facilitated resistance to parasites and altering the distribution of resistance phenotypes in populations. Furthermore, in host species that produce diapausing propagules (e.g., seeds, spores, or resting eggs) after sex, accumulation of propagules into and gene flow out of a germ bank introduce allele combinations from past populations. Thus, recombination and gene flow might shift populations away from the trait distribution reached after selection by parasites. To understand how recombination and gene flow alter host population resistance, we tracked the genotypic diversity and resistance distributions of two wild populations of cyclical parthenogens. In one population, resistance and genetic diversity increased after recombination whereas, in the other, recombination did not shift already high resistance and genetic diversity. In both lakes, resistance remained high after temporal gene flow. This observation surprised us: due to costs to resistance imposed by a fecundity-resistance trade-off, we expected that high population resistance would be a transient state that would be eroded through time by recombination and gene flow. Instead, low resistance was the transient state, while recombination and gene flow re-established or maintained high resistance to this virulent parasite. We propose this outcome may have been driven by the joint influence of fitness trade-offs, genetic slippage after recombination, and temporal gene flow via the egg bank.
Hypothetical distribution of mutational effects. We often expect deleterious mutations (negative fitness effects) to appear more frequently than beneficial mutations (positive fitness effects). Available evidence suggests both types of mutations may have skewed distributions, where weak effects are common and strong effects are rare. Under MA, the effective population size (Ne) will determine which mutations will behave neutrally. As Ne increases, a larger fraction of mutations will be subject to effective selection, i.e., deleterious (beneficial) mutations would be less (more) likely to fix than the neutral expectation
The fitness landscape concept. Lighter shades indicate higher fitness. (a) In a well-adapted genotype (+ symbol) we expect the vast majority of mutations to be deleterious (red arrows). (b) In a poorly adapted genotype, the same genetic changes are more likely to be beneficial (green arrows)
All adaptive alleles in existence today began as mutations, but a common view in ecology, evolution, and genetics is that non-neutral mutations are much more likely to be deleterious than beneficial and will be removed by purifying selection. By dramatically limiting the effectiveness of selection in experimental mutation accumulation lines, multiple studies have shown that new mutations cause a detectable reduction in mean fitness. However, a number of exceptions to this pattern have now been observed in multiple species, including in highly replicated, intensive analyses. We briefly review these cases and discuss possible explanations for the inconsistent fitness outcomes of mutation accumulation experiments. We propose that variation in the outcomes of these studies is of interest and understanding the underlying causes of these diverse results will help shed light on fundamental questions about the evolutionary role of mutations.
Set up of the experimental tank (view from above). Fish from the predation treatment were allowed to swim freely in the tank (N = 180), whereas control fish were placed in 11 L transparent tanks (N = 16 each, shown in dashed squares) to provide visual cues, with a filter pump that allowed water to get into the tank to provide olfactory cues. Water flow from the pumps is indicated with arrows. A predatory cichlid was placed at the deepest area with a clay pipe for shelter. Different shades of blue represent different depths
Body size for (a) females and (b) males for control (grey) and predation (purple) treatment fish measured before (T0; light colours) and after (T1; dark colours) the predation event. The white box indicates the median and interquartile range (IQR), whiskers extend to 1.5*IQR. Black data points indicate values outside the 1.5*IQR. The violin shapes show the distribution of the data
Differences in brain size between the control (grey circles) and predation (purple triangles) treatments for (a) females and (b) males. Model predictions are plotted as the best fit line with 95% CI
Cognitive and sensory abilities are vital in affecting survival under predation risk, leading to selection on brain anatomy. However, how exactly predation and brain evolution are linked has not yet been resolved, as current empirical evidence is inconclusive. This may be due to predation pressure having different effects across life stages and/or due to confounding factors in ecological comparisons of predation pressure. Here, we used adult guppies ( Poecilia reticulata ) to experimentally test how direct predation during adulthood would impact the relative brain size and brain anatomy of surviving individuals to examine if predators selectively remove individuals with specific brain morphology. To this end, we compared fish surviving predation to control fish, which were exposed to visual and olfactory predator cues but could not be predated on. We found that predation impacted the relative size of female brains. However, this effect was dependent on body size, as larger female survivors showed relatively larger brains, while smaller survivors showed relatively smaller brains when compared to control females. We found no differences in male relative brain size between survivors and controls, nor for any specific relative brain region sizes for either sex. Our results corroborate the important, yet complex, role of predation as an important driver of variation in brain size.
Model system and experimental protocol. a Life cycle of the microsporidian parasite Edhazardia aedis and of its host Aedes aegypti
(modified from Koella and Agnew 1999). The parasite has a fixed developmental program alternating the production of two spore types. The production of a new batch of uninucleate spores after the infection of a juvenile requires first the production of binucleate spores. “Shortcut” horizontal transmission occurs when juveniles (larvae or pupae) die in the aquatic environment; vertical transmission occurs via infected females laying infected eggs. Once the new generation of vertically infected larvae emerges, they either die and new events of horizontal transmission occur, or they emerge to become adults with the potential for vertical transmission. b Protocol of the experimental evolution part of the study. At each generation, uninfected larvae from the stock colony were horizontally infected with uninucleate spores obtained by hatching eggs and harvesting the vertically infected larvae from the previous generation. Infected larvae were raised under permissive high-food conditions (red, Evo HF) or restricted low-food conditions (blue, Evo LF), which resulted in fast or slow development into adults and thereby changing the match with parasite development. The rearing of the vertically infected larvae and the infection of the next generation followed a standardized protocol (main text)
Transmission components of the parasite. a For the horizontal transmission we measured four transmission proxies: The number of juveniles not emerging, the probability of these individuals carrying uninucleate spores, the uninucleate spore load and the juvenile survival. b For vertical transmission we measured five transmission proxies: The number of females emerging, the probability of these females carrying binucleate spores, binucleate spore load, wing size (fecundity) and longevity
Means of the a–e vertical and f–i horizontal parasite transmission components. a The number of adul females emerging, b the probability of the females carrying binucleate spores, c the binucleate spore load (spores/0.9μL), d the wing size (in cm; proxy for fecundity and number of eggs laid) and e the longevity (in days). f The number of juveniles not emerging and dying in the water, g the probability of the dead juveniles carrying uninucleate spores, h the uninucleate spore load of the juveniles (spores/0.9μL) and i their survival (in days). Big symbols and bars are the overall mean and standard errors, small symbols are the mean for each parasite selection line. Red and blue symbols represent evolution in permissive (Evo HF) and restricted ecological (Evo LF) conditions respectively. Full and empty symbols are the conditions of the final test, corresponding to high (Test HF) and low (Test LF) food levels
PCA for the a vertical and b horizontal transmission components. The first two principal component axes (PC1 and PC2) are shown. Each arrow represents a single trait/component used for the PCA. The length and the direction of the arrow indicate which vertical and horizontal transmission traits/components are driving the separation between treatments. Each point represents the average value of a given parasite line in multivariate space: Evolved in permissive (Evo HF, red) or restricted (Evo LF, blue) ecological conditions; tested in the high (Test HF, full circles and solid lines) or low (Test LF, empty circles and dashed lines) food. The ellipses are the 95% containment probability region for the four treatments
Reduction of the several traits measured for the horizontal and vertical transmission components to one dimension (PC1) after PCA and multivariate analysis. Synthetic measurement of a parasite vertical and b horizontal transmission potential. For visualization, PC1 vertical transmission values were multiplied by − 1, in order to have positive values corresponding to higher transmission. c Relationship between the synthetic measurement of horizontal and vertical transmission. Red and blue symbols represent evolution in permissive (Evo HF) and restricted (Evo LF) ecological conditions respectively. Full and empty symbols are the conditions of the final test, corresponding to high (Test HF) and low (Test LF) food levels. Big symbols and bars are the overall mean and standard errors, small symbols are the mean for each parasite selection line
Ecological conditions may greatly affect the relative importance of vertical and horizontal transmission, in particular for parasites with a mixed mode of transmission. Resource availability is one important environmental factor, affecting host growth and fecundity, but also the parasite’s own development. The consequences for the potential of vertical and horizontal transmission and for the evolution of transmission mode are largely unknown. We let the mixed-mode microsporidian parasite Edhazardia aedis evolve on its mosquito host Aedes aegypti under high-food or low-food conditions, representing permissive and restricted conditions. These alter the timing of development of infected larvae and thereby the probabilities for the parasites to enter the vertical or horizontal transmission pathways. After 10 generations, evolved parasites were assayed under the two food levels. There was an ecological trade-off between transmission modes, mediated by nutrient effects on host development, resulting in a higher vertical transmission (VT) potential under high-food and a higher horizontal transmission (HT) potential under low-food test conditions. Evolution under high food increased the VT potential of the parasite, particularly if it was tested at low food. This involved higher probability of carrying binucleate spores for the emerging females, greater fecundity and a longer life compared to parasites that were tested in the same conditions but had evolved under low food. The changes are related to the developmental regulation and switch in the production of two spore types, affecting investment in VT or HT. In contrast, the HT potential remained relatively unaffected by the parasite’s evolutionary history, suggesting that, within our experiential design, the VT mode evolved independently of the HT mode. Our work illustrates the possible links between resource availability, within-host developmental processes and the evolution of parasite transmission investment. Future work, theoretical and experimental, should scale up from within-host to between-host levels, including eco-evolutionary and epidemiological dynamics.
