A Comparative Study of the Role of Sex-Specific Condition Dependence in the Evolution of Sexually Dimorphic Traits.
TL;DR: A comparative study suggests a common genetic/developmental basis of sexual dimorphism and sex-specific plasticity that evolves across the phylogeny—and that the evolution of size consistently alters scaling relationships and thus contributes to the allometric variation of sexual armaments or ornaments in animals.
Abstract: Sexual selection can displace traits acting as ornaments or armaments from their viability optimum in one sex, ultimately giving rise to sexual dimorphism. The degree of dimorphism should n...
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TL;DR: It is shown here that males of one species have proportionally larger weapons, and, despite that, males fight similarly to females in every aspect analyzed, suggesting that fighting per se might not be the sole source of selection to explain sexual dimorphism.
Abstract: Contesting scarce resources can trigger the evolution of specialized morphological structures (i.e., animal weapons). While most research focus on male weapons, females might also bear weapons, although generally smaller and less conspicuous than male weapons. Social selection is evoked to explain female weaponry in which females fight for nonsexual resources such as food and shelter. Males might fight for similar resources but are expected to have proportionally larger weapons due to additional inputs from sexual selection. We tested whether males have proportionally larger weapons than females in two species of Aegla crabs. Interestingly, only males of one species had proportionally larger claws than females. Given that these larger weapons typically correlate to increased aggression, we expected males to fight more intensely than females. Thus, we compared intrasexual contests of males and females of the same species. Females fought similarly to males: latency, contest duration, and frequency of highly aggressive acts were similar between the sexes. Therefore, despite males having proportionally larger weapons in one species (as predicted by sexual selection), they fought similarly to females. Our results hint that fighting might not necessarily be the source of selection for sexual dimorphism we typically expect. Other sources, such as the frequency of fighting and predation pressure, might be selecting larger claws in males despite the similar fights, while fecundity costs might downsize female claws. We highlight that comparing female with male weapons and the associated fighting behavior shows that selection on weapons is not as straightforward as we might think. We show that studying the highly neglected female weapon allometry and usage allows us to infer on the selective process acting on animal weapons. We show here that males of one species have proportionally larger weapons, and, despite that, males fight similarly to females in every aspect analyzed. Therefore, fighting per se might not be the sole source of selection to explain sexual dimorphism. Other sources, such as frequency of fighting, and how expensive it is to produce gametes might be additional sources of selection.
11 citations
TL;DR: It is shown that persistence is affected by sexual dimorphism for phenotypic plasticity, trait genetic architecture, and sex‐specific selection, and it is predicted that female‐biased adaptive plasticity—particularly in traits with modest‐to‐low cross‐sex genetic correlations—typically promotes persistence.
Abstract: Abstract Populations must adapt to environmental changes to remain viable. Both evolution and phenotypic plasticity contribute to adaptation, with plasticity possibly being more important for coping with rapid change. Adaptation is complex in species with separate sexes, as the sexes can differ in the strength or direction of natural selection, the genetic basis of trait variation, and phenotypic plasticity. Many species show sex differences in plasticity, yet how these differences influence extinction susceptibility remains unclear. We first extend theoretical models of population persistence in changing environments and show that persistence is affected by sexual dimorphism for phenotypic plasticity, trait genetic architecture, and sex‐specific selection. Our models predict that female‐biased adaptive plasticity—particularly in traits with modest‐to‐low cross‐sex genetic correlations—typically promotes persistence, though we also identify conditions where sexually monomorphic or male‐biased plasticity promotes persistence. We then perform a meta‐analysis of sex‐specific plasticity under manipulated thermal conditions. Although examples of sexually dimorphic plasticity are widely observed, systematic sex differences are rare. An exception—cold resistance—is systematically female‐biased and represents a trait wherein sexually dimorphic plasticity might elevate population viability in changing environments. We discuss our results in light of debates about the roles of evolution and plasticity in extinction susceptibility.
10 citations
TL;DR: In this paper, the authors used a flexible Bayesian generalized additive model framework (GAMM) to examine when and how sexual size dimorphism developed in body mass, tarsus length and bill length from hatching until fledging.
