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Viability Costs of Condition-Dependent Sexual Male Display in a Drumming Wolf Spider
Abstract
According to the conditional handicap models females use male ornaments as honest signals of male viability. The assumptions for honest signalling are that the traits are costly and that they reflect male phenotypic condition, and hence optimal trait size is largest in the most viable males. However, experimental evidence for the costs of signalling are scarce. In this study we experimentally tested whether acoustic signalling, drumming, in a wolf spider Hygrolycosa rubrofasciata is a condition dependent, costly trait, and thus offers an honest signal of quality to females. Males of this species court females by drumming dry leaves with their abdomen. Females prefer to mate with males of high drumming rate, but body mass of males does not affect female choice. We manipulated phenotypic condition of males by keeping them in high, intermediate and low food levels. Males in a high food level treatment maintained their drumming rate at a high level, while males with intermediate and low food levels exhibited a reduction in drumming rates. Thus, phenotypic condition of the males affects their sexual signalling. We induced another set of males to increase their drumming activity by presenting females in proximity. These males suffered higher mortality and lost significantly more weight than other males, confirming that drumming is costly. However, within the increased treatment group males that drummed most actively survived better than less active males. Thus, males vary in their ability to bear the costs of drumming, which suggests that drumming is an honest signal of male quality (= conditional handicap) for females.
... Such context-or environment-dependent effects are not uncommon. Traits that are useful during competitive interactions, like conspicuous traits to attract mates (Dougherty, 2021;Mappes et al., 1996;Woods et al., 2007) or fighting appendages like antlers or horns (Emlen, 2008;Miller, 2013), are costly to produce, but expression costs likely depend on the environment, at least partly. Indeed, individuals that grow in better conditions or are better provisioned often show more extravagant traits without suffering a greater cost of expression (Mappes et al., 1996;Vehrencamp et al., 1989). ...
... Traits that are useful during competitive interactions, like conspicuous traits to attract mates (Dougherty, 2021;Mappes et al., 1996;Woods et al., 2007) or fighting appendages like antlers or horns (Emlen, 2008;Miller, 2013), are costly to produce, but expression costs likely depend on the environment, at least partly. Indeed, individuals that grow in better conditions or are better provisioned often show more extravagant traits without suffering a greater cost of expression (Mappes et al., 1996;Vehrencamp et al., 1989). The suggestion from our analysis is that context-dependent traits of the sort should become linked to characters that improve the environment when this environment is bequeathed to relatives. ...
Organisms continuously modify their environment, often impacting the fitness of future conspecifics due to ecological inheritance. When this inheritance is biased towards kin, selection favours modifications that increase the fitness of downstream individuals. How such selection shapes trait variation within populations remains poorly understood. Using mathematical modelling, we investigate the coevolution of multiple traits in a group-structured population when these traits affect the group environment, which is then bequeathed to future generations. We examine when such coevolution favours polymorphism as well as the resulting associations among traits. We find in particular that two traits become associated when one trait affects the environment while the other influences the likelihood that future kin experience this environment. To illustrate this, we model the coevolution of (a) the attack rate on a local renewable resource, which deteriorates environmental conditions, with (b) dispersal between groups, which reduces the likelihood that kin suffers from such deterioration. We show this often leads to the emergence of two highly-differentiated morphs: one that readily disperses and depletes local resources; and another that maintains these resources and tends to remain philopatric. More broadly, we suggest that ecological inheritance can contribute to phenotypic diversity and lead to complex polymorphism.
... One hypothesis called the handicap principle suggests that sexual traits are costly, and 40 these costs ensure that trait expression is not arbitrary. Costly traits lower fitness by reducing 41 survival (Kotiaho et al., 1998;Møller & de Lope, 1994;Mappes et al., 1996) Individuals should therefore express traits at a level that maximizes their benefits relative to their 44 unit of cost (Grafen, 1990a(Grafen, , 1990bNur & Hasson, 1984;Zahavi, 1977). For example, the 45 handicap principle posits that sexually selected traits scale with quality because low-quality 46 individuals pay more for, or benefit less from, costly traits compared to high-quality individuals. ...
... Females 391 prefer to mate with males that drum at higher rates . However, drumming is 392 energetically demanding and, sometimes, lethal (Kotiaho, 2000;Mappes et al., 1996). Males fed 393 high-volume diets are better able to sustain and survive these costs compared to males on low-394 volume diets (Kotiaho, 2000). ...
