The evolution of static allometry in sexually selected traits

Although it has been the subject of verbal theory since Darwin, the evolution of morphological trait allometries remains poorly understood, especially in the context of sexual selection. Here we present an allocation trade-off model that predicts the optimal pattern of allometry under different selective regimes. We derive a general solution that has a simple and intuitive interpretation and use it to investigate several examples of fitness functions. Verbal arguments have suggested cost or benefit scenarios under which sexual selection on signal or weapon traits may favor larger individuals with disproportionately larger traits (i.e., positive allometry). However, our results suggest that this is necessarily true only under a precisely specified set of conditions: positive allometry will evolve when the marginal fitness gains from an increase in relative trait size are greater for large individuals than for small ones. Thus, the optimal allometric pattern depends on the precise nature of net selection, and simple examples readily yield isometry, positive or negative allometry, or polymorphisms corresponding to sigmoidal scaling. The variety of allometric patterns predicted by our model is consistent with the diversity of patterns observed in empirical studies on the allometries of sexually selected traits. More generally, our findings highlight the difficulty of inferring complex underlying processes from simple emergent patterns.     

The genomic basis of eco‐evolutionary dynamics

Recent recognition that ecological and evolutionary processes can operate on similar timescales has led to a rapid increase in theoretical and empirical studies on eco‐evolutionary dynamics. Progress in the fields of evolutionary biology, genomics and ecology is greatly enhancing our understanding of rapid adaptive processes, the predictability of adaptation and the genetics of ecologically important traits. However, progress in these fields has proceeded largely independently of one another. In an attempt to better integrate these fields, the centre for ‘Adaptation to a Changing Environment’ organized a conference entitled ‘The genomic basis of eco‐evolutionary change’ and brought together experts in ecological genomics and eco‐evolutionary dynamics. In this review, we use the work of the invited speakers to summarize eco‐evolutionary dynamics and discuss how they are relevant for understanding and predicting responses to contemporary environmental change. Then, we show how recent advances in genomics are contributing to our understanding of eco‐evolutionary dynamics. Finally, we highlight the gaps in our understanding of eco‐evolutionary dynamics and recommend future avenues of research in eco‐evolutionary dynamics.     

Eco-evolutionary dynamics

Evolutionary ecologists and population biologists have recently considered that ecological and evolutionary changes are intimately linked and can occur on the same time-scale. Recent theoretical developments have shown how the feedback between ecological and evolutionary dynamics can be linked, and there are now empirical demonstrations showing that ecological change can lead to rapid evolutionary change. We also have evidence that microevolutionary change can leave an ecological signature. We are at a stage where the integration of ecology and evolution is a necessary step towards major advances in our understanding of the processes that shape and maintain biodiversity. This special feature about ‘eco-evolutionary dynamics’ brings together biologists from empirical and theoretical backgrounds to bridge the gap between ecology and evolution and provide a series of contributions aimed at quantifying the interactions between these fundamental processes.     

A cascade of evolutionary change alters consumer-resource dynamics and ecosystem function

It is becoming increasingly clear that intraspecific evolutionary divergence influences the properties of populations, communities and ecosystems. The different ecological impacts of phenotypes and genotypes may alter selection on many species and promote a cascade of ecological and evolutionary change throughout the food web. Theory predicts that evolutionary interactions across trophic levels may contribute to hypothesized feedbacks between ecology and evolution. However, the importance of 'cascading evolutionary change' in a natural setting is unknown. In lakes in Connecticut, USA, variation in migratory behaviour and feeding morphology of a fish predator, the alewife (Alosa pseudoharengus), drives life-history evolution in a species of zooplankton prey (Daphnia ambigua). Here we evaluated the reciprocal impacts of Daphnia evolution on ecological processes in laboratory mesocosms. We show that life-history evolution in Daphnia facilitates divergence in rates of population growth, which in turn significantly alters consumer-resource dynamics and ecosystem function. These experimental results parallel trends observed in lakes. Such results argue that a cascade of evolutionary change, which has occurred over contemporary timescales, alters community and ecosystem processes.     

Rapid adaptation of herbivore consumers to nutrient limitation: eco‐evolutionary feedbacks to population demography and resource control

Humans alter biogeochemical cycles of essential elements such as phosphorus (P). Prediction of ecosystem consequences of altered elemental cycles requires integration of ecology, evolutionary biology and the framework of ecological stoichiometry. We studied micro‐evolutionary responses of a herbivorous rotifer to P‐limited food and the potential consequences for its population demography and for ecosystem properties. We subjected field‐derived, replicate rotifer populations to P‐deficient and P‐replete algal food, and studied adaptation in common garden transplant experiments after 103 and 209 days of selection. When fed P‐limited food, populations with a P‐limitation selection history suffered 37% lower mortality, reached twice the steady state biomass, and reduced algae by 40% compared to populations with a P‐replete selection history. Adaptation involved no change in rotifer elemental composition but reduced investment in sex. This study demonstrates potentially strong eco‐evolutionary feedbacks from shifting elemental balances to ecosystem properties, including grazing pressure and the ratio of grazer:producer biomass.     