Experimental design to test for the average fitness effects of somatic mutations accumulating in stems of Mimulus guttatus during vegetative growth. A proportion of somatic mutations accumulating during stem growth (dark blue arrows) is made homozygous after within-flower (autogamous) self-pollinations, while all somatic mutations will be heterozygous after between-stem (geitonogamous) self-pollinations. Comparison of the mean fitness of autogamous seedlings (w¯k(A)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\overline{w} }_{k(A)}$$\end{document}) to geitonogamous seedlings from the same stem (w¯k(G)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\overline{w} }_{k(G)}$$\end{document}) provides an estimate of the average fitness effects of somatic mutations unique to each stem (δAD(k) = w¯k(A)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\overline{w} }_{k(A)}$$\end{document} − w¯k(G)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\overline{w} }_{k(G)}$$\end{document})
Estimates of δAD(k) for fourteen different stems (ramets) of Mimulus guttatus from two separate experiments (Experiment 1–blue bars; Experiment 2–orange bars) based on mean progeny fitness after autogamous w¯k(A)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\overline{w} }_{k(A)}$$\end{document} and geitonogamous w¯k(G)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\overline{w} }_{k(G)}$$\end{document} self-pollinations (δAD(k) = w¯k(A)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\overline{w} }_{k(A)}$$\end{document} − w¯k(G)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\overline{w} }_{k(G)}$$\end{document}). Horizontal lines represent standard errors. Asterisks indicate values of δAD(k) that are significantly different from zero based on the t value, calculated as t=δAD(k)/SE\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$t={\delta }_{AD(k)}/\sqrt{SE}$$\end{document} with n-1 df, where n is the mean of sample sizes for progeny from autogamy and geitonogamy. The relationship between w¯k(A)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\overline{w} }_{k(A)}$$\end{document} and w¯k(G)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\overline{w} }_{k(G)}$$\end{document} across stems is shown in Fig. S3. Means and sample sizes for progeny groups are available in Table S2 and Fig. S4 in Appendix 3
Relationships between estimates of fitness effects of somatic mutations in Mimulus guttatus, based either on the difference in fitness of progeny from autogamy and geitonogamy (δAD(k)), or the standard deviation in fitness within progeny groups from autogamy for each stem (wSD). Estimates of wSD corresponding to negative values of δAD(k) were transformed to negative values. Estimates from Experiment 1 are indicated by blue circles and from Experiment 2 are orange squares. Dashed lines indicate the separate relationships for positive and negative values of fitness estimates
The unique life form of plants promotes the accumulation of somatic mutations that can be passed to offspring in the next generation, because the same meristem cells responsible for vegetative growth also generate gametes for sexual reproduction. However, little is known about the consequences of somatic mutation accumulation for offspring fitness. We evaluate the fitness effects of somatic mutations in Mimulus guttatus by comparing progeny from self-pollinations made within the same flower (autogamy) to progeny from self-pollinations made between stems on the same plant (geitonogamy). The effects of somatic mutations are evident from this comparison, as autogamy leads to homozygosity of a proportion of somatic mutations, but progeny from geitonogamy remain heterozygous for mutations unique to each stem. In two different experiments, we find consistent fitness effects of somatic mutations from individual stems. Surprisingly, several progeny groups from autogamous crosses displayed increases in fitness compared to progeny from geitonogamy crosses, likely indicating that beneficial somatic mutations occurred in some stems. These results support the hypothesis that somatic mutations accumulate during vegetative growth, but they are filtered by different forms of selection that occur throughout development, resulting in the culling of expressed deleterious mutations and the retention of beneficial mutations.
Proportion of photos showing groups of butterflies.
Source: https://www.ukbutterflies.co.uk
Change in predation risk from signalling. As a function of time, selected combinations of dpred,dcons\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\mathrm{d}}_{\mathrm{pred}} ,{\mathrm{d}}_{\mathrm{cons}}$$\end{document}. Δpred=Δcons=5%\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\Delta }_{\mathrm{pred}}={\Delta }_{\mathrm{cons}}=5\%$$\end{document} for all graphs. Predation is reduced as a result of signalling when the result is below 0
Butterflies are frequently conspicuous. The function of this conspicuousness is understudied and may vary between species or family. Aposematism has frequently been proposed, as well as sexual signalling; even allowing for other functions, gaps seem to remain. Butterflies are also frequently social and many species will aggregate in large clusters. Here I propose that striking colourations may have evolved in some species to improve visibility to conspecifics, even if it also increases visibility to predators and even if colouration provides no other benefit, merely because the improved visibility increases the probability of being part of a cluster which provides protection against predation through dilution. As well as showing the potential existence of a new mechanism which can lead to bright colour occurring in flying insects, the proposed mechanism may provide an explanation to the mimicry rings of Heliconius butterflies that is superior to Müllerian mimicry. Several features of Heliconius rings seem to contradict the logic and premises of Müllerian mimicry, but would be predicted by, or consistent with, the hypothesis that the marks on Heliconius wings are signals towards co-roosters.
Evolutionary and environmental factors influencing the outcome of parasitoid host regulation toward an early arrestment of the host development or toward a promotion of its growth. a: host feeding ecology, b: parasitoid host-utilization strategies, c: parasitoid developmental strategies, d: host quality and e: host availability
Non-exhaustive review of the literature reporting a decrease in parasitized herbivore weight or food consumption compared to unparasitized herbivores. Decrease of herbivore growth has been found in Hemipteran and Lepidopteran hosts and may yield hosts that are up to 97% smaller than unparasitized hosts
Tritrophic interactions among plants, herbivorous insects and their parasitoids have been well studied in the past four decades. Recently, a new angle has been uncovered: koinobiont parasitoids, that allow their host to keep feeding on the plant for a certain amount of time after parasitism, indirectly alter plant responses against herbivory via the many physiological changes induced in their herbivorous hosts. By affecting plant responses, parasitoids may indirectly affect the whole community of insects interacting with plants induced by parasitized herbivores and have extended effects on plant fitness. These important findings have renewed research interests on parasitoid manipulation of their host development. Parasitoids typically arrest their host development before the last instar, resulting in a lower final weight compared to unparasitized hosts. Yet, some parasitoids prolong their host development, leading to larger herbivores that consume more plant material than unparasitized ones. Furthermore, parasitoid host regulation is plastic and one parasitoid species may arrest or promote its host growth depending on the number of eggs laid, host developmental stage and species as well as environmental conditions. The consequences of plasticity in parasitoid host regulation for plant–insect interactions have received very little attention over the last two decades, particularly concerning parasitoids that promote their host growth. In this review, we first synthesize the mechanisms used by parasitoids to regulate host growth and food consumption. Then, we identify the evolutionary and environmental factors that influence the direction of parasitoid host regulation in terms of arrestment or promotion of host growth. In addition, we discuss the implication of different host regulation types for the parasitoid’s role as agent of plant indirect defence. Finally, we argue that the recent research interests about parasitoid plant-mediated interactions would strongly benefit from revival of research on the mechanisms, ecology and evolution of host regulation in parasitoids.
Mean (± SE) offspring body size and developmental time in relation to parental body size (L: large; S: small) in the parasitoid wasp Lysiphlebus fabarum.
Mean (± SE) offspring egg load and egg size in relation to parental body size (L: large; S: small) in the parasitoid wasp Lysiphlebus fabarum.
Mean (± SE) offspring emergence rate and sex ratio in relation to parental body size (L: large; S: small) in the parasitoid wasp Lysiphlebus fabarum.
Maternal and paternal effects are now acknowledged as a significant source of variation in offspring phenotypes, with potentially lifelong consequences for individuals' life histories. While a large body of evidence exists on maternal effects across animal taxa, paternal effects have been largely underestimated. The purpose of this study was to investigate non-genetic paternal effects in a parasitoid wasp, Lysiphlebus fabarum (Braconidae: Aphi-diinae), in which maternal and paternal body sizes were manipulated and mated in a cross design. Following that, early adulthood life history traits of the offspring were recorded. Large mothers produced larger offspring with quicker developmental times. This pattern was also seen when looking at effects of fathers on their offspring. Interestingly, the egg load of the offspring was influenced by paternal, but not maternal body size, suggesting direct paternal effects in this species of parasitoid wasp. Consequently, females may benefit from mating with large male, as their offspring emerge with enhanced life histories, posing indirect selection on female sexual preferences. Our findings provide insight into the relative importance of both maternal and paternal body size to the offspring early adulthood life histories and shed light on the underlying mechanisms by which offspring phenotypes have been shaped.
Population variation rates of plant P\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$P$$\end{document} and pollinator A\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$A$$\end{document}. Blue arrows indicate the density variations via other means than the mutualistic interaction, green arrows the effects of the mutualistic interaction, and red arrows the effects of intraspecific competition. Note that the plant intrinsic growth rate rP\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${r}_{P}$$\end{document} is in trade-off with the plant attractiveness α\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\alpha$$\end{document}. The parameters are described in the main text
Variation of the attractiveness ratio ααmax\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\frac{\alpha }{{\alpha }_{max}}$$\end{document} with the plant intrinsic growth rate rP\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${r}_{P}$$\end{document} depending on the trade-off strength. Continuous lines show convex trade-offs, the dashed line a linear trade-off, and dashed-dotted lines concave trade-offs
Pairwise invasibility plots (PIPs) representing the invasibility potential of a rare mutant within a resident plant population at ecological equilibrium. Grey areas indicate that the mutant relative fitness ωαm,α\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\omega \left({\alpha }_{m},\alpha \right)$$\end{document} is positive, so that it invades and replaces the resident population. In panels a and c, arrows show the direction of evolutionary trajectories. The system exhibits several singular strategies depending on the parameter values. Circles represent convergent strategies, whereas squares are non-convergent. Filled symbols represent invasible strategy, while not filled symbols are non-invasible. In panels a and b, the singular strategy is non-convergent and invasible (repellor). In panel c, the singular strategy is convergent and non-invasible (CSS). Panel d displays two strategies, one CSS and one which is non-convergent and non-invasible (Garden of Eden). Parameter values are: cA=cP=γA=γP=1\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${c}_{A}={c}_{P}={\gamma }_{A}={\gamma }_{P}=1$$\end{document}, and αmax=0.8∗αcl\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\alpha }_{max}=0.8*{\alpha }_{cl}$$\end{document}
Ecology–evolution–environment (E3\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${E}^{3}$$\end{document}) diagram representing the impact of pollinator environmental deterioration on the evolution of plant attractiveness and on pollinator (panel a) and plant (panel b) equilibrium biomass densities. White areas show parameters for which extinction occurs for either plants or pollinators. The blue intensity correlates with population densities of pollinators (panel a) or plants (panel b). Black lines show the position of singular strategies; continuous lines show convergent and non-invasible singular strategies (CSS), and dashed lines show Garden of Edens (non-invasible, divergent). Vertical black arrows (1, 2, 4, 7) display the direction of evolution. Environmental disturbance is represented by a red arrow (3). White arrows (5, 6) represent restoration attempts at different times along the evolutionary trajectory. On panel b) the red point and dotted lines represent the lowest rA\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${r}_{A}$$\end{document} and ααmax\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\frac{\alpha }{{\alpha }_{max}}$$\end{document} values for allowing a CSS, therefore the maintenance of the mutualistic interaction. This point is what we call an eco-evolutionary tipping point. Parameters values are s=2.5\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$s=2.5$$\end{document},cA=cP=γP=1\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${c}_{A}={c}_{P}={\gamma }_{P}=1$$\end{document}, γA=0.2\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\gamma }_{A}=0.2$$\end{document}, and αmax=0.8∗αcl\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\alpha }_{max}=0.8*{\alpha }_{cl}$$\end{document}. Similar E³ diagrams can be found in Dieckmann and Ferrière 2004; Ferriere and Legendre 2013
Influence of trade-off shape and mutualistic gains on eco-evolutionary dynamics. Columns differ in trade-off concavity. Lines differ in the asymmetry of mutualistic gains: in the top line (panels a, b, and c) pollinators benefit more than plants; the middle line (panels d, e, and f) shows equal gains while in the bottom line plant gains are larger (panels g, h, and i). Red point and dotted lines represent the lowest rA\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${r}_{A}$$\end{document} and ααmax\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\frac{\alpha }{{\alpha }_{max}}$$\end{document} values for allowing a CSS and the maintenance of the mutualistic interaction. Colours and lines are the same as in Fig. 4. The parameter values are cA=cP=1\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${c}_{A}={c}_{P}=1$$\end{document} and αmax=0.8∗αcl\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\alpha }_{max}=0.8*{\alpha }_{cl}$$\end{document}
With current environmental changes, evolution can rescue declining populations, but what happens to their interacting species? Mutualistic interactions can help species sustain each other when their environment worsens. However, mutualism is often costly to maintain, and evolution might counter-select it when not profitable enough. We investigate how the evolution of the investment in a mutualistic interaction by a focal species affects the persistence of the system. Specifically, using eco-evolutionary dynamics, we study the evolution of the focal species investment in the mutualistic interaction of a focal species (e.g. plant attractiveness via flower or nectar production for pollinators or carbon exudate for mycorrhizal fungi), and how it is affected by the decline of the partner population with which it is interacting. We assume an allocation trade-off so that investment in the mutualistic interaction reduces the species intrinsic growth rate. First, we investigate how evolution changes species persistence, biomass production, and the intensity of the mutualistic interaction. We show that concave trade-offs allow evolutionary convergence to stable coexistence. We next assume an external disturbance that decreases the partner population by lowering its intrinsic growth rate. Such declines result in the evolution of lower investment of the focal species in the mutualistic interaction, which eventually leads to the extinction of the partner species. With asymmetric mutualism favouring the partner, the evolutionary disappearance of the mutualistic interaction is delayed. Our results suggest that evolution may account for the current collapse of some mutualistic systems like plant-pollinator ones, and that restoration attempts should be enforced early enough to prevent potential negative effects driven by evolution.