Abstract: Most studies on sexual size dimorphism address proximate and functional questions related to adults, but sexual size dimorphism usually develops during ontogeny and developmental trajectories of sexual size dimorphism are poorly understood We studied three bird species with variation in adult sexual size dimorphism: black coucals (females 69% heavier than males), white‐browed coucals (females 13% heavier than males) and ruffs (males 70% heavier than females) Using a flexible Bayesian generalized additive model framework (GAMM), we examined when and how sexual size dimorphism developed in body mass, tarsus length and bill length from hatching until fledging In ruffs, we additionally examined the development of intrasexual size variation among three morphs (Independents, Satellites and Faeders), which creates another level of variation in adult size of males and females We found that 27–100% of the adult inter‐ and intrasexual size variation developed until fledging although none of the species completed growth during the observational period In general, the larger sex/morph grew more quickly and reached its maximal absolute growth rate later than the smaller sex/morph However, when the daily increase in body mass was modelled as a proportion, growth patterns were synchronized between and within sexes Growth broadly followed sigmoidal asymptotic models, however only with the flexible GAMM approach, residual distributions were homogeneous over the entire observation periods These results provide a platform for future studies to relate variation in growth to selective pressures and proximate mechanisms in these three species, and they highlight the advantage of using a flexible model approach for examining growth variation during ontogeny
9 citations
TL;DR: The putative roles of developmental constraints and natural selection in the evolution of wing allometry in the Schizophora are discussed, suggesting a shared developmental programme underlying size‐dependent phenotypic plasticity.
Abstract: The proximate and ultimate mechanisms underlying scaling relationships as well as their evolutionary consequences remain an enigmatic issue in evolutionary biology. Here, I investigate the evolution of wing allometries in the Schizophora, a group of higher Diptera that radiated about 65 million years ago, by studying static allometries in five species using multivariate approaches. Despite the vast ecological diversity observed in contemporary members of the Schizophora and independent evolutionary histories throughout most of the Cenozoic, size-related changes represent a major contributor to overall variation in wing shape, both within and among species. Static allometries differ between species and sexes, yet multivariate allometries are correlated across species, suggesting a shared developmental programme underlying size-dependent phenotypic plasticity. Static allometries within species also correlate with evolutionary divergence across 33 different families (belonging to 11 of 13 superfamilies) of the Schizophora. This again points towards a general developmental, genetic or evolutionary mechanism that canalizes or maintains the covariation between shape and size in spite of rapid ecological and morphological diversification during the Cenozoic. I discuss the putative roles of developmental constraints and natural selection in the evolution of wing allometry in the Schizophora.
8 citations
Additional excerpts
...…Kleiber, 1947; Voje, Hansen, Egset, Bolstad, & Pelabon, 2014), others highlight the potential of particularly rapid divergence (Casasa et al., 2017; Emlen, 1996; Frankino, Zwaan, Stern, & Brakefield, 2005; Puniamoorthy, Blanckenhorn, & Schäfer, 2012; Rohner & Blanckenhorn, 2018; Wilkinson, 1993)....
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TL;DR: Contrary to expectation, wing morphology showed as much shape differentiation between evolutionary independent lineages as fore femora, providing no evidence for faster diversification of traits primarily engaged in mating.
Abstract: Sexual selection represents a potent force that can drive rapid population differentiation in traits related to reproductive success. Hence, sexual traits are expected to show greater population divergence than non‐sexual traits. We test this prediction by exploring patterns of morphological differentiation of the exaggerated fore femur (a male‐specific sexual trait) and the wing (a non‐sexual trait) among allopatric and sympatric populations of the widespread sister dung fly species Sepsis neocynipsea and Sepsis cynipsea (Diptera: Sepsidae). While both species occur in Eurasia, S. neocynipsea also abounds in North America, albeit previous studies suggest strong differentiation in morphology, behavior, and mating systems. To evaluate the degree of differentiation expected under neutrality between S. cynipsea, European S. neocynipsea, and North American S. neocynipsea, we genotyped 30 populations at nine microsatellite markers, revealing almost equal differentiation between and minor differentiation among geographic populations within the three lineages. Landmark‐based analysis of 18 populations reared at constant 18 and 24°C in a laboratory common garden revealed moderate temperature‐dependent phenotypic plasticity and significant heritable differentiation in size and shape of male forelegs and wings among iso‐female lines of the three lineages. Following the biological species concept, there was weaker differentiation between cross‐continental populations of S. neocynipsea relative to S. cynipsea, and more fore femur differentiation between the two species in sympatry versus allopatry (presumably due to character displacement). Contrary to expectation, wing morphology showed as much shape differentiation between evolutionary independent lineages as fore femora, providing no evidence for faster diversification of traits primarily engaged in mating.
8 citations
Cites background from "A Comparative Study of the Role of ..."
...…Morf, Reusch, & Reuter, 2000; Dmitriew & Blanckenhorn, 2012, Puniamoorthy, Blanckenhorn, & Schäfer, 2012; but see Ingram, Laamanen, Puniamoorthy, & Meier, 2008) as well as male–male competition (Busso & Blanckenhorn, 2018; Rohner & Blanckenhorn, 2018; Rohner, Blanckenhorn, & Puniamoorthy, 2016)....
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...Similarly, sex‐ ual dimorphism in fore femur width, and its condition dependence, co‐varies with the mating system in sepsids, suggesting sexual se‐ lection to act on fore femur morphology (Rohner & Blanckenhorn, 2018)....