Severity of impacts of an introduced species corresponds with regional eco‐evolutionary experience

Invasive plant impacts vary widely across introduced ranges. We tested the hypothesis that differences in the eco‐evolutionary experience of native communities with the invader correspond with the impacts of invasive species on native vegetation, with impacts increasing with ecological novelty. We compared plant species richness and composition beneath Pinus contorta to that in adjacent vegetation and other P. contorta stands across a network of sites in its native (Canada and USA) and non‐native (Argentina, Chile, Finland, New Zealand, Scotland, Sweden) ranges. At sites in North America and Europe, within the natural distribution of the genus Pinus, P. contorta was not associated with decreases in diversity. In the Southern Hemisphere, where there are no native Pinaceae, plant communities beneath P. contorta were less diverse than in other regions and compared to uninvaded native vegetation. Effects on native vegetation were particularly pronounced where P. contorta was a more novel life form and exhibited higher growth rates. Our results support the hypothesis that the eco‐evolutionary experience of the native vegetation, and thus the novelty of the invader, determines the magnitude of invader impacts on native communities. Understanding the eco‐evolutionary context of invasions will help to better understand and predict where invasion impacts will be greatest and to prioritize invasive species management.     

The implications of rapid eco‐evolutionary processes for biological control ‐ a review

Novel environmental conditions experienced by introduced species can drive rapid evolution of diverse traits. In turn, rapid evolution, both adaptive and non‐adaptive, can influence population size, growth rate, and other important ecological characteristics of populations. In addition, spatial evolutionary processes that arise from a combination of assortative mating between highly dispersive individuals at the expanding edge of populations and altered reproductive rates of those individuals can accelerate expansion speed. Growing experimental evidence shows that the effects of rapid evolution on ecological dynamics can be quite large, and thus it can affect establishment, persistence, and the distribution of populations. We review the experimental and theoretical literature on such eco‐evolutionary feedbacks and evaluate the implications of these processes for biological control. Experiments show that evolving populations can establish at higher rates and grow larger than non‐evolving populations. However, non‐adaptive processes, such as genetic drift and inbreeding depression can also lead to reduced fitness and declines in population size. Spatial evolutionary processes can increase spread rates and change the fitness of individuals at the expansion front. These examples demonstrate the power of eco‐evolutionary dynamics and indicate that evolution is likely more important in biocontrol programs than previously realized. We discuss how this knowledge can be used to enhance efficacy of biological control.     

Experimental evolution of a sexually selected display in yeast

The fundamental principle underlying sexual selection theory is that an allele conferring an advantage in the competition for mates will spread through a population. Remarkably, this has never been demonstrated empirically. We have developed an experimental system using yeast for testing genetic models of sexual selection. Yeast signal to potential partners by producing an attractive pheromone; stronger signallers are preferred as mates. We tested the effect of high and low levels of sexual selection on the evolution of a gene determining the strength of this signal. Under high sexual selection, an allele encoding a stronger signal was able to invade a population of weak signallers, and we observed a corresponding increase in the amount of pheromone produced. By contrast, the strong signalling allele failed to invade under low sexual selection. Our results demonstrate, for the first time, the spread of a sexually selected allele through a population, confirming the central assumption of sexual selection theory. Our yeast system is a powerful tool for investigating the genetics of sexual selection.     

Sexual selection and the evolution of secondary sexual traits: sex comb evolution in Drosophila

Sexual selection can drive rapid evolutionary change in reproductive behaviour, morphology and physiology. This often leads to the evolution of sexual dimorphism, and continued exaggerated expression of dimorphic sexual characteristics, although a variety of other alternative selection scenarios exist. Here, we examined the evolutionary significance of a rapidly evolving, sexually dimorphic trait, sex comb tooth number, in two Drosophila species. The presence of the sex comb in both D. melanogaster and D. pseudoobscura is known to be positively related to mating success, although little is yet known about the sexually selected benefits of sex comb structure. In this study, we used experimental evolution to test the idea that enhancing or eliminating sexual selection would lead to variation in sex comb tooth number. However, the results showed no effect of either enforced monogamy or elevated promiscuity on this trait. We discuss several hypotheses to explain the lack of divergence, focussing on sexually antagonistic coevolution, stabilizing selection via species recognition and nonlinear selection. We discuss how these are important, but relatively ignored, alternatives in understanding the evolution of rapidly evolving sexually dimorphic traits.     