Evolutionary theory suggests that individuals should express costly traits at a magnitude that optimizes the trait bearer’s cost-benefit difference. Trait expression varies across a species because costs and benefits vary among individuals. For example, if large individuals pay lower costs than small individuals, then larger individuals should reach optimal cost-benefit differences at greater trait magnitudes. Using the cavitation-shooting weapons found in the big claws of male and female snapping shrimp, we test whether size- and sex-dependent expenditures explain scaling and sex differences in weapon size. We found that males and females from three snapping shrimp species (Alpheus heterochaelis, Alpheus angulosus, and Alpheus estuariensis) show patterns consistent with tradeoffs between weapon and abdomen size. For male A. heterochaelis, the species for which we had the greatest statistical power, smaller individuals showed steeper tradeoffs. Our extensive dataset in A. heterochaelis also included data about pairing, breeding season, and egg clutch size. Therefore, we could test for reproductive tradeoffs and benefits in this species. Female A. heterochaelis exhibited tradeoffs between weapon size and egg count, average egg volume, and total egg mass volume. For average egg volume, smaller females exhibited steeper tradeoffs. Furthermore, in males but not females, large weapons were positively correlated with the probability of being paired and the relative size of their pair mates. In conclusion, we identified size-dependent tradeoffs that could underlie reliable scaling of costly traits. Furthermore, weapons are especially beneficial to males and burdensome to females, which could explain why males have larger weapons than females.
... Traits that are proportional to size or condition might therefore change with decreasing size or condition (Ryan and Brenowitz 1985;Hagman and Forsman 2003;Bonduriansky 2007;Han et al. 2020). For example, in acoustic signals, body mass is typically negatively correlated with dominant frequency (i.e., pitch; Gillooly and Ophir 2010), and body condition is generally positively correlated with more exaggerated expression of temporal features such as call rate (Mappes et al. 1996;Scheuber et al. 2003;Humfeld 2013). If mass and condition decline under climate change, dominant frequency of signals could increase and temporal features could "slow down" concomitantly. ...
Climate change is altering species' habitats, phenology, and behavior. Although sexual behaviors impact population persistence and fitness, climate change's effects on sexual signals are understudied. Climate change can directly alter temperature-dependent sexual signals, cause changes in body size or condition that affect signal production, or alter the selective landscape of sexual signals. We tested whether temperature-dependent mating calls of Mexican spadefoot toads (Spea multiplicata) had changed in concert with climate in the southwestern United States across 22 years. We document increasing air temperatures, decreasing rainfall, and changing seasonal patterns of temperature and rainfall in the spadefoots' habitat. Despite increasing air temperatures, spadefoots' ephemeral breeding ponds have been getting colder at most elevations, and male calls have been slowing as a result. However, temperature-standardized call characters have become faster, and male condition has increased, possibly due to changes in the selective environment. Thus, climate change might generate rapid, complex changes in sexual signals with important evolutionary consequences.
... Energetic costs of vibrational signaling have been so far studied only in four arthropod species, the tenebrionid beetle Psammodes striatus (Lighton 1987), the wolf spider Hygrolycosa rubrofasciata (Kotiaho et al. 1998a), the bushcricket Docidocercus gigliotosi (Römer et al. 2010), and the leafhopper Aphrodes makarovi (Kuhelj et al. 2015b). Indicatively, since male drumming in H. rubrofasciata is audible to humans, in the original publications on sexual selection and associated costs in this species, the authors either described drumming exclusively as an air-borne signal or mentioned the possibility that it may be perceived as substrateborne vibrations as less likely Mappes et al. 1996;Parri et al. 1997;Kotiaho et al. 1998a,b;Kotiaho et al. 1999;Rivero et al. 2000) and only later acknowledged the importance of the vibrational channel (e.g., Kotiaho et al. 2004;Huber 2005). As shown in Table 4.2, P. striatus and D. gigliotosi are relatively large insects, while H. rubrofasciata and A. makarovi are smaller and comparable in size. ...
