Darrell J. Kemp

Can older males deliver the good genes

Females of many species choose to mate with old rather than young males, possibly because older males pass superior genes on to their offspring. Recent theoretical and empirical investigations have rejuvenated interest in the evolution of mating preferences based on age, and in the relationship between longevity and fitness. If the cost of signalling is a reduction in future survival and reproduction, mate choice based on age is one possible outcome when males signal their genetic quality. These recent investigations highlight the importance of understanding sexual selection from a life-history perspective.

Residency effects in animal contests.

The question of why territorial residents usually win asymmetrical owner-intruder contests is critical to our understanding of animal contest evolution. Game theory suggests that, under certain conditions, residency could be used as an arbitrary means of contest settlement in a manner analogous to tossing a coin. Key empirical support for this idea is provided by a study on the speckled wood butterfly (Pararge aegeria); however, this result has proven controversial. We show conclusively that residency does not serve as an arbitrary cue for contest settlement in this species. By means of a series of manipulative experiments, conducted on two phenotypically divergent populations of P. aegeria, we also rule out the recently presented alternative that contests are settled due to resource-correlated asymmetries in thoracic temperature. Our results instead suggest that more intrinsically aggressive males accumulate as residents and continue to win due to the self-reinforcing effect of prior winning experience. Truly arbitrary contest settlement may be rare or non-existent in the wild.

CONDITION DEPENDENCE, QUANTITATIVE GENETICS, AND THE POTENTIAL SIGNAL CONTENT OF IRIDESCENT ULTRAVIOLET BUTTERFLY COLORATION

Abstract Structural colors result from an interaction between light and the fine-scale physical structure of a surface, and are often extremely bright, chromatic, and iridescent. Given that these visual features depend upon the aggregate abundance and architectural precision of photonic structures, structurally colored sexual ornaments seem well placed to indicate a range of mate quality characteristics. We tested this hypothesis by investigating the signaling potential of structural coloration in the sexually dimorphic butterfly Colias eurytheme. Males of this species display iridescent ultraviolet (UV) markings (arising from multilayer thin films) that overlay a broad area of yellowish-orange pigmentation on their dorsal wing surface. Only the structural UV has demonstrated function as a sexual signal; hence we predicted that it should contain more reliable phenotypic and/or genetic quality information, which would be indicated by phenotypic and/or genetically mediated condition dependence. In two split-family breeding experiments we manipulated condition by exposing full siblings to different stressors at two different juvenile life-history stages: (1) reduced larval host-plant quality and (2) transient heat/cold shocks during metamorphosis. Both stressors had profound effects on key developmental and life-history traits. Each stressor also significantly affected male dorsal coloration; thus, the expression of both structural and pigmentary coloration is phenotypically condition dependent. As predicted, the strongest condition dependence was evident in the brightness and angular visibility (i.e., iridescence) of the UV. Characteristics of both the iridescent UV and pigmentary orange also exhibited moderate-high and significant heritability (H2~h2~ 0.4–0.9). However, genetic and residual variances did not increase under stress; thus, the observed condition dependence was not genetically mediated as predicted if wing color trait signals “good” genes for the ability to either withstand or circumvent developmental stress. The heightened stress sensitivity of the iridescent UV suggests that it offers an informative lifetime indicator of juvenile environments and, henceforth, adult male phenotypic condition, which may be salient to females seeking a highly fertile and/or nutritious male ejaculate.