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References
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TL;DR: In this article, a model is described in an lmer call by a formula, in this case including both fixed-and random-effects terms, and the formula and data together determine a numerical representation of the model from which the profiled deviance or the profeatured REML criterion can be evaluated as a function of some of model parameters.
Abstract: Maximum likelihood or restricted maximum likelihood (REML) estimates of the parameters in linear mixed-effects models can be determined using the lmer function in the lme4 package for R. As for most model-fitting functions in R, the model is described in an lmer call by a formula, in this case including both fixed- and random-effects terms. The formula and data together determine a numerical representation of the model from which the profiled deviance or the profiled REML criterion can be evaluated as a function of some of the model parameters. The appropriate criterion is optimized, using one of the constrained optimization functions in R, to provide the parameter estimates. We describe the structure of the model, the steps in evaluating the profiled deviance or REML criterion, and the structure of classes or types that represents such a model. Sufficient detail is included to allow specialization of these structures by users who wish to write functions to fit specialized linear mixed models, such as models incorporating pedigrees or smoothing splines, that are not easily expressible in the formula language used by lmer.
50,607 citations
"A Comparative Study of the Role of ..." refers methods in this paper
...To test for a general relationship independent of species and trait identity, we pooled all data and used a mixed model with species and trait as crossed random effects (using the lme4 R package; Bates et al. 2015)....
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2,096 citations
"A Comparative Study of the Role of ..." refers background in this paper
...That is, sexual selection may promote further evolutionary amplification of the hyperallometric male slope (Gould 1966; Bonduriansky 2007c), thus strengthening the relationship between sex-specific condition dependence and sexual dimorphism of particular secondary sexual and other morphologically…...
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TL;DR: Sexual dimorphism may result from natural and/or sexual selection, and systems of mating are often thought to evolve in response to ecological pressures, although mating preferences may be self-reinforcing.
Abstract: Conspicuous sexual dimorphism is a feature of many species of higher animals. The genetic basis of variation in metrical characters, including that in sexual dimorphism between families or lines, is usually polygenic (Falconer, 1960; Frankham, 1968b; Wright, 1968, 1977; Bird and Schaffer, 1972; Ehrman and Parsons, 1976). Genetic experiments on mice, birds and Drosophila flies indicate that artificial selection practiced on a character of one sex causes not only a direct response of the character in the selected sex, but also a correlated response of the homologous character, if any, in the opposite sex (Shaklee et al., 1952; Harrison, 1953; Korkman, 1957; Becker et al., 1964; Eisen and Legates, 1966; Frankham, 1968a, 1968b; Eisen and Hanrahan, 1972). Such correlated selective responses are attributable to pleiotropy (and linkage) of genes affecting the characters of both sexes, that is, correlations between the additive effects of genes as expressed in males and females. The genetic correlation between homologous characters of the sexes is often quite high (op. cit.). As will be shown, this greatly restricts the rate of evolution of sexual dimorphism relative to that for the average phenotype of the two sexes. Sexual dimorphism may result from natural and/or sexual selection. Darwin (1874, Part 2) elucidated how natural selection operating differently on males and females arises from their distinctive roles in reproduction, or from competition between the sexes for resources such as food, leading to adaptive sexual dimorphism. He also reasoned that intrasexual contests for mates and intersexual mating preferences exert sexual selection, usually on the males, producing sexual dimorphism which is maladaptive with respect to natural selection. Comparisons within and between closely related species led Darwin to conclude that adult males typically are more modified than adult females or juveniles of either sex, but that females have often acquired male characters by "transference." It was difficult for Darwin to believe that sex-limitation of characters could evolve by selection, but Fisher (1958, Ch. 6) outlined how divergent selection on the two sexes could accumulate genes with different effects in males and females, causing a character at first expressed equally in both sexes to become sexually dimorphic and finally sex-limited. The strength of sexual selection is enhanced by a polygamous mating system, but the possibility of sexual selection in monogamous systems of mating exists due to male competition for early-breeding females, and mate choice exercised by these females (Darwin, 1874; Fisher, 1958; O'Donald, 1977). Systems of mating are often thought to evolve in response to ecological pressures (reviewed by Selander, 1972; Brown, 1975; Emlen and Oring, 1977), although mating preferences may be self-reinforcing (Fisher, 1958; O'Donald, 1967, 1977; Lande, unpubl.). Darwin and Fisher described qualitative methods by which an observed sexual dimorphism could be attributed mainly to either natural or sexual selection. To assign natural selection as the primary cause requires ecological observations that males and females follow different ways of life and employ the dimorphic character(s) adaptively in their distinct modes of survival or reproduction. Darwin presented several such examples, mostly among the lower classes of animals. Selander (1972) 292
1,692 citations
"A Comparative Study of the Role of ..." refers background in this paper
...However, even under consistent and sexually antagonistic directional selection, the evolution of sexual dimorphism in any trait must be hampered by genetic correlations between sexes (Lande 1980)....