Costs associated with the production of signals used in sexual communication play a central role in the sexual selection theory. Arthropods relying on substrate-borne vibrations have often been included among examples of acoustic communication; however, taking into account that air-borne and substrate-borne mechanical signals are subject to different selection pressures when they travel through the environment via different transmission media, the costs associated with the production of these two types of mechanical signals are also likely to differ. So far, remarkably little is known about costs associated with substrate-borne vibrational communication. In this chapter, we provide an overview of our current knowledge on energy expenditure associated with the production of vibrational signals and indirect costs of male vibrational signaling. We also discuss some technical challenges encountered when measuring respiration rates and determining a relationship between the effort of vibrational signaling and survival. Our goal is to point out an important gap in our understanding of vibrational communication systems and stimulate further studies in this area.
... For example, large weapons can increase predation risk [6] and impose tradeoffs with primary sexual characteristics [7,8]. Weapons can also impose energetic costs that reduce viability and fitness [9]. Most studies of energetic costs focus on signalling and growth, which can be ephemeral if weapon growth is episodic [10]. ...
The cost-minimization hypothesis proposes that positive allometry in sexually selected traits can be explained if the proportional energetic maintenance costs of weapons decrease as traits increase in size. Energetic maintenance costs are the costs of maintaining homeostasis. They are slow, persistent energy sinks that are distinct from ephemeral costs of growth. Because some tissues expend more energy on maintenance than others, energetic maintenance costs can be inferred from proportional tissue composition. For example, soft tissues require more energy for maintenance than exoskeleton, so an arthropod claw that is 50% soft tissue and 50% exoskeleton would have higher energetic maintenance costs than one that is 30% soft tissue and 70% exoskeleton. I tested the cost-minimization hypothesis using proportional tissue composition as a proxy for energetic maintenance costs in snapping shrimp ( Alpheus heterochaelis and Alpheus estuariensis ) and fiddler crabs ( Uca pugilator ). As predicted, larger weapons comprised proportionally less soft tissue mass and more exoskeleton mass than smaller weapons. Furthermore, I extended cost-minimization to explain trait exaggeration: individuals might exaggerate traits by investing more mass in exoskeleton. As predicted, exoskeleton mass proportional to weapon mass increased as exaggeration increased. These results support and extend the cost-minimization hypothesis to explain positive allometry and weapon exaggeration.
Evolutionary theory suggests that individuals should express costly traits at a magnitude that optimizes the cost-benefit ratio for the trait-bearer. Trait expression varies across a species because costs and benefits vary among individuals. For example, if large individuals pay lower costs than small individuals, then larger individuals should reach optimal cost-benefit ratios at a greater magnitude of trait expression. Using the remarkable cavitation-shooting weapons found in the big claws of male and female alpheid snapping shrimp, we test whether size- and sex-dependent expenditures explain the scaling of weapon size relative to body size and why males have larger proportional weapon size than females. We found that males and females from three snapping shrimp species ( Alpheus heterochaelis, Alpheus angulosus, and Alpheus estuariensis ) exhibit resource allocation tradeoffs between weapon and abdomen mass. For male A. heterochaelis , the species for which we had the greatest sample size and statistical power, the smallest individuals showed the steepest tradeoff. Our extensive dataset in A. heterochaelis also included data about pairing, breeding season, and egg clutch size. Therefore, we could test for reproductive tradeoffs and benefits in this species. Female A. heterochaelis exhibited additional tradeoffs between weapon size and egg count, average egg volume, and total egg mass volume. For average egg volume, the smallest females exhibited the steepest tradeoff relative to weapon size. Furthermore, in males but not females, large weapons were positively correlated with the probability of being paired and the relative size of their pair mate. In conclusion, we establish that size-dependent tradeoffs underlie reliable scaling relationships of costly traits. Furthermore, we show that males and females differ in weapon investment, suggesting that weapons are especially beneficial to males and especially burdensome to females.
Spiders are often underestimated as suitable behavioural models because of the general belief that due to their small brains their behaviour is innate and mostly invariable. Challenging this assumption, this fascinating book shows that rather than having a limited behavioural repertoire, spiders show surprising cognitive abilities, changing their behaviour to suit their situational needs. The team of authors unravels the considerable intra-specific as well as intra-individual variability and plasticity in different behaviours ranging from foraging and web building to communication and courtship. An introductory chapter on spider biology, systematics and evolution provides the reader with the necessary background information to understand the discussed behaviours and helps to place them into an evolutionary context. Highlighting an under-explored area of behaviour, this book will provide new ideas for behavioural researchers and students unfamiliar with spiders as well as a valuable resource for those already working in this intriguing field.