An Integrative Framework for the Appraisal of Coloration in Nature

The world in color presents a dazzling dimension of phenotypic variation. Biological interest in this variation has burgeoned, due to both increased means for quantifying spectral information and heightened appreciation for how animals view the world differently than humans. Effective study of color traits is challenged by how to best quantify visual perception in nonhuman species. This requires consideration of at least visual physiology but ultimately also the neural processes underlying perception. Our knowledge of color perception is founded largely on the principles gained from human psychophysics that have proven generalizable based on comparative studies in select animal models. Appreciation of these principles, their empirical foundation, and the reasonable limits to their applicability is crucial to reaching informed conclusions in color research. In this article, we seek a common intellectual basis for the study of color in nature. We first discuss the key perceptual principles, namely, retinal photoreception, sensory channels, opponent processing, color constancy, and receptor noise. We then draw on this basis to inform an analytical framework driven by the research question in relation to identifiable viewers and visual tasks of interest. Consideration of the limits to perceptual inference guides two primary decisions: first, whether a sensory-based approach is necessary and justified and, second, whether the visual task refers to perceptual distance or discriminability. We outline informed approaches in each situation and discuss key challenges for future progress, focusing particularly on how animals perceive color. Given that animal behavior serves as both the basic unit of psychophysics and the ultimate driver of color ecology/evolution, behavioral data are critical to reconciling knowledge across the schools of color research.

Female butterflies prefer males bearing bright iridescent ornamentation

Butterflies are among natures most colourful animals, and provide a living showcase for how extremely bright, chromatic and iridescent coloration can be generated by complex optical mechanisms. The gross characteristics of male butterfly colour patterns are understood to function for species and/or sex recognition, but it is not known whether female mate choice promotes visual exaggeration of this coloration. Here I show that females of the sexually dichromatic species Hypolimnas bolina prefer conspecific males that possess bright iridescent blue/ultraviolet dorsal ornamentation. In separate field and enclosure experiments, using both dramatic and graded wing colour manipulations, I demonstrate that a moderate qualitative reduction in signal brightness and chromaticity has the same consequences as removing the signal entirely. These findings validate a long-held hypothesis, and argue for the importance of intra- versus interspecific selection as the driving force behind the exaggeration of bright, iridescent butterfly colour patterns.

Gaping Displays Reveal and Amplify a Mechanically Based Index of Weapon Performance

Physical prowess, a key determinant of fight outcomes, is contingent on whole‐organism performance traits. The advertisement of performance, via display, is poorly understood because it is unclear how information about performance is encoded into display characteristics. Previous studies have shown that weapon performance (i.e., bite force) predicts dominance and reproductive success in male lizards. We tested the hypothesis that gaping displays by adult male collared lizards (Crotaphytus) can provide an index of weapon performance by exposing the major jaw‐adductor muscle complex and that white patches at the mouth corners amplify this index. For territorial adult males, the breadth of the muscle complex, which is not correlated with body size, was a strong predictor of bite force. For nonterritorial yearling males and females, however, measures of body and head size predicted bite force. The patches are highly conspicuous, exhibit UV‐reflecting properties within the visual range of lizards, and provide size‐independent information about bite force only in adult males. We conclude that exposure of the muscle complex during gaping displays can provide rival males with a reliable, body‐size independent, biomechanically based index of weapon performance, an index that the mouth‐corner patches amplify. Indexes that transmit information through mechanistic links to performance are expected to be widespread among animals.

Lifetime Resource Utilization, Flight Physiology, and the Evolution of Contest Competition in Territorial Insects

Adaptationist analyses of animal contests have contributed much to our understanding of behavioral evolution. One class of contest, however, the war of attrition, has proven difficult to interpret. In wars of attrition involving aerial displays, there is evidence that asymmetries in performance parameters such as flight energetics may be important determinants of contest resolution. This paradigm is not universal, however, and we presently lack a framework for understanding why certain biophysical parameters are important only in some cases. One possibility is that the relevance of these parameters is determined by evolutionarily conserved life‐history‐scale patterns of resource allocation and acquisition. We evaluated this hypothesis by investigating the correlates of competitive success in two territorial insects that exemplify markedly different lifetime patterns of resource utilization. We found that in the bot fly Cuterebra austeni, an extreme capital breeding species that depends entirely on energy acquired during its immature stages, territorial residency was most strongly correlated with a size‐independent measure of energetic availability. In contrast, residency in the tarantula hawk wasp Hemipepsis ustulata was best predicted by variation in body size per se. Adult H. ustulata are able to supplement their larval‐derived nutrient capital in the manner of an income breeder, and fuel reserves were independent of age and actually correlated negatively with residency in this species. These results underscore how the study of sexually selected phenomena may be enriched by an explicit consideration of life‐history principles.