In pursuit of pollination, a Cryptostylis subulata orchid tricks its ichneumonid wasp pollinator, Lissopimpla excelsa, into ejaculating and wasting his sperm. Sperm loss and missed mating opportunities could impose great costs on deceived pollinators’ populations – how does this relationship persist? Image courtesy of C. Young
Relative proportions of haplodiploid and not haplodiploid pollinators across different known pollination strategies for 755 species of Orchidaceae (excluding autogamous orchids; data from Van der Cingel 2001). Pollinators included Hymenoptera (haplodiploid), and Diptera, Coleoptera, Lepidoptera and birds (all not haplodiploid). Pollinator type (haplodiploid or not) appears to relate to pollination strategy. Pollination strategies that were not rewarding, but otherwise unclear were described as ‘sensory traps’
Contrasting different mechanisms for persistance: resistance, exaptation, tolerance against ‘robustness’. Citations: Resistance – ¹de Jager and Ellis 2014; Exaptation ²Schiestl and Cozzolino 2008, chemical compound example from Bohman et al. 2019; Tolerance –³Tiffin 2000; Robustness – ⁴(Kitano 2004; Whitacre 2012)
Animals and plants trick others in an extraordinary diversity of ways to gain fitness benefits. Mimicry and deception can, for example, lure prey, reduce the costs of parental care or aid in pollination–in ways that impose fitness costs on the exploited party. The evolutionary maintenance of such asymmetric relationships often relies on these costs being mitigated through counter-adaptations, low encounter rates, or indirect fitness benefits. However, these mechanisms do not always explain the evolutionary persistence of some classic deceptive interactions. Sexually deceptive pollination (in which plants trick male pollinators into mating with their flowers) has evolved multiple times independently, mainly in the southern hemisphere and especially in Australasia and Central and South America. This trickery imposes considerable costs on the males: they miss out on mating opportunities, and in some cases, waste their limited sperm on the flower. These relationships appear stable, yet in some cases there is little evidence suggesting that their persistence relies on counter-adaptations, low encounter rates, or indirect fitness benefits. So, how might these relationships persist? Here, we introduce and explore an additional hypothesis from systems biology: that some species are robust to exploitation. Robustness arises from a species’ innate traits and means they are robust against costs of exploitation. This allows species to persist where a population without those traits would not, making them ideal candidates for exploitation. We propose that this mechanism may help inform new research approaches and provide insight into how exploited species might persist.
Four general color phenotypes of Red-eyed Treefrogs (Agalychnis callidryas) that occur in Costa Rica and Panamá. The orange/blue phenotype of southeastern Costa Rica/Panamá has both blue and red on the flank and legs. See text for complete references of the extent of geographic variation of color patterns. Digital illustrations drawn from photographs by Cynthia J. Hitchcock
Brightness contrast measures for 29 individual Agalychnis callidryas sampled from 10 localities throughout Costa Rica and Panama, representing four regional phenotypes, according to the primary flank and leg color (flank/leg): blue/blue; blue/orange; brown/orange; violet/violet. Each open circle represents the average brightness of an individual. The thick horizontal bar shows the average value for the phenotype. A contrast ratio > 1.96 represents sufficient discrimination of the visual spectral sensitivities of the species with 95% confidence and is shown as a dotted line (Lythgoe and Partridge 1991). Brightness contrasts shown for five regions of the body relative to the background leaf. The schematic cartoon shows all color patches examined in these analyses
A Brightness contrast measures of Agalychnis callidryas sampled from Costa Rica and Panama, representing four regional phenotypes, according to the primary flank and leg color (flank/leg): blue/blue; blue/orange; brown/orange; violet/violet. The thick horizontal bar shows the mean value for the phenotype and each unfilled circle represents a brightness contrast for each flank to leg (left) and flank to stripe (right) comparison. A contrast ratio > 1.96 represents sufficient discrimination of the visual spectral sensitivities of the species with 95% confidence and is shown as a dotted line (Lythgoe and Partridge 1991). B Visual modeling based on spectral reflectance of the blue/blue and brown/orange morph and two rod photoreceptors of A. callidryas result show the luminosity contrasts (dL) and chromaticity contrasts (dS) for each comparison under standard daylight and moonlight conditions. A JND value greater than 1 represents barely noticeable (dotted red line) and greater than 2 signifies very noticeable differences (solid red line)
A Digital photographs of a blue/blue phenotype (above) and brown/orange phenotype (below) are modified to demonstrate how A. callidryas is perceived according to human color vision (left) and RH1-rod-based frog vision (right). This figure is intended for heuristic purposes and does not account for potential differences in visual acuity between humans and frogs. These photographs were not taken with the video camera configured with the filter pack because it is not possible to simultaneously photograph an individual with both human and frog-based vision filters. Instead, we imported the digital photograph in Adobe Photoshop, removed input from the red channel, and converted the image to greyscale to mimic scotopic, rod-based vision. B Spectral reflectance for four body regions of A. callidryas measured from one ‘blue’ and one ‘orange’ phenotype. The reflectance spectra show large differences in intensity within the range of the RH1 rod spectral sensitivity (grey shaded region). The blue flank and leg reflect light at wavelengths similar to dorsal coloration but differ in the intensity of reflectance at this wavelength. The orange flank and leg differ in both the range of the spectrum and intensity of reflectance relative to dorsal coloration
Some crepuscular and nocturnal animals are brightly marked yet the adaptive significance of their colorful patterns in low light, as found at twilight and night, is poorly understood. This phenomenon is particular prevalent in amphibians. Of the nearly 80% of nocturnal frogs, many exhibit color patterns with red, yellow, green and blue hues and/or contrasting spots and stripes. Despite the prevalence of these conspicuous visual signals in frogs, the function and adaptive significance of bright coloration for crepuscular/nocturnal frogs is still poorly understood. A critical first step in linking color pattern evolution with premating reproductive isolation and lineage divergence is determining whether color pattern plays a role in mate recognition in dim light. We studied the brightly colored Red-eyed Treefrog (Agalychnis callidryas), a crepuscular/nocturnal Neotropical treefrog that exhibits noteworthy geographic variation in color pattern and female choice for local male phenotypes. We measured retinal photoreceptor cell absorbance via microspectrophotometry and used visual modeling to assess whether distinct color pattern phenotypes were distinguishable as luminosity and chromaticity cues. We found that the Red-eyed Treefrog visual system is capable of discriminating differences in color patterns as brightness (luminosity) in their perception of nighttime visual cues. Differences in color (chromaticity) were also detectable in dim light, although less prominent than brightness. Combined, our data indicate that differences in these visual traits are discernable, can function for species and population recognition, and evolve through sexual selection. These social signals are thus analogous to the widespread visual displays exhibited by diurnal vertebrates, suggesting that the richness of similar sensory interactions among animals at twilight and after dark might be severely underappreciated. More generally, we demonstrate that combining studies of the visual system with population genetics, behavior, and natural history provides a framework for testing the evolution and adaptive function of color pattern.
Variations in climatic conditions over space and time play an important role in speciation. In this study, climate variables that may be influencing the evolution of the genus Neurergus were explored at both interspecific levels for the four recognized species (N. strauchii, N. crocatus, N. derjugini, and N. kaiseri) and intraspecific levels for three of the species. This was accomplished by predictions in geographical (G)-space using an ensemble of ten algorithms and ordination techniques, which included equivalency and background statistics of niche overlap and niche divergence tests in environmental (E)-space. At the interspecific level, results revealed significant evidence for niche divergence in species' bioclimatic preferences, supporting the hypothesis that niche divergence drives Neurergus diversification. These patterns, however, were not found at the intraspecific level and were identical in their environmental niches. Results of the present study provide an important insight into the evolutionary history of Neurergus in the Near East and help to elucidate how environmental changes contributed to lineage diversification.