Many of the most spectacular and beautiful traits of animals function in communication. A second focus will be the relationship between animal communication and human language. Human language is far more complex and cognitively sophisticated than the communication system of any non-human animal. Signal reliability is an important issue for any communication system that is informational. Signals subject to a physical constraint are termed index signals and are often considered to be inherently honest because of an inescapable relationship between a signal feature and the physical characteristics of the signaler. The best known hypothesis for how signal costs can produce signal reliability is the handicap principle of Amotz Zahavi. Eavesdropping refers to the use of signals by unintended receivers and represents another way that signaling systems can be diverted from the functions for which they originally evolved. In the study of human language, pragmatics concerns how context influences communication in general and meaning in particular.
Body size, nuptial gift characteristics and courtship behaviour, among other traits, can reflect the quality of a potential mate and, thus, might be under sexual selection. To maximize their mating success, individuals can show behavioural plasticity in sexual context. Allocosa senex is a burrow-digging wolf spider that exhibits reversal courtship roles and in sexual size-dimorphism expected for spiders. Males construct the mating refuge and females prefer males that build longer burrows, which are considered as nuptial gifts because they are delivered to them after mating. This study aims to determine whether male body size and female reproductive status influence burrow dimensions, courtship displays, female preferences and cannibalism rate in A. senex. For that purpose, we allowed males to construct burrows and performed sexual trials under laboratory conditions. Larger males were more courted by females, and in turn, they expressed more vibratory behaviours during courtship. However, and contrary to our expectations, smaller males constructed longer burrows. We suggest that males of A. senex exhibit size-dependent behavioural plasticity, and when they are smaller, they invest more in burrow construction to compensate their lower opportunities of courting intensively as larger males. In addition, females courted differentially according to their reproductive status, overriding male preferences for virgin females. This study opens several doors to future research regarding mutual choice in A. senex and the traits assessed by males and females during courtship, as well as about the influence of intrinsic and extrinsic factors shaping reproductive decision-making in this and other wandering spider species.
Fisher's runaway process is the standard explanation of the evolution of exaggerated female preferences. But mathematical formulations of Fisher's process (haploid and additive diploid) show it cannot cause stable exaggeration if female preference carries a cost. At equilibrium female fitness must be maximized. Our analysis shows that evolutionary stable exaggeration of female preference can be achieved if mutation pressure on the male character is biased, that is, mutation has a directional effect. At this equilibrium female fitness is not maximized. We discuss the reasons and evidence for believing that mutation pressure is typically biased. Our analysis highlights the previously unacknowledged importance of biased mutation for sexual selection.
Males of Cystosoma saundersii produced their calling songs while tethered to holders. Oxygen consumption during singing was 0·136 ml min−1, equivalent to 45· 0 mW, an increase of 42· 55 mW over the resting metabolic rate. Maximum sound output was 90·6 dB at 20 cm. The whole sound-field was measured and represents a power output of 0·35 mW. The efficiency of sound production is 0·82%. Heat production, estimated from the weight of singing muscle, was 28·7 mW. This leaves 13·5 mW of output unaccounted for. Comparison with other species of insects suggests that none are more than an order of magnitude more efficient than C. saundersii.
Females are often believed to actively choose highly ornamented males (males with extravagant morphological signals or intense sexual display), and ornaments should be honest signals of male viability. However, this belief is relying only on some pieces of empirical evidence from birds. Our study reports active female choice on sexual display that indicates male viability in spiders. We established trials in which we studied female choice in relation to male courtship drumming activity and body size. Females chose the most actively drumming males as mating partners, but the body size of the males did not seem to be selected. Male drumming activity turned out to be a good predictor of male viability, whereas male viability was independent of male body mass. Our results suggest that by actively choosing mates according to male drumming performance, but independently of male body mass, females are preferring viable males as mates. Because Hygrolycosa rubrofasciata males do not provide obvious direct benefits to their offspring, females may gain some indirect benefits; offspring may have higher chance of survival, or the offspring may inherit the attractiveness of their father.
Fisher's runaway process is the standard explanation of the evolution of exaggerated female preferences. But mathematical formulations of Fisher's process (haploid and additive diploid) show it cannot cause stable exaggeration if female preference carries a cost. At equilibrium female fitness must be maximized. Our analysis shows that evolutionary stable exaggeration of female preference can be achieved if mutation pressure on the male character is biased, that is, mutation has a directional effect. At this equilibrium female fitness is not maximized. We discuss the reasons and evidence for believing that mutation pressure is typically biased. Our analysis highlights the previously unacknowledged importance of biased mutation for sexual selection.