Contest behaviour in the speckled wood butterfly (Pararge aegeria): seasonal phenotypic plasticity and the functional significance of flight performance

Although contemporary animal contest theory emphasises the importance of physical asymmetries in resolving disputes, such asymmetries do not obviously settle fights in all groups. Territorial male butterflies, for example, compete via elaborate non-contact aerial interactions in which success is determined by relative persistence. Prior research suggests that the resolution of these contests is not clearly related to physical variables such as body size or energy reserves. However, given that the contests involve elaborate aerial manoeuvres, one long-standing suggestion is that asymmetries in flight performance, and thus flight morphology, may be important. We addressed this hypothesis via a manipulative investigation into the biophysical correlates of contest success in the speckled wood butterfly, Pararge aegeria. This species possesses the ability for significant adaptive phenotypic plasticity in relevant flight morphological parameters. We took advantage of this plasticity to rear 90 individuals of markedly varying flight morphologies, which we then pitted against each other in a semi-controlled experimental fashion. Multiple logistic and lognormal analyses provided little evidence for the relevance of morphological parameters, including relative flight musculature, wing loading and wing aspect ratio (wing length relative to area), to the outcome and/or duration of experimental contests. Instead, we found a positive effect of age upon contest success. Given that ability for high acceleration is strongly linked to variation in these morphological parameters, our findings suggest that flight performance is not a strong determinant of resource-holding potential in this notably territorial butterfly.

Mating success of resident versus non-resident males in a territorial butterfly

Male–male competition over territorial ownership suggests that winning is associated with considerable benefits. In the speckled wood butterfly, Pararge aegeria, males fight over sunspot territories on the forest floor; winners gain sole residency of a sunspot, whereas losers patrol the forest in search of females. It is currently not known whether residents experience greater mating success than non-residents, or whether mating success is contingent on environmental conditions. Here we performed an experiment in which virgin females of P. aegeria were allowed to choose between a resident and a non-resident male in a large enclosure containing one territorial sunspot. Resident males achieved approximately twice as many matings as non-residents, primarily because matings were most often preceded by a female being discovered when flying through a sunspot. There was no evidence that territorial residents were more attractive per se, with females seen to reject them as often as non-residents. Furthermore, in the cases where females were discovered outside of the sunspot, they were just as likely to mate with non-residents as residents. We hypothesize that the proximate advantage of territory ownership is that light conditions in a large sunspot greatly increase the males ability to detect and intercept passing receptive females.

Multimodal signalling: structural ultraviolet reflectance predicts male mating success better than pheromones in the butterfly Colias eurytheme L. (Pieridae)

In sexual selection, multimodal signals elicit mate choice when more than one sensory modality is activated. However, determining the relative use of each signal is difficult because it requires a comprehensive understanding of the mating system and how this system works under natural conditions. We examined the role of structural ultraviolet (UV) reflectance and pheromones in the butterfly Colias eurytheme. Both traits are important in mediating interspecific interactions and pheromones have been implicated in intraspecific mate choice. UV reflectance, which arises from the presence of a multilayer thin-film interference array, has potential as an honest indicator of male condition, viability and/or age. We investigated the relevance of these signal traits to courtship success by releasing virgin females in the path of free-flying males until each female had rejected and accepted at least one male. This design facilitated a within-subjects (females) analysis of mate choice, thus controlling for potentially confounding variation in intrinsic female receptivity. Principal component analysis indicated that variation across males in UV brightness and pheromones was essentially orthogonal. Females preferred younger males (as subjectively adjudged by wing wear), and while age covaried with UV brightness and almost all pheromone descriptors, UV brightness emerged as the best and most general predictor of male mating success. Our results suggest that this trait serves as an important intraspecific sexual signal in C. eurytheme, and they provide the clearest evidence to date regarding the functional relevance of structural coloration to female mate choice in butterflies. We discuss the preferential use of one secondary sexual characteristic (UV reflectance) over another (pheromones) with regard to evolutionary strategies.