Biting a and mandible flaring b in male Kosciuscola trisits tristis males from Thredbo while a female lays eggs. Photos: Kate Umbers
Skyhoppers of the Australian Alps: a female K. tristis, b male K. tristis, c distribution map of K. tristis sensu lato (s.l.), d female K. usitatus, e male K. usitatus, f distribution map of K. usitatus s.l., g female K. cuneatus, h male K. cuneatus, i distribution map of K. cuneatus s.l., j female K. cognatus, k male K. cognatus, l distribution map of K. cognatus s.l.. Distribution maps show the distributions of the Kosciuscola as previously described by Rehn (1957), different colour points represent new clades as described by Umbers et al (2021), upper white line represents Australian Capital Territory border, lower white line represents New South Wales/Victorian state border, black arrows indicate sampling site for this study
of the number of each behaviours observed corrected for the number of trials for each species. Number in parentheses in legend indicates the aggression score for each behaviour (see Table 2)
Predictors of aggressive behaviour in skyhoppers where each data point represents an individual male’s aggression score and measurement a weighted aggression score for four species (data are presented in box plots, depicting the median value (solid horizontal line), 25th and 75th percentile (box outline), minimum and maximum (whiskers)), b model predictions for the relationship between mandible length and weighted aggression score for each species, c model predictions for the relationship between pronotum length on weighted aggression score for each species. Table S1 provides the statistical results of comparisons between species’ aggression scores and shows that all pairwise comparisons are significant except between K. tristis and K. usitatus
Scatterplots of mean log length (mm) of traits per species. a relationships between mandible length and femur length for each species, b relationships between pronotum length and femur length for each species
The evolution of male-male aggression is of interest because at its extreme it can be very energetically costly, leave males vulnerable to preadtors, and give rise to weaponry such as exaggerated traits. In grasshoppers (Acrididae), one group stands out as exceptionally aggressive, the skyhoppers ( Kosciuscola ) in which males bite, kick, mandible flare, and wrestle each other for access to females or when females are laying eggs. In this study we asked whether there is variation in aggressive behaviour among four skyhopper species and aimed to determine whether the traits used in fighting bear signatures of sexual selection in their size, variability, and allometric scaling. We found clear differences in the numbers and types of aggressive behaviours among species. Kosciuscola tristis and K. usitatus were the most aggressive, K. cognatus was the least aggressive, and K. tristis was the only species that performed the ‘mandible flare’ behaviour. Mandible size was larger among the three species that showed aggressive behaviour, all except K. cognatus , and was negatively allometric for all species possibly suggesting a functional size constraint. Pronotum size was different among most species and K. tristis ’ pronotum was the largest and borderline positively allometric perhaps suggesting that pronotum size is related to aggressive behaviour but the nature of that relationship remains obscured. Our study suggests that further work investigates skyhoppers’ aggressive behaviour and how it varies with ecology, and paves the way for establishing them as a model system in the evolution of aggressive behaviour.
Timeline of the experiment testing transmission from varied within-host parasite communities to naïve recipient plants. Actions related to the transmission
source plants, planted in a common garden inside insect web cages and inoculated with the parasite combinations shown on the gray table on the right, are shown on green. Actions related to healthy recipient plants, grown in a greenhouse and brought to the cages in pots, are listed on brown. Actions related to both recipient and source plants are listed on white. Lines link the actions to the timing on the timeline on dark gray. Gray table illustrates the different treatment combinations. All treatments had Phomopsis subordinaria and treatment 8 was a control with P. subordinaria only
Results of the transmission experiment testing transmission from varied within-host parasite communities to naïve recipient plants shows that coinfection with powdery mildew causes more severe disease and increases transmission of P. subordinaria. A Change in the number of Phomopsis subordinaria infected flower stalks and B Total number of flower stalks from the beginning to the end of the experiment. Each unique color and shape combination shows a different parasite community treatment. Small points represent individual plants. Predicted averages and 95% confidence intervals calculated with the effects package in R are shown with large points and associated lines. An asterisk (*) shows the treatment where the change significantly differed from control in pairwise comparison. Treatments with powdery mildew are shaded with blue tones and treatments without it are shaded with yellow tones. Purple circle is the control with P. subordinaria only. C Number of Phomopsis subordinaria infected flower stalks in the
source plants at the beginning and the end of the experiment. Each unique color and shape combination shows a different parasite community treatment. Each small point represents an individual plant. Large points show the average and a line shows the change of the average between the time points. An asterisk (*) shows the treatment where the change significantly differed from control in pairwise comparison (p < 0.05). Treatments with powdery mildew are shaded with blue tones and treatments without powdery mildew are shaded with yellow tones. The purple circle is the control with P. subordinaria only. DPhomopsis subordinaria infection status (infected/not infected) of recipient plants in different treatments in the end of the experiment. Each unique color and shape combination shows a different treatment. Treatments with powdery mildew are shaded with blue tones and treatments without it are shaded with yellow tones. Purple circle is the control with P. subordinaria only. Each small point represents one recipient plant and large points show the averages. Black lines show standard errors of the averages. E Relationship between the number of infected flower stalks in source plants in a cage at the end of the experiment on X-axis and recipient P. subordinaria infection status in Y-axis. Each empty circle represents an individual recipient plant. The lines show smoothed conditional means
Results of a path model testing whether the effect of parasite community treatment on Phomopsis subordinaria transmission to recipient plants is caused by an effect of the treatment on the number of infected flower stalks in
source plants. Coefficient values presented next to the significant paths are standardized estimates. For the full list of coefficients please see Table S8 in the Appendix S1
A positive relationship between Phomopsis subordinaria occurrence in 2018 and historical powdery mildew infections in 261 Plantago lanceolata populations in the Åland Islands. A Relationship between P. subordinaria presence (n = 124) and absence (n = 137) and average historical powdery mildew population size (calculated over years 2014–2017) in the surveyed host populations. Population size was measured on a categorical scale of five categories: (1) 1–10 infected plants, (2) 10–50 infected plants, (3) 50–100 infected plants, (4) 100–1000 infected plants, (5) > 1000 infected plants. The line denotes a smoothed average. B Relationship between P. subordinaria population size in 2018 and the average historical powdery mildew population size, both measured on the categorical scale described above. The line denotes a smoothed average. C Frequency of historical powdery mildew population size in the surveyed host populations grouped to 11 spatial clusters of 10–49 populations each. For the locations of individual populations and clusters, please see figure S2 in the Appendix S1
Interactions among parasite species coinfecting the same host individual can have far reaching consequences for parasite ecology and evolution. How these within-host interactions affect epidemics may depend on two non-exclusive mechanisms: parasite growth and reproduction within hosts, and parasite transmission between hosts. Yet, how these two mechanisms operate under coinfection, and how sensitive they are to the composition of the coinfecting parasite community, remains poorly understood. Here, we test the hypothesis that the relationship between within- and between-host transmission of the fungal pathogen, Phomopsis subordinaria, is affected by co-occurring parasites infecting the host plant, Plantago lanceolata. We conducted a field experiment manipulating the parasite community of transmission source plants, then tracked P. subordinaria within-host transmission, as well as between-host transmission to naïve recipient plants. We find that coinfection with the powdery mildew pathogen, Podosphaera plantaginis, causes increased between-host transmission of P. subordinaria by affecting the number of infected flower stalks in the source plants, resulting from altered auto-infection. In contrast, coinfection with viruses did not have an effect on either within- or between-host transmission. We then analyzed data on the occurrence of P. subordinaria in 2018 and the powdery mildew in a multi-year survey data set from natural host populations to test whether the positive association predicted by our experimental results is evident in field epidemiological data. Consistent with our experimental findings, we observed a positive association in the occurrence of P. subordinaria and historical powdery mildew persistence. Jointly, our experimental and epidemiological results suggest that within- and between-host transmission of P. subordinaria depends on the identity of coinfecting parasites, with potentially far-reaching effects on disease dynamics and parasite co-occurrence patterns in wild populations.
Past studies investigating female responses to the manipulation of male sexual structures have A reported a range of different preferences for ornament size and B largely tested ornament sizes within the natural range of populations. Those handful of studies that included a super-sized ornament (i.e., a size outside the natural range) uniformly found female preferences for the super-sized structure, whereas those studies that tested ornament sizes within the natural range tended to report mixed preferences for larger ornaments
Head crest size and influence on conspecific behaviour. A A male Alticus sp. cf. simplicirrus exhibiting a prominent head crest (NB: this male is not showing the typical charcoal black courtship colouration; photo courtesy of Georgina Cooke). B The allometry of male head crests in Alticus sp. cf. simplicirrus (blue circles) and Alticus monochrus (orange circles; data from Summers and Ord 2022). Shown are the head crest sizes of the models used in presentations (filled circles): control (0mm²); average (11mm²); and super-sized (48mm²). The standard length of models was kept consistent (30 mm), equivalent to the display position of an average male (60 mm). Data are ln-transformed, with head crest area first linearised by a square-root (see Summers and Ord 2022). C The time females and males spent inspecting each male model (data are the mean ± SE total time individuals spent within the zone of approach, weighted by the proportion of individuals that approached that model out of all the individuals observed to approach any model during the trial)
It has been argued that disproportionately larger ornaments in bigger males—positive allometry—is the outcome of sexual selection operating on the size of condition dependent traits. We reviewed the literature and found a general lack of empirical testing of the assumed link between female preferences for large ornaments and a pattern of positive allometry in male ornamentation. We subsequently conducted a manipulative experiment by leveraging the unusual terrestrial fish, Alticus sp. cf. simplicirrus , on the island of Rarotonga. Males in this species present a prominent head crest to females during courtship, and the size of this head crest in the genus more broadly exhibits the classic pattern of positive allometry. We created realistic male models standardized in body size but differing in head crest size based on the most extreme allometric scaling recorded for the genus. This included a crest size well outside the observed range for the study population (super-sized). The stimuli were presented to free-living females in a manner that mimicked the spatial distribution of courting males. Females directed greater attention to the male stimulus that exhibited the super-sized crest, with little difference in attention direct to other size treatments. These data appear to be the only experimental evidence from the wild of a female preference function that has been implicitly assumed to drive selection that results in the evolution of positive allometry in male ornamentation.
Distribution of the number of shifts in the optima detected by the ℓ1ou analyses of standard length, body depth, fish width, geometric mean and body mass during the radiation of 42 teleost orders
Number of shifts in the optima detected by the ℓ1ou analyses of standard length, body depth and body width across each order
Common shifts in the optima between the three size components (standard length, body depth and body width). Dark grey bars depict the total number of shifts detected by the ℓ1ou analyses for each order and light grey bars depict the number of these shifts that occur in the same phylogenetic position (i.e. same branch of the phylogeny) across the three size components
A) Number of allometric shifts detected by bayou for the three allometric relationships explored: length vs. depth (red), length vs. width (orange), and depth vs. width (blue) across the order-level phylogeny of teleosts. Numbers in parentheses represent species sampling and richness respectively. B) Distribution of the estimated slopes of the allometric regimes detected across teleost orders for the three allometric relationships. Dashed line indicates a slope equal to one. Slopes estimated for each regime can be found in Table S6. C) Distribution of the estimated intercepts of the allometric regimes detected across teleost orders for the three allometric relationships. Intercepts estimated for each regime can be found in Table S6. Phylogenetic tree modified from Rabosky et al. 2018
of the estimated slopes (left) and intercepts (right) of the allometric regimes (shifts and background regimes) detected by bayou across teleost orders for the three allometric relationships: length and depth, depth and width, and length and width. Each allometric regime corresponds to a branch in the phylogeny. For example, orders represented by one branch have no shifts and have one regime; orders represented by two branches have one shift and, therefore, are described by two regimes. Slopes are presented as the difference relative to isometry. SL = standard length; BD = body depth; BW = body width. Plots produced using the function CountMap in the R package Phytools (Revell 2012). Phylogenies modified from Rabosky et al. (2018)
Body size influences nearly every aspect of an organism’s biology and ecology. When studying body size, researchers often focus on a single dimension, such as length, despite the fact that size can evolve by altering multiple body dimensions. The distinct ways organisms change their size can have profound consequences on evolutionary and ecological processes. Here, we investigate the evolution of size as a complex trait by exploring the interaction between body length, depth, and width across 42 orders of teleost fishes. Using Ornstein-Uhlenbeck models, we compare shifts in the adaptive landscapes of each of the three size components, and in the scaling relationships between them. We find that fishes change their size in a myriad of ways: changes in length, depth and width rarely co-occur on the phylogeny or in accordance with composite measures of size (body mass or the geometric mean). Body size diversity tends to accumulate along trajectories close to isometry but there is also some variation in the allometric regimes. Finally, orders with scaling shifts are more species rich than those without shifts, suggesting that body size diversity trajectories have the potential to be associated with distinct diversification scenarios in teleosts. Based on the evolutionary relationships we found between size components, we recommend that researchers treat body size as a complex trait to properly evaluate the patterns and processes of size variation in nature.