The proportion of phenotypic variance in the length of the sexually selected tail of the monogamous barn swallow Hirundo rustica that is attributable to genetic variance was studied in the field in Denmark during a seven-year period. Tail length was on average 20% greater in males than in females. Tail length correlated with wing length, but not with other morphological traits. Tail length increased with the first molt, but remained constant during subsequent years. Changes in tail length between years, owing to molt were significantly affected by sex and by degree of infection with an haematophagous mite (Ornithonyssus bursa). There were significant differences in sexual size dimorphism between years, apparently as a result of environmental conditions in the African winter quarters during molt. Tail length was a highly repeatable morphological trait, and standardization of tail length for age effects only marginally increased repeatability. Heritability of tail length as estimated from regression of values for sons on those of their fathers was 0.59. This suggests that secondary sexual traits affected by strong directional selection still may show a statistically significant heritability.
The evolution of reliable signaling can be explained by the handicap principle, which assumes that(1) the cost of a signal guarantees its reliability, and (2) cheating is prevented because the cost of a unit of display is greater for low-quality than for high-quality individuals. A test of these two assumptions was performed using manipulations of the length of the outermost tail feathers of male barn swallows Hirundo rustica, a trait currently subject to a directional female mate preference. We found that survival decreased with tail elongation and increased with tail shortening of males, supporting the assumption that the secondary sexual character is costly. Naturally long-tailed males were better able to survive with an elongated tail, whereas naturally short-tailed males improved their survival following tail shortening. This observation supports the second assumption of a differential cost of a signal. One mechanism imposing differential costs on sexually signaling barn swallows is foraging. Males with elongated tails captured smaller, less profitable Diptera, whereas males with shortened tails captured large, profitable prey items. The conditions for reliable sexual signaling by the tail ornament of male barn swallows are thus fulfilled.
Males of Uperoleia rugosa form aggregations around the breeding pond. Within the aggregations, each calling male maintains an exclusive zone in which it does not tolerate another calling male. However, attacks on silent intruders, satellite males or females were never observed. Territorial males warned calling intruders by changing from advertisement calls to encounter calls (a display); if the intruder persisted in calling the resident would either attack or retreat and call elsewhere. Fights were usually won by the heavier males, and males of similar weight were more likely to fight, whereas males retreated from opponents that were substantially heavier. Calling was energetically costly and territorial males lost weight and thus their fighting abilities declined, whereas silent satellite males gained weight and were able to oust lighter territorial males. There was thus a dynamic interchange between territorial and satellite males depending on their relative weights. The playback of recorded advertisement calls showed that males can assess each others' fighting abilities on the basis of their vocalizations. Males retreated from a loudspeaker broadcasting the calls of a larger male but they attacked the loudspeaker if the calls of smaller or similar sized males were played (N=39, P<0·001, one-tailed binomial test). Dominant frequency was probably the call parameter used in assessment as it was correlated with the weight (r=−0·71, P<0·001, N=100) and hence the fighting ability of the caller, but this hypothesis needs further testing.
Territorial behaviour of Rana clamitans was studied in an experimental pond containing natural vegetation and artificial shelters. Males defended territories from June through August. Five vocalizations were used in territorial advertisement and agonistic encounters. Agonistic behaviour included patrolling, splashing displays, chases, attacks and wrestling. About 23% of all encounters ended in wrestling bouts. Most bouts were less than 30 s long, but some lasted up to 45 min. Most fights were won by residents. Intruders were most successful in fights when they were larger than residents or previously had been residents of other territories. Weight loss by large males enabled some smaller males to oust residents from territories. Possible costs of fighting include energetic costs and exposure to predation. Large male body size in R. clamitans and other territorial frogs may be an adaptation for fighting.
Precopulatory mate guarding is the habit, practised by many species, of the two sexes' joining together in intimate pairs for some time, usually days, before mating. It is mainly found in species in which mating is confined to a very short period of the female's reproductive cycle. A mathematical model confirms that precopula will evolve when mating is restricted in time. The model also specifies the evolutionary stable duration of precopula. There are two models: in the simpler, males cannot take over paired females; in the second, larger males can take over females from smaller males. In the model with takeovers, larger males guard for less time than smaller males, and the average guarding duration for all males is shorter than in the model in which there were no takeovers.