The microevolutionary response to male‐limited X‐chromosome evolution in Drosophila melanogaster reflects macroevolutionary patterns

Due to its hemizygous inheritance and role in sex determination, the X‐chromosome is expected to play an important role in the evolution of sexual dimorphism and to be enriched for sexually antagonistic genetic variation. By forcing the X‐chromosome to only be expressed in males over >40 generations, we changed the selection pressures on the X to become similar to those experienced by the Y. This releases the X from any constraints arising from selection in females and should lead to specialization for male fitness, which could occur either via direct effects of X‐linked loci or trans‐regulation of autosomal loci by the X. We found evidence of masculinization via up‐regulation of male‐benefit sexually antagonistic genes and down‐regulation of X‐linked female‐benefit genes. Potential artefacts of the experimental evolution protocol are discussed and cannot be wholly discounted, leading to several caveats. Interestingly, we could detect evidence of microevolutionary changes consistent with previously documented macroevolutionary patterns, such as changes in expression consistent with previously established patterns of sexual dimorphism, an increase in the expression of metabolic genes related to mito‐nuclear conflict and evidence that dosage compensation effects can be rapidly altered. These results confirm the importance of the X in the evolution of sexual dimorphism and as a source for sexually antagonistic genetic variation and demonstrate that experimental evolution can be a fruitful method for testing theories of sex chromosome evolution.     

Patterns of rectrix rachis modification in pintails and the evolution of sexually selected traits

In order to transmit aerodynamic forces to the rest of the body, tail feathers need to be stiff to resist lift forces with minimum deformation. Because delta-wing theory predicts that such feathers do not produce lift forces beyond the point of the maximum continuum width of the tail, species with pintails should not require stiff central rectrices distal to that point. We tested this prediction by comparing the relative thickness of the central rectrix rachis in taxa with pintails and triangular tails. Fourteen pairs of closely related species or species groups belonging to the families Phaethontidae, Phalacrocoracidae, Anatidae, Stercorariidae, Psittacidae, Trochilidae, Alcedinidae, Momotidae, Meropidae, Bucerotidae, Tyrannidae, Pipridae and Nectariniidae were compared. Twelve of the phylogenetically independent comparisons showed that the taxa with triangular tails have higher relative rachis thickness (RRT) than their pintailed relatives just behind the point of the maximum continuum width of the tail. In contrast, two taxa with pintails showed proportionately higher RRT than their triangular-tailed relatives. Triangular tails showed an approximately linear relationship between RRT and relative rachis length, which contrasts with a proportionately greater increase in RRT from distal to proximal parts of the feather in 12 pintailed taxa. These results show that in most of the pintailed taxa studied the distal part of the central rectrix rachis has not been selected to resist lift forces and may be adaptively reduced to attenuate the costs of a hypertrophied ornament. However, the presence of distally reinforced rachices in Eumomota superciliosa and Colonia colonus suggests that a different explanation may be required to account for the design of pintail structure in other taxa.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 477–485.     

Age‐specific oxidative status and the expression of pre‐ and postcopulatory sexually selected traits in male red junglefowl, Gallus gallus

Oxidative stress is emerging as a key factor underpinning life history and the expression of sexually selected traits. Resolving the role of oxidative stress in life history and sexual selection requires a pluralistic approach, which investigates how age affects the relationship between oxidative status (i.e., antioxidants and oxidative damage) and the multiple traits contributing to variation in reproductive success. Here, we investigate the relationship between oxidative status and the expression of multiple sexually selected traits in two‐age classes of male red junglefowl, Gallus gallus, a species which displays marked male reproductive senescence. We found that, irrespective of male age, both male social status and comb size were strongly associated with plasma oxidative status, and there was a nonsignificant tendency for sperm motility to be associated with seminal oxidative status. Importantly, however, patterns of plasma and seminal antioxidant levels differed markedly in young and old males. While seminal antioxidants increased with plasma antioxidants in young males, the level of seminal antioxidants remained low and was independent of plasma levels in old males. In addition, old males also accumulated more oxidative damage in their sperm DNA. These results suggest that antioxidant allocation across different reproductive traits and somatic maintenance might change drastically as males age, leading to age‐specific patterns of antioxidant investment.     