Daphnia dentifera in Little Appleton Lake experienced a large epidemic of Pasteuria ramosa; host density decreased substantially during the epidemic. (a) Prevalence of P. ramosa increased steadily from the beginning of sampling, peaked at 39% of hosts infected, and decreased more sharply during October. (b) D. dentifera density was high at the beginning of August and decreased during September and the first part of October. Host and parasite samples were collected at three time points throughout the epidemic trajectory in the Fall of 2017; these three timepoints are indicated with colors that match the timepoints in Figs. 3 and 4
D. dentifera that were infected with P. ramosa had shorter lives and many fewer clutches than unexposed control hosts; there was no significant difference between the lifespan and reproduction of control hosts and hosts that were exposed but not infected. Statistical analyses used individual-level data; in order to more clearly visualize the data, averages for each host clone x parasite exposure combination are plotted
There was no difference in the proportion of hosts that became infected when hosts from a given time point were exposed to contemporary parasites (panel a), nor when time 3 hosts were exposed to parasites from time 1 vs. time 3 (panel b)
Virulence of parasites against contemporary host clones did not significantly differ across the three time points, nor did the impact of parasites from two different time points on time 3 hosts; however, time 3 parasites yielded fewer spores and had a slower within host growth rate in time 3 hosts, as compared to time 1 parasites. Left panels: virulence of parasites against hosts from the same time point (e.g., when hosts from time 2 were exposed to parasites from time 2). Right panels: virulence of parasites from time 1 and time 3 in hosts from time 3; this allows for isolation of the effects of parasite evolution. There were no significant differences in lifespan (a&b) or reproduction (c&d). The number of spores produced per infected host, and the parasite growth rate within infected hosts, did not differ significantly for hosts from the three time points exposed to their contemporary parasites (e&g). However, when time 3 hosts were exposed to parasites from time 1 vs. time 3, hosts infected with time 1 parasites produced significantly more spores (f) and had a significantly faster growth rate (h); this suggests that the parasite evolved to grow slower and produce fewer spores, which was contrary to our expectations. Statistical analyses used individual-level data; in order to more clearly visualize the data, averages for each host clone x parasite exposure combination are plotted
Virulence, the degree to which a pathogen harms its host, is an important but poorly understood aspect of host-pathogen interactions. Virulence is not static, instead depending on ecological context and potentially evolving rapidly. For instance, at the start of an epidemic, when susceptible hosts are plentiful, pathogens may evolve increased virulence if this maximizes their intrinsic growth rate. However, if host density declines during an epidemic, theory predicts evolution of reduced virulence. Although well-studied theoretically, there is still little empirical evidence for virulence evolution in epidemics, especially in natural settings with native host and pathogen species. Here, we used a combination of field observations and lab assays in the Daphnia-Pasteuria model system to look for evidence of virulence evolution in nature. We monitored a large, naturally occurring outbreak of Pasteuria ramosa in Daphnia dentifera, where infection prevalence peaked at ~ 40% of the population infected and host density declined precipitously during the outbreak. In controlled infections in the lab, lifespan and reproduction of infected hosts was lower than that of unexposed control hosts and of hosts that were exposed but not infected. We did not detect any significant changes in host resistance or parasite infectivity, nor did we find evidence for shifts in parasite virulence (quantified by host lifespan and number of clutches produced by hosts). However, over the epidemic, the parasite evolved to produce significantly fewer spores in infected hosts. While this finding was unexpected, it might reflect previously quantified tradeoffs: parasites in high mortality (e.g., high predation) environments shift from vegetative growth to spore production sooner in infections, reducing spore yield. Future studies that track evolution of parasite spore yield in more populations, and that link those changes with genetic changes and with predation rates, will yield better insight into the drivers of parasite evolution in the wild. Supplementary information: The online version contains supplementary material available at 10.1007/s10682-022-10169-6.
Genome-wide per-locus diversity metrics for mice categorized according to infection status (Uninfected: n = 9; Infected n = 22). Per-locus genomic diversity metrics are significantly lower in Uninfected vs Infected mice for a) observed heterozygosity (HO; p < 0.001),b) expected heterozygosity (HE; p = 0.001479),c) the inbreeding coefficient (FIS; p < 0.001) and,d) private allelic richness (PAR; non-overlapping 95% CIs). Across all sample sizes, e) allelic richness (AR) does not differ among groups (overlapping confidence intervals). Points are means and error bars are ± one standard error, with the exception of FIS which is shown with ± two standard errors for visualization purposes. For AR (e), the curve is the smoothed conditional mean for Uninfected (dashed) and Infected (solid) mice, and the shading represents 95% confidence intervals
Genome-wide per locus diversity metrics for mice categorized according to infection severity (Uninfected: n = 9; Low: n = 11; High: n = 10). Per-locus genomic diversity metrics include a) observed heterozygosity (HO; all comparisons p < 0.001),b) expected heterozygsity (HE; High vs Low/Uninfected p < 0.001; Low vs Uninfected ns),c) the inbreeding coefficient (FIS; all comparisons p < 0.001),d) private allelic richness (PAR; Uninfected vs Low/High non-overlapping CIs; Low vs High ns), and e) allelic richness (AR; overlapping CIs). Points are means and error bars are ± two standard errors. For AR (e), the curve is the smoothed conditional mean for Uninfected (white, dotted), Low (medium gray, long dash), and High mice (dark grey, solid), and the shading represents 95% confidence intervals
Coinfected individuals show (a) significantly lower per-locus levels of private allelic richness (PAR; non-overlapping CIs) and (b) a non-significant trend towards lower levels of per-locus allelic richness (AR). Points are means and error bars are ± two standard errors. For AR (e), the curve is the smoothed conditional mean for Uninfected (dashed, lightest gray), Low (long dash, medium gray), High (dotted, dark gray), and coinfected (solid, black) groups, and the shading represents 95% confidence intervals. Group colors are the same in (a) and (b). Samples sizes are as follows: Uninfected (n = 9), Low (n = 9), High (n = 7) and coinfected (n = 5)
Partial residual plots from linear regression models show a) the marginally positive correlation between per-individual FIS and coccidia abundance (p = 0.083), b) the negative correlation between residual body condition and coccidia abundance (p = 0.007), and c) the lack of relationship between per-individual FIS and residual body condition (p = 0.76)
Effects of genomic variation on host fitness can be mediated by parasite infection via effects of heterozygosity on immune function and infection. The gray box depicts an individual host and the bi-directional interactions among immunity, infection, condition, and reproduction. The lower body condition observed in infected animals could be a) a consequence of infection, b) a cause of infection, or c) both. The observed relationships between per-locus host genomic diversity and infection could be a direct effect or mediated via host immunity, and could interact with the infection-condition association to affect host fitness and future genomic diversity (gray dashed arrow)
Whether, when, and how genetic diversity buffers individuals and populations against infectious disease risk is a critical and open question for understanding wildlife disease and zoonotic disease risk. Several, but not all, studies have found negative relationships between infection and heterozygosity in wildlife. Since they can host multiple zoonotic infections, we sampled a population of wild deer mice (Peromyscus maniculatus), sequenced their genomes, and examined their fecal samples for coccidia and nematode eggs. We analyzed coccidia infection status, abundance, and coinfection status in relation to per-locus and per-individual measures of heterozygosity, as well as identified SNPs associated with infection status. Since heterozygosity might affect host condition, and condition is known to affect immunity, it was included as a co-variate in the per-individual analyses and as response variable in relation to heterozygosity. Not only did coccidia-infected individuals have lower levels of genome-wide per-locus diversity across all metrics, but we found an inverse relationship between genomic diversity and severity of coccidia infection. We also found weaker evidence that coinfected individuals had lower levels of private allelic variation than all other groups. In the per-individual analyses, relationships between heterozygosity and infection were marginal but followed the same negative trends. Condition was negatively correlated with infection, but was not associated with heterozygosity, suggesting that effects of heterozygosity on infection were not mediated by host condition in this system. Association tests identified multiple loci involved in the inflammatory response, with a particular role for NF-κB signaling, supporting previous work on the genetic basis of coccidia resistance. Taken together, we find that increased genome-wide neutral diversity, the presence of specific genetic variants, and improved condition positively impact infection status. Our results underscore the importance of considering host genomic variation as a buffer against infection, especially in systems that can harbor zoonotic diseases.