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...…recent, and in response, sex-specific condition dependence (i.e., plasticity) may be more likely to evolve than functional genetic sex differences, particularly if plasticity can better alleviate any constraints imposed by strong genetic correlations between sexes (as argued above; Lande 1980)....
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TL;DR: This paper offers a resolution to the lek paradox and rests on only two assumptions; condition dependence of sexually selected traits and high genetic variance in condition, which lead inevitably to the capture of genetic variance into sexually selected trait concomitantly with the evolution of condition dependence.
Abstract: Recent evidence suggests that sexually selected traits have unexpectedly high genetic variance. In this paper, we offer a simple and general mechanism to explain this observation. Our explanation offers a resolution to the lek paradox and rests on only two assumptions; condition dependence of sexually selected traits and high genetic variance in condition. The former assumption is well supported by empirical evidence. We discuss the evidence for the latter assumption. These two assumptions lead inevitably to the capture of genetic variance into sexually selected traits concomitantly with the evolution of condition dependence. We present a simple genetic model to illustrate this view. We then explore some implications of genic capture for the coevolution of female preference and male traits. Our exposition of this problem incidentally leads to new insights into the similarities between sexually selected traits and life history traits, and therefore into the maintenance of high genetic variance in the latter. Finally, we discuss some shortcomings of a recently proposed alternative solution to the lek paradox; selection on variance.
1,330 citations
"A Comparative Study of the Role of ..." refers background in this paper
...…dependence—a form of phenotypic plasticity linking an individual’s genomewide genetic quality to trait expression under a given amount of resources (Rowe and Houle 1996)—allows for a flexible trade-off of survival costs that arise through trait exaggeration with the corresponding reproductive…...
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...Thus, in species subjected to an increased degree of sex-specific directional selection on a given trait (e.g., followingmating system evolution), sexual dimorphism should become amplified and so should the benefit of condition dependence (Rowe and Houle 1996)....
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...…bear particular traits typically varies to the extent that only individuals in good condition—that is, those with access to more metabolic resources (Rowe and Houle 1996)—will be able to afford expressing a certain degree of trait exaggeration that then can act as an indicator of their intrinsic…...
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TL;DR: If ecological causation for dimorphism can be demonstrated in so many cases, despite the inadequacies of the available criteria, the degree of sexual sizeDimorphism in many other animal species may well also have been influenced by ecological factors, and it may be premature of dismiss this hypothesis.
Abstract: Can sexual dimorphism evolve because of ecological differences between the sexes? Although several examples of this phenomenon are well known from studies on birds, the idea has often been dismissed as lacking general applicability. This dismissal does not stem from contradictory data so much as from the difficulties inherent in testing the hypothesis, and its apparent lack of parsimony, in comparison to the alternative explanation of sexual selection. The only unequivocal evidence for the evolution of sexual dimorphism through intersexual niche partitioning would be disproportionate dimorphism in trophic structures (e.g., mouthparts). This criterion offers a minimum estimate of the importance of ecological causes for dimorphism, because it may fail to identify most cases. A review of published literature reveals examples of sexually dimorphic trophic structures in most animal phyla. Many of these examples seem to be attributable to sexual selection, but others reflect adaptations for niche divergence between the sexes. For example, dwarf non-feeding males without functional mouthparts have evolved independently in many taxa. In other cases, males and females differ in trophic structures apparently because of differences in diets. Such divergence may often reflect specific nutritional requirements for reproduction in females, or extreme (sexually selected?) differences between males and females in habitats or body sizes. Ecological competition between the sexes may be responsible for intersexual niche divergence in some cases, but the independent evolution of foraging specializations by each sex may be of more general importance. If ecological causation for dimorphism can be demonstrated in so many cases, despite the inadequacies of the available criteria, the degree of sexual size dimorphism in many other animal species may well also have been influenced by ecological factors. Hence, it may be premature to dismiss this hypothesis, despite the difficulty of testing it.
1,312 citations
"A Comparative Study of the Role of ..." refers background in this paper
...This contrasts with cases where dimorphism is associated with selection driven by ecological nichedifferentiationbetween sexes (i.e., ecological sexual dimorphism; Shine 1989, 1991; Temeles et al. 2000)....
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...…does not impose major constraints, the displacement from the viability selection optimum reflects the net costs and benefits of (exaggerated) trait expression (which may not be the case if dimorphism is due to ecological character displacement; e.g., Shine 1989, 1991; Temeles et al. 2000)....
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...…optima, resulting from variation in the strength, shape, and direction of natural and sexual selection between the sexes (Hedrick and Temeles 1989; Shine 1989; Blanckenhorn 2005; Fairbairn et al. 2007; although the specific role of ecology in shaping sexual dimorphisms remains contentious,…...
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