Precopulatory but not postcopulatory male reproductive traits diverge in response to mating system manipulation in Drosophila melanogaster

Competition between males creates potential for pre‐ and postcopulatory sexual selection and conflict. Theory predicts that males facing risk of sperm competition should evolve traits to secure their reproductive success. If those traits are costly to females, the evolution of such traits may also increase conflict between the sexes. Conversely, under the absence of sperm competition, one expectation is for selection on male competitive traits to relax thereby also relaxing sexual conflict. Experimental evolution studies are a powerful tool to test this expectation. Studies in multiple insect species have yielded mixed and partially conflicting results. In this study, we evaluated male competitive traits and male effects on female costs of mating in Drosophila melanogaster after replicate lines evolved for more than 50 generations either under enforced monogamy or sustained polygamy, thus manipulating the extent of intrasexual competition between males. We found that in a setting where males competed directly with a rival male for access to a female and fertilization of her ova polygamous males had superior reproductive success compared to monogamous males. When comparing reproductive success solely in double mating standard sperm competition assays, however, we found no difference in male sperm defense competitiveness between the different selection regimes. Instead, we found monogamous males to be inferior in precopulatory competition, which indicates that in our system, enforced monogamy relaxed selection on traits important in precopulatory rather than postcopulatory competition. We discuss our findings in the context of findings from previous experimental evolution studies in Drosophila ssp. and other invertebrate species.     

Latitudinal variation and coevolutionary diversification of sexually dimorphic traits in the false blister beetle Oedemera sexualis

Sexual traits are subject to evolutionary forces that maximize reproductive benefits and minimize survival costs, both of which can depend on environmental conditions. Latitude explains substantial variation in environmental conditions. However, little is known about the relationship between sexual trait variation and latitude, although body size often correlates with latitude. We examined latitudinal variation in male and female sexual traits in 22 populations of the false blister beetle Oedemera sexualis in the Japanese Archipelago. Males possess massive hind legs that function as a female‐grasping apparatus, while females possess slender hind legs that are used to dislodge mounting males. Morphometric analyses revealed that male and female body size (elytron length), length and width of the hind femur and tibia, and allometric slopes of these four hind leg dimensions differed significantly among populations. Of these, three traits showed latitudinal variation, namely, male hind femur was stouter; female hind tibia was slenderer, and female body was smaller at lower latitudes than at higher latitudes. Hind leg sizes and shapes, as measured by principal component analysis of these four hind leg dimensions in each sex, covaried significantly between sexes, suggesting coevolutionary diversification in sexual traits. Covariation between sexes was weaker when variation in these traits with latitude was removed. These results suggest that coevolutionary diversification between male and female sexual traits is mediated by environmental conditions that vary with latitude.     

Genic capture and the genetic basis of sexually selected traits in the zebra finch

Abstract The lek paradox, in which female choice erodes genetic variation in male sexually selected traits, is a fundamental issue in sexual selection. If females gain only genetic benefits from preferentially having their ova fertilized by males with particular traits, what maintains variation in these traits? Under strong directional selection mediated through mate choice, the alleles for beneficial male traits are expected to go to fixation and exhibit little variation. A theoretical solution to the lek paradox is the genic capture hypothesis which states that: costly male traits subject to female choice are condition dependent, that male condition is dependent on genes at many loci and exhibits additive genetic variance, and that positive genetic correlations exist between sexually selected traits and condition. Using a captive population of the zebra finch Taeniopygia guttata, we tested two key predictions from this model: (1) that genetic variance exists in beak color which is a sexually selected trait, but also in condition and immune function, and (2) that positive genetic correlations exist between condition and beak color, and between beak color, condition, and immune function. Genetic parameters were estimated from a large breeding experiment involving 81 sires, 972 offspring, a pedigree of 1526 individuals, using the animal model. We employed the following index of body condition: residuals from a log‐log plot of body mass on tarsus length following a standardized and extended period of exercise, in which residual mass is known to reflect fat and protein reserves. Our results were broadly consistent with the genic capture hypothesis because we found (1) additive genetic variation in beak color and immune function and condition, and (2) positive genetic correlations between condition and beak color, and between condition, beak color, and several assays of immune responsiveness. However, both of these results need qualification. In the first case we identified an important general problem in estimating the coefficient of additive genetic variance (CV_A) in body condition. In the second case, although most of the genetic correlations were positive as predicted, only some were statistically significant, possibly due to our relatively small sample sizes, because genetic correlations typically have large standard errors and therefore require very large samples to be statistically significant. The statistically significant, positive genetic correlations included those between beak color and immune function (response to tetanus), and between immune function (response to tetanus) and condition, both of which indicate that females gain good genes from mating with males in good condition and/or with a redder beak color. We discuss the implications of our results for devising more rigorous but pragmatic tests of the genic capture hypothesis.     