Effects of 200 generations of unbounded range expansion on evolution of the dispersal trait. Panels a and b show the average dispersal phenotypes of edge populations after 200 generations (filled points) compared to the starting populations (hollow points) across different numbers of loci defining the dispersal trait. Panels c and d show the average additive genetic variance of edge populations after expansion (filled points) compared to average additive genetic variance of initial populations (hollow points) with loci number again on the x axis. Panels a and c show results for scenarios in which there is no genetic mixing among individuals (asexual and obligately self-fertilizing populations) and panels b and d show results for the other scenarios. In all panels, the color and shape of points correspond to the population type as indicated in the legends on panels a and b. Points are the means across replicate simulations and line segments show the interquartile ranges. Additive genetic variance of asexual and obligately selfing populations (c) is essentially 0 for all numbers of loci, indicating the dominance of only a few or even one genotype after expansion
Effects of 200 generations of range shifts on evolution of the dispersal trait. Panels a and b show the average dispersal phenotypes of surviving populations after 200 generations (filled points) compared to the starting populations (hollow points) across different numbers of loci defining the dispersal trait. Panels c and d show the average additive genetic variance of surviving populations after expansion (filled points) compared to average additive genetic variance of initial populations (hollow points) with loci number again on the x axis. Panels a and c show results for scenarios in which there is no genetic mixing among individuals (asexual and obligately self-fertilizing populations) and panels b and d show results for the other scenarios. In all panels, the color and shape of points correspond to the population type as indicated in the legends on panels a and b. Points are the means across replicate simulations and line segments show the interquartile ranges. Additive genetic variance of asexual and obligately selfing populations (c) is essentially 0 for all numbers of loci, indicating the dominance of only a few or even one genotype after the range shift
Extinction risk of evolving populations undergoing climate driven range shifts for 200 generations. The y axis shows the proportion of replicate simulations in each category to go extinct during the 200 generations. The x axis shows the number of loci defining dispersal in each simulation. As in previous graphs, the color and shape of points correspond to the population type as indicated in the legend
Effect of evolution on distance spread in unbounded range expansions. The y axis shows the change in distance spread between simulations with evolution compared to simulations without evolution in units of discrete patches. Positive values indicate an increased distance spread due to evolution. The dashed grey line at 0 corresponds to no change in distance spread due to evolution. When evolution was prevented, simulated populations spread about 470 patches, on average, in 200 generations. Spread rates did not differ among population types or numbers of loci when evolution was prevented. The x axis shows the number of loci defining dispersal in each simulation. As in previous graphs, the color and shape of points correspond to the population type as indicated in the legend. Points are the among simulation means and line segments show the interquartile ranges
Change in extinction risk due to evolution in climate driven range shifts. The y axis shows the change in the proportion of replicate simulations to go extinct in scenarios with evolution compared to scenarios without evolution. Negative values indicate a reduced extinction risk due to evolution. The dashed grey line at 0 corresponds to no change in extinction risk due to evolution. The x axis shows the number of loci defining dispersal in each simulation. As in previous graphs, the color and shape of points correspond to the population type as indicated in the legend
Research has conclusively demonstrated the potential for dispersal evolution in range expansions and shifts, however the degree of dispersal evolution observed has varied substantially among organisms. Further, it is unknown how the factors influencing dispersal evolution might impact other ecological processes at play. We use an individual-based model to investigate the effects of the underlying genetics of dispersal and mode of reproduction in range expansions and shifts. Consistent with predictions from stationary populations, dispersal evolution increases with sexual reproduction and loci number. Contrary to our predictions, however, increased dispersal does not always improve a population’s ability to track changing conditions. The mate finding Allee effect inherent to sexual reproduction increases extinction risk during range shifts, counteracting the beneficial effect of increased dispersal evolution. Our results demonstrate the importance of considering both ecological and evolutionary processes for understanding range expansions and shifts.
Conceptual diagram illustrating the effects of (A) developmental environments experienced early in life on (B) reversible plasticity of labile traits expressed later in life (‘reaction norm’, Via et al. 1995). Developmental environment can also influence (C) repeatability of plastic responses (consistent among individual variation in slopes), this is typically represented by the variation in the slope of the reaction norm, Via et al. 1995)”
Predicted thermal reaction norm of metabolic rate (VCO2 min⁻¹ g⁻¹) for the ‘cold’ developmental temperature group (blue line, nlizards = 26) and the ‘hot’ developmental temperature group (red line, nlizards = 25) Points are raw data and are coloured according to treatment groups, nobs = 3818. Dashed lines represent the upper and lower bounds of 95% credible intervals
Thermal reaction norms of mass-adjusted metabolic rate for lizards reared at (A) ‘hot’ developmental temperatures (top, red lines, nlizards = 25) and (B) ‘cold’ developmental temperatures (bottom, blue lines, nlizards = 26) at session number one, five and ten. Each uniquely coloured line represents an individual reaction norm. A random subset of 10 individuals from each treatment are presented
(A) Temperature-specific adjusted repeatability for average metabolic rate for the ‘cold’ developmental temperature group (blue, nlizards = 26) and the ‘hot’ developmental temperature group (red, nlizards = 25). Error bars represent 95% credible intervals. (B) Violin and boxplot showing the posterior distribution of overall adjusted repeatability of each treatment group irrespective of temperature. (C) Posterior distribution of the difference in repeatability (Hot–Cold) overall and at each temperature. Point represents the median; thicker lines represent the interquartile range and thin lines represent the 95% credible intervals. The probability of direction is presented on each distribution and describes the probability that the difference in repeatability is either positive or negative. Grey regions of the distribution represent negative estimates indicating repeatability was greater in the cold treatment, whereas black regions represent positive estimates which indicates that repeatability was greater in the hot treatment. All values were calculated from imputation models (Supplementary Materials, Sect. 4 Table S15–16). Contrasts are presented in Table S12
Phenotypic plasticity is an important mechanism that allows populations to adjust to changing environments. Early life experiences can have lasting impacts on how individuals respond to environmental variation later in life (i.e., individual reaction norms), altering the capacity for populations to respond to selection. Here, we incubated lizard embryos ( Lampropholis delicata ) at two fluctuating developmental temperatures (cold = 23 ºC + / − 3 ºC, hot = 29 ºC + / − 3 ºC, n cold = 26, n hot = 25) to understand how it affected metabolic plasticity to temperature later in life. We repeatedly measured individual reaction norms across six temperatures 10 times over ~ 3.5 months (n obs = 3,818) to estimate the repeatability of average metabolic rate (intercept) and thermal plasticity (slope). The intercept and the slope of the population-level reaction norm was not affected by developmental temperature. Repeatability of average metabolic rate was, on average, 10% lower in hot incubated lizards but stable across all temperatures. The slope of the thermal reaction norm was overall moderately repeatable ( R = 0.44, 95% CI = 0.035 – 0.93) suggesting that individual metabolic rate changed consistently with short-term changes in temperature, although credible intervals were quite broad. Importantly, reaction norm repeatability did not depend on early developmental temperature. Identifying factors affecting among-individual variation in thermal plasticity will be increasingly more important for terrestrial ectotherms living in changing climate. Our work implies that thermal metabolic plasticity is robust to early developmental temperatures and has the capacity to evolve, despite there being less consistent variation in metabolic rate under hot environments.
Comparison of pollinaria length, stigma height and stigma width of Ophrys normanii (blue) and Ophrys chestermanii (yellow) among allopatric, natural and artificial sympatric populations sampled in 2018. Significant differences are indicated by stars
Comparison among sympatric and allopatric populations of Ophrys chestermanii (yellow) and O. normanii (blue) sampled in Gögler et al. (2015) and in the present study
Principal component analysis based on the three floral characters involved in the mechanical barrier (pollinaria length, stigma height and stigma width) of Ophrys chestermanii (yellow) and O. normanii (blue) in natural sympatry (A) and in artificial sympatry (B) in 2018. Triangles indicate individuals with hybrid fruits
An increased divergence in characters between species in secondary contact can be shaped by selection against competition for a common resource (ecological character displacement, ECD) or against maladapted hybridization (reproductive character displacement, RCD). These selective pressures can act between incipient species (reinforcement) or well-separated species that already completed the speciation process, but that can still hybridize and produce maladapted hybrids. Here, we investigated two well-separated sexually deceptive orchid species that, unusually, share their specific pollinator. Sympatric individuals of these species are more divergent than allopatric ones in floral characters involved in a mechanical isolating barrier, a pattern suggestive of RCD. To experimentally test this scenario, we built an artificial sympatric population with allopatric individuals. We measured flower characters, genotyped the offspring in natural and artificial sympatry and estimated fertility of hybrids. Different from naturally sympatric individuals, allopatric individuals in artificial sympatry hybridized widely. Hybrids showed lower pollination success and seed viability than parentals. Character displacement did not affect plant pollination success. These findings suggest that RCD evolved between these species to avoid hybridization and that selection on reinforcement may be very strong even in plants with highly specialized pollination.
We exploited ecotypic variation in Impatiens capensis (Balsaminaceae) to test the hypothesis that mutation accumulation accompanying relaxed selection on the chasmogamous (CH) flower leads to more variable flower shapes and smaller flowers. Sun ecotype populations of this species occur along sunny riverbanks and marshes and produce both CH and cleistogamous (CL) flowers, while shade ecotype populations occur in shady forest floors and produce only CL flowers. In the shade ecotype, it is assumed that selection on the CH flower has been relaxed. Seedlings from population samples of the two ecotypes exhibited different first internode growth responses to low ratios of red:far-red light as seen in earlier studies of ecotypic differentiation to sunny versus shady conditions, helping to verify historical illumination conditions in the populations. We examined the CH floral mutation accumulation hypothesis by comparing the shape and size of the modified CH flower sepal under greenhouse conditions that triggered CH flowering in plants of both ecotypes. Contrary to our predictions, geometric morphometric analysis of sepal shape variation indicated little difference between the shade and sun ecotypes. We suggest that mutations that influence CH flower shape may have pleiotropic effects on structures or processes that remain under selection even when the CH flowers are not produced. On the other hand, sepal size was significantly smaller in the shade ecotype populations. In the case of CH sepal size, the mutational effects appear to be directional, towards producing smaller sepals, and would likely be deleterious if shade ecotype plants encounter sunnier conditions where the plants can produce CH flowers.
Schematic representation of visual antipredator strategies in spiders clustered in quadrants following two axes: The X-axis represents the visual signal's conspicuousness while the Y-axis represents its honesty. We highlighted the strategies that involve movement in italics. Quadrant numbers go clockwise, starting from the top left. Spatial position of the strategies is according to the rationale provided in Table 1
Some examples of the visual antipredator defences discussed in the Text. Quadrant 1: a Cryptic spider Talthybia sp. (Araneidae) matches the background colouration. b Masquerading Pasilobus sp. spider (Araneidae) that resembles bird droppings. cChrysilla sp. spider (Salticidae) with structural colouration. Quadrant 2: dSynemosyna sp. (Salticidae) that mimic morphological and behavioural traits of an ant. ePhiale sp. (Salticidae) probably resemble some traits of the general aspect of a mutillid wasp. fCyclosa sp. (Araneidae) has in its web decorations made of debris that misdirect the predator’s attack away from the actual spider location. Quadrant 3: gArgiope aurantia (Araneidae), which builds a web decoration, and performs a fast web flexing behaviour when a predator attempts to attack the spider. hLatrodectus sp. (Theridiidae) with aposematic colouration thought to warn the predator about its potential defences. Quadrant 4: iAnelosimus eximius (Theridiidae) spiders that might gather protection against visually oriented predators with its social habits. Photos a–c, h–i by Nicky Bay; d–e by Thomas Shahan; and f–g by Dinesh Rao
Many animals use visual traits as a predator defence. Understanding these visual traits from the perspective of predators is critical in generating new insights about predator–prey interactions. In this paper, we propose a novel framework to support the study of strategies that exploit the visual system of predators. With spiders as our model taxon, we contextualise these strategies using two orthogonal axes. The first axis represents strategies using different degrees of conspicuousness to avoid detection or recognition of the spider and deter predator attacks. The second axis represents the degree of honesty of the visual signal. We explore these issues with reference to the three main vision parameters: spectral sensitivity, visual acuity, and temporal resolution, as well as recent tools to study it, including multispectral digital imaging.
Relationship between species-specific average lifespan and male wing length (mm). Each rectangle represents one species (N = 64 species). The side lengths of the rectangles are proportional to the inverse of species-specific standard errors of respective variables. The indication of reliability is relative and should not be read against the scale on the axes. Non-phylogenetic linear regression line is added to visualise the results presented in Table 1
Relationship of lifespan and mean temperature in the Ugandan sample (red regression line; each spot represents a single individual). The red regression line is added to illustrate results presented in Table 1. Mean values for the temperate region lifespans and the blue regression line are based on the results published in Holm et al 2016. MMLS = mean male lifespan (days). MFLS = mean female lifespan (days)
Comparative studies on insects can significantly contribute to understanding the evolution of lifespan, as the trait can feasibly be measured in a high number of species. If the evolutionary determinants of longevity were mainly extrinsic (ecological), related species from different habitats should systematically differ in individual lifespans. We recorded adult longevities for 110 species of geometrid moths from a tropical community and paralleled the lifespans in this tropical assemblage with a temperate counterpart. Comparative analyses using an original phylogenetic reconstruction revealed that in the studied tropical assemblage, larger moth species tended to live longer, and that females had slightly shorter lifespans than males. Average adult lifespans in tropical geometrids, and the relationships of lifespan with other variables, were found to be highly similar to those reported for their temperate region relatives. The among-region similarity leads to the conclusion that intrinsic (physiological) determinants of longevity dominate over extrinsic (ecological) ones: the contrasting environments of tropical and temperate forests have hardly produced differences in moth longevities.
Allometry has been the focus of growing interest in studies using geometric morphometric methods to address a wide range of research questions at the interface of ecology and evolution. This study uses computer simulations to compare four methods for estimating allometric vectors from landmark data: the multivariate regression of shape on a measure of size, the first principal component (PC1) of shape, the PC1 in conformation space, and a recently proposed method, the PC1 of Boas coordinates. Simulations with no residual variation around the allometric relationship showed that all four methods are logically consistent with one another, up to minor nonlinearities in the mapping between conformation space and shape tangent space. In simulations that included residual variation, either isotropic or with a pattern independent of allometry, regression of shape on size performed consistently better than the PC1 of shape. The PC1s of conformation and of Boas coordinates were very similar and very close to the simulated allometric vectors under all conditions. An extra series of simulations to elucidate the relation between conformation and Boas coordinates indicated that they are almost identical, with a marginal advantage for conformation. Empirical examples of ontogenetic allometry in rat skulls and rockfish body shape illustrate simple biological applications of the methods. The paper concludes with recommendations how these methods for estimating allometry can be used in studies of evolution and ecology.
Mantispoidea exhibit a remarkably diverse morphology and life history for a relatively small group of insects, in part, complicating our understanding of its evolutionary history. Dietary specialisation of the larvae, however, seems to have played an important evolutionary role in this group. Symphrasinae (Rhachiberothidae) larvae are thought to be predators of aculeate Hymenoptera brood, while Mantispinae (Mantispidae) larvae are predators of spider eggs. Herewith the first observation of a Mantispinae adult emerging from the nest of a mud-dauber wasp (Sphecidae) is described. This is also the first genus record of Afromantispa Snyman & Ohl from the Oriental Region, including three new name combinations. The curious coincidence of a Mantispinae emerging from an aculeate wasp nest, the food source of a related taxon, is discussed in the light of our current understanding of Mantispoidea classification.
As snakes are limbless, gape-limited predators, their skull is the main feeding structure involved in prey handling, manipulation and feeding. Ontogenetic changes in prey type and size are likely to be associated with distinct morphological changes in the skull during growth. We investigated ontogenetic variation in diet from stomach contents of 161 Dugite specimens ( Pseudonaja affinis , Elapidae) representing the full range of body size for the species, and skull morphology of 46 specimens (range 0.25–1.64 m snout-vent-length; SVL). We hypothesised that changes in prey type throughout postnatal ontogeny would coincide with distinct changes in skull shape. Dugites demonstrate a distinct size-related shift in diet: the smallest individuals ate autotomised reptile tails and reptiles, medium-sized individuals predominantly ate mammals, and the largest individuals had the most diverse diet, including large reptiles. Morphometric analysis revealed that ~40% of the variation in skull shape was associated with body size (SVL). Through ontogeny, skulls changed from a smooth, bulbous cranium with relatively small trophic bones (upper and lower jaws and their attachments), to more rugose bones (as a likely reflection of muscle attachment) and relatively longer trophic bones that would extend gape. Individual shape variation in trophic bone dimensions was greater in larger adults and this likely reflects natural plasticity of individuals feeding on different prey sizes/types. Rather than a distinct morphological shift with diet, the ontogenetic changes were gradual, but positive allometry of individual trophic bones resulted in disproportionate growth of the skull, reflected in increased gape size and mobility of jaw bones in adults to aid the ingestion of larger prey and improve manipulation and processing ability. These results indicate that allometric scaling is an important mechanism by which snakes can change their dietary niche.
Obligate brood parasitic birds lay their eggs in the nests of other species, reducing the host’s own reproductive output. To circumvent these fitness costs, many—but not all—host species have evolved the ability to recognize and reject brood parasitic eggs. What factors constrain egg rejection, and why do host species vary in their likelihood of rejection? Previous comparative studies have found that egg rejection rates covary with several biotic factors (including larger body size, smaller relative brain size, and more northerly breeding latitudes), but much behavioral variation in the occurrence of egg rejection remains unexplained. In this study, we test a corollary of the maternal investment hypothesis, by assessing whether species with higher clutch sizes are more likely to eliminate parasitic eggs. We examined two published data sets comprising over 200 unique bird species, controlling for phylogeny and other known interspecific correlates of egg rejection rates. Contrary to the prediction, we found no evidence for a positive relationship between clutch size and egg rejection rate. Rather, our analyses suggest a weak but consistent negative relationship between absolute and relative metrics of clutch size versus egg rejection rate across species. These results are instead consistent with two previously proposed alternative hypotheses: that egg rejection is constrained by a trade-off between maternal investment and anti-parasitic defenses, possibly mediated by endocrine mechanisms linked to parental care, and/or that cognitive decision rules facilitate the detection of dissimilar eggs in smaller clutches.
Despite only comprising seven species, extant sea turtles (Cheloniidae and Dermochelyidae) display great ecological diversity, with most species inhabiting a unique dietary niche as adults. This adult diversity is remarkable given that all species share the same dietary niche as juveniles. These ontogenetic shifts in diet, as well as a dramatic increase in body size, make sea turtles an excellent group to examine how morphological diversity arises by allometric processes and life habit specialisation. Using three-dimensional geometric morphometrics, we characterise ontogenetic allometry in the skulls of all seven species and evaluate variation in the context of phylogenetic history and diet. Among the sample, the olive ridley (Lepidochelys olivacea) has a seemingly average sea turtle skull shape and generalised diet, whereas the green (Chelonia mydas) and hawksbill (Eretmochelys imbricata) show different extremes of snout shape associated with their modes of food gathering (grazing vs. grasping, respectively). Our ontogenetic findings corroborate previous suggestions that the skull of the leatherback (Dermochelys coriacea) is paedomorphic, having similar skull proportions to hatchlings of other sea turtle species and retaining a hatchling-like diet of relatively soft bodied organisms. The flatback sea turtle (Natator depressus) shows a similar but less extreme pattern. By contrast, the loggerhead sea turtle (Caretta caretta) shows a peramorphic signal associated with increased jaw muscle volumes that allow predation on hard shelled prey. The Kemp’s ridley (Lepidochelys kempii) has a peramorphic skull shape compared to its sister species the olive ridley, and a diet that includes harder prey items such as crabs. We suggest that diet may be a significant factor in driving skull shape differences among species. Although the small number of species limits statistical power, differences among skull shape, size, and diet are consistent with the hypothesis that shifts in allometric trajectory facilitated diversification in skull shape as observed in an increasing number of vertebrate groups.
Comparison of static allometry of thorax width, and mid femur and mid tibia length and with wing length, in two species of Coelopidae, Coelopella curvipes and Chaetocoelopa littoralis. Coefficient values for each species and sex can be found in Table 2. The dashed lines in each plot show a comparative isometric slope of 1
Variation in trait size in males from mating trials with Chaetocoelopa littoralis. Plots (a – c) show a comparison of male mid tibia length of males which did or did not engage in mating interactions during trials (a), did or did not successful mate with at least one female during the trial (b), and did or did not successfully copulate during the trial across only males which attempted to mate (c). Plots (d – e) represent the equivalent comparisons paired with plots (a – c) but with wing length. Curves are fitted from linear models with a binomial distribution
The need to respond quickly to the presence of an ephemeral resource required for breeding is often a feature of scramble competition mating systems. Scramble competition mating systems can feature extreme levels of sexual conflict and coercive mating by males. As a result, sexual selection can act on various traits used by males to overcome female resistance behaviours. Selection on these traits may result in significant intra and intersexual size variation and sexual dimorphism. Additionally, traits that influence mating success in males often show positive static allometry. Kelp flies (Coelopidae) are a small family of Diptera which specialise on wrack (beach cast marine macroalgae), a highly ephemeral resource. The mating system of these flies involves high levels of sexual conflict, with females rejecting all male mating attempts. In this study we describe intra and intersexual size variation and static allometry of traits in two of Aotearoa|New Zealand’s species, Coelopella curvipes and Chaetocoelopa littoralis . In addition, we investigate the mating behaviour of C. littoralis under ecologically relevant mating conditions. We found high levels of variation in both species with significant evidence of sexual dimorphism across all traits measured in C. littoralis, and in mid tibia length in C. curvipes . Furthermore, mid tibia length in both species exhibits positive static allometry and is disproportionally larger in larger males, suggesting that this trait in particular may be under strong sexual selection. We found that larger male C. littoralis which attempt to mate are significantly more likely to mate successfully demonstrating a large-size advantage in this species similar to findings across the Coelopidae. However, we only found a non-significant trend towards a mating advantage for males with longer mid-tibiae. We discuss these findings with reference to the population dynamics and ecology of these species.