Intralocus sexual conflict and the genetic architecture of sexually dimorphic traits in Prochyliza xanthostoma (Diptera: Piophilidae)

Because homologous traits of males and females are likely to have a common genetic basis, sex-specific selection (often resulting from sexual selection on one sex) may generate an evolutionary tug-of-war known as intralocus sexual conflict, which will constrain the adaptive divergence of the sexes. Theory suggests that intralocus sexual conflict can be mitigated through reduction of the intersexual genetic correlation (rMF), predicting negative covariation between rMF and sexual dimorphism. In addition, recent work showed that selection should favor reduced expression of alleles inherited from the opposite-sex parent (intersexual inheritance) in traits subject to intralocus sexual conflict. For traits under sexual selection in males, this should be manifested either in reduced maternal heritability or, when conflict is severe, in reduced heritability through the opposite-sex parent in offspring of both sexes. However, because we do not know how far these hypothesized evolutionary responses can actually proceed, the importance of intralocus sexual conflict as a long-term constraint on adaptive evolution remains unclear. In this study, we investigated the genetic architecture of sexual and nonsexual morphological traits in Prochyliza xanthostoma. The lowest rMF and greatest dimorphism were exhibited by two sexual traits (head length and antenna length) and, among all traits, the degree of sexual dimorphism was correlated negatively with rMF. Moreover, sexual traits exhibited reduced maternal heritabilities, and the most strongly dimorphic sexual trait (antenna length) was heritable only through the same-sex parent in offspring of both sexes. Our results support theory and suggest that intralocus sexual conflict can be resolved substantially by genomic adaptation. Further work is required to identify the proximate mechanisms underlying these patterns.     

The quantitative genetics of sexually selected traits,preferred traits and preference: a review and analysis of the data

The maintenance of variation in sexually selected traits is a puzzle that has received increasing attention in the past several decades. Traits that are related to fitness, such as life‐history or sexually selected traits, are expected to have low additive genetic variance (and hence, heritability) due to the rapid fixation of advantageous alleles. However, previous analyses have suggested that the heritabilities of sexually selected traits are on average higher than nonsexually selected traits. We show that the heritabilities of sexually selected traits are not significantly different from those of nonsexually selected traits overall or when separated into the three trait categories: behavioural, morphological and physiological. In contrast with previous findings, the heritability of preference is quite low (h² = 0.25 ± 0.06) and is in the same range as life‐history traits. We distinguish preferred traits as a category of sexually selected traits and find that the heritability of the former is not significantly different than sexually selected traits overall (0.48 ± 0.04 vs. 0.46 ± 0.03). We test the hypothesis that the heritability of sexually selected traits is negatively correlated with the strength of sexual selection. As predicted, there is a significant negative correlation between the heritabilities of sexually selected traits and the strength of selection. This suggests that heritabilities do indeed decrease as sexual selection increases but sexual selection is not strong enough to cause heritabilities of sexually selected traits to deviate from the same type of nonsexually selected traits.     

Prospecting and informed dispersal: Understanding and predicting their joint eco‐evolutionary dynamics

The ability of individuals to leave a current breeding area and select a future one is important, because such decisions can have multiple consequences for individual fitness, but also for metapopulation dynamics, structure, and long‐term persistence through non‐random dispersal patterns. In the wild, many colonial and territorial animal species display informed dispersal strategies, where individuals use information, such as conspecific breeding success gathered during prospecting, to decide whether and where to disperse. Understanding informed dispersal strategies is essential for relating individual behavior to subsequent movements and then determining how emigration and settlement decisions affect individual fitness and demography. Although numerous theoretical studies have explored the eco‐evolutionary dynamics of dispersal, very few have integrated prospecting and public information use in both emigration and settlement phases. Here, we develop an individual‐based model that fills this gap and use it to explore the eco‐evolutionary dynamics of informed dispersal. In a first experiment, in which only prospecting evolves, we demonstrate that selection always favors informed dispersal based on a low number of prospected patches relative to random dispersal or fully informed dispersal, except when individuals fail to discriminate better patches from worse ones. In a second experiment, which allows the concomitant evolution of both emigration probability and prospecting, we show the same prospecting strategy evolving. However, a plastic emigration strategy evolves, where individuals that breed successfully are always philopatric, while failed breeders are more likely to emigrate, especially when conspecific breeding success is low. Embedding information use and prospecting behavior in eco‐evolutionary models will provide new fundamental understanding of informed dispersal and its consequences for spatial population dynamics.