Weapon-signal continuum ranging from pure weapons (left) to pure aggressive signals (right). Allometric slopes become steeper as the relative importance of signaling increases, based on comparisons of three armaments that span the weapon-signal continuum: hindlegs of bulb mites, claws of fiddler crabs, and eye-spans of stalk-eyed flies. In comparison to their reference traits, bulb mite legs (pure weapon) had the shallowest allometric slope, fiddler crab claws (dual weapon-signal) had an intermediate allometric slope, and stalk-eyed fly eye-spans (pure signal) had the steepest allometric slope. Allometric slopes (estimate ± SE) of focal traits (βfocal, plotted in black) and reference traits (βref, plotted in gray) are from ordinary least squares regression on log10-transformed length measurements. Figure adapted from McCullough et al. (2016). Photo credits: Jan Van Arkel (bulb mite), Daisuke Muramatsu (fiddler crab), and Jerry Wilkinson (stalk-eyed fly)
Structures used in intrasexual competition span a continuum, with pure weapons that are used exclusively in physical fights at one extreme and pure aggressive signals that are used exclusively to assess and threaten rivals at the other. We propose this weapon-signal continuum offers a framework for understanding the variation in allometric slopes among intra-sexually selected structures. We predict allometric slopes will become steeper as the relative importance of signaling increases, because aggressive signaling will favor the evolution of hypervariable structures that facilitate the assessment of subtle differences in body size. We provide preliminary empirical support for the continuum hypothesis using species with different types of armaments and offer suggestions for how to test the weapon-signal continuum among closely related species.
The identification of biological pattern is often complicated by the lack of methodologically consistent data with broad geographic coverage, especially when considering functional characteristics of organisms that differ greatly in body size and morphology. In our study (Dahlke et al. 2020), we addressed the problem of data scarcity by using different types of observational and experimental data together with statistical (phylogenetic) data imputation, and by placing our analysis into the context of a physiological concept, which provides a mechanism-based explanation for the observed pattern (ontogenetic shift in thermal tolerance of fish) and with respect to transition from sublethal to lethal thresholds. Here, we show with comparative examples that our results were not affected by the use of methodologically inconsistent data.
Comparative analyses require researchers to not only ensure data quality, but to also make prudent and justifiable assumptions about data comparability. A failure to do so can lead to unreliable conclusions. As a case in point, we comment on a study that estimated the vulnerability of the world’s fish species to climate change using comparisons between life stages (Dahlke et al. 2020, Science 369: 65-70). We highlight concerns with the data quality and argue that the metrics used to investigate ontogenetic differences in thermal tolerance were incomparable and confounded. Therefore, we recommend caution when interpreting their results in light of climate vulnerability. We suggest potential remedies and recommend thermal tolerance metrics that may be comparable across life stages. We also encourage the creation of guidelines to design, report, and assess comparative analyses to increase their reliability and reproducibility. See the full-text at: https://rdcu.be/cG5LV
Animal contests involve threatening displays and physical coercion, which are respectively performed by threat devices used in mutual evaluation of size or strength, and weapons used for grasping, stabbing, striking, or dislodging a rival. According to the functional allometry hypothesis, directional selection consistently favors hyper-allometry in threat devices, whereas the allometry of weapons depends on the way they are used in contests. Here, we tested this hypothesis using the Amazonian tusked harvestman Phareicranaus manauara (Arachnida: Opiliones), a male-dimorphic species, as a study system. Behavioral observations allowed us to recognize four contest-related traits and three control traits, not used in contests. Two weapons used to grasp or prod the opponents from afar and one threat device were hyper-allometric, whereas one tactile signaling device (used to tap the opponent) and all control traits were either iso- or hypo-allometric. These findings support the hypothesis that function predicts the allometry of contest-related traits. However, function does not explain allometric differences in homologous traits between males and females (whose traits also were used as controls). We suggest that if a trait used in contests by males is used by both sexes in another context, natural selection and cross-sexual genetic correlations may constrain its developmental trajectory, preventing the evolution of sexual dimorphism in allometric slopes. Therefore, using female traits as controls for homologous contest-related male traits may not be appropriate. Finally, we show that function does not explain differences between male morphs in the allometric slopes of male-dimorphic traits. Thus, an important next step in allometric studies is to understand what factors affect the slopes of male-dimorphic traits.
Study area. Location of the studied populations of Stenocereus pruinosus and S. stellatus are shown in the Valle de Tehuacán and the Mixteca Baja regions. Black bold line delimitates the states of Oaxaca and Puebla; green line delimitates Mixteca Baja region; yellow line delimitates Valle de Tehuacán region
Branch mortality percentage in Stenocereus pruinosus and S. stellatus populations under three forms of management in two regions of central Mexico, sampled for 2 years.
Stenocereus pruinosus and S. stellatus are columnar cacti from central Mexico, distributed in the Valle de Tehuacán and the Mixteca Baja regions. Both species have populations subject to three different forms of human management: wild, in situ and cultivated, growing in sympatry. The objectives of the present study were to compare variation in damage levels, defense mechanisms and fitness components between (1) both species due to differences in the intensity of management; (2) populations of both species subject to different forms of management; (3) two regions with different management practices and physical conditions, in these two columnar cacti. We estimated the percentage of damage, abundance of spines as resistance component, and branching rate as tolerance component, number of fruits produced in 1 year, number of seeds/fruit and germination rate as fitness components. The differences between species, forms of management and regions were estimated with a Nested ANOVA. A Multiple Correlation Analysis was followed between all traits at the species level and forms of management within each species. We found differences in mean values between species, forms of management and regions. Significant correlations between damage, defense strategies and fitness were detected in both species and forms of management, some of them concordant with domestication syndrome: More damage/less resistance, or more damage/more branching rate. Our results suggest that S. pruinosus evolved a tolerance response under human management, while S. stellatus has not modified any of them through the same process. Also, domestication process has influenced the mean values of some traits, but not all the correlations.
Principal component analysis (PCA) of average scale shape for all 92 Etheostomatinae darter species examined. Dots on the graph represent the averaged scale shape score for each species and are colored by genus-level clades. Numbers identify species codes and correspond to those in Table 1. Transformation grids on Principal Component axes 1 and 2 depict scale shape changes relative to the overall average scale shape of all darter species along each respective axis. Lines connecting points represent the phylogenetic relationships among species based on Near et al. (2011). The inset phylogeny at the bottom right of the figure shows relationships among darter genera (Near et al. 2011). The upper right image of E. barrenense (photo credit: Mark Hoger) shows the body placement from which scales were extracted from all specimens and an enlarged scale image that shows the placement of the 7 landmarks (white dots) used to assess scale shape variation. Letters “A” and “P” on the scale image denote “anterior” and “posterior” regions of the scale. Clades highlighted in the text are labelled and circled or have an arrow pointing to the clade node
Phylogenetic PCAs (Phy-PCA) of scale shape variation for all 92 species of Etheostomatinae darters with the average scale shape for each species coded by ecological variables of water column position and body size. Numbers identify species codes and correspond to those in Table 1. Transformation grids associated with graph axes depict scale shape change from the overall average scale shape of all darters along each axis. Grey lines connecting points represent the phylogenetic relationships among species based on Near et al. (2011). a Phy-PCA of all species examined with averaged scale shape scores of species coded by WCP. b Phy-PCA of all species examined with averaged scale shape scores of species coded by body size groups. Other ecological variables examined showed considerable overlap in morphospace for scale shape variation and were not significant in the PGLS and are not shown
Principal component analysis (PCA) and Phylogenetic PCA (Phy-PCA) of scale shape variation for the 72 benthic species of Etheostomatinae darters with the average scale shape for each species, represented by dots. Transformation grids associated with graph axes depict scale shape changes from the overall average scale shape of all darters along each axis. Grey lines connecting points represent the phylogenetic relationships among species based on Near et al. (2011). a PCA in phylomorphospace of benthic species examined with averaged scale shape scores for each species coded by genus. b Phy-PCA of benthic species examined with averaged scale shape scores for each species coded by body size. Other ecological variables examined were not significant in the PGLS and showed considerable overlap in morphospace for scale shape variation and are not shown
Examples of darter scale shape variation observed for the different ecological variables examined including those that were classified as Sub-benthic in water column position (a–e), restricted to pool microhabitats (f, g) or benthic, riffle habitats (h–j), and extra-large, hyperbenthic species (k–m). Species (and species codes from Table 1) represented by photos are: aAmmocrypta beani (01), bA. pellucida (02), cA. vivax (03), dCrystallaria asprella (04), eEtheostoma vitreum (59), fE. proeliare (46), gE. parvipinne (43), hNothonotus jordani (66), iE. caeruleum (14), jPercina phoxocephala (84), kP. kathae (76), lP. lenticula (77), and mP. aurantiaca (70)
The influence of environment and phylogeny on morphological characteristics of organisms is well documented. However, little is known about how these factors influence scale shape in fishes, a feature which may be important for drag reduction. We evaluated the impact of both on scale shape variation in the primarily benthic, riverine darter clade (Percidae: Etheostomatinae) of fishes. We predicted that darters with close phylogenetic relationships and/or shared ecologies would have more similar scale shapes, but this relationship would be mediated by use of the substrate boundary layer. We used geometric morphometrics and seven homologous landmarks for 92 species of darters representing all genera and 37 clades within genera to measure scale shape. Phylogenetic relationships and ecological variables describing habitat, spawning mode, and maximum body size of each species were summarized from the literature. We used ordinations to examine scale shape variation among phylogenetic and ecological groups. We conducted Phylogenetic Generalized Least Squares analyses to test for relationships between scale shape and ecological characteristics. Scale shape variation occurred within and among darter clades, and was significantly related to phylogeny. However, we found divergent scale shapes between close relatives and similar scale shapes between distantly related species. After accounting for phylogenetic signal, size and water column position were related to scale shape. Extra-large, hyperbenthic species had longer, narrower scales that may decrease laminar drag. Sub-benthic darters had scales that were narrower at the insertion, and with enlarged ctenial margins that may facilitate burying. Among benthic darters, size was significantly related to scale shape though a lack of clustering among many taxonomic and ecological groups may indicate that boundary layer use has reduced selective pressures from drag. Our results are consistent with others that have found both environment and phylogeny influence Teleost fish morphology.
Top-cited authors
Marcus W Feldman
  • Stanford University
Blake Matthews
  • Eawag: Das Wasserforschungs-Institut des ETH-Bereichs
Kevin Laland
  • University of St Andrews
Matheus Souza Lima-Ribeiro
  • Universidade Federal de Jataí
Vera Solferini
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