The evolution of male-biased sexual size dimorphism is associated with increased body size plasticity in males
TL;DR: The findings indicate that primarily selection on size, rather than the reproductive role per se, drives the evolution of sex-specific body size plasticity, which is congruent with theory in suggesting that condition dependence plays a pivotal role in the Evolution of sexual size dimorphism.
Abstract: 1. Sexual size dimorphism (SSD) can vary drastically across environments, demonstrating pronounced sex-specific plasticity. In insects, females are usually the larger and more plastic sex. However, the shortage of taxa with male-biased SSD hampers the assessment of whether the greater plasticity in females is driven by selection on size or represents an effect of the female reproductive role. Here, we specifically address the role of sex-specific plasticity of body size in the evolution of SSD reversals to disentangle sex and size effects.
2. We first investigate sex-specific body size plasticity in Sepsis punctum and Sepsis neocynipsea as two independent cases of intraspecific SSD reversals in sepsid flies. In both species, directional variation in SSD between populations is driven by stronger sexual selection on male size. Using controlled laboratory breeding, we find evidence for sex-specific plasticity and increased condition dependence of male size in populations with male-biased SSD, but not of female size in populations with female-biased SSD.
3. To extend the comparative scope, we next estimate sex-specific body size plasticity in eight additional fly species that differ in the direction of SSD under laboratory conditions. In all species with male-biased SSD we find males to be the more plastic sex, while this was only rarely the case in species with female-biased SSD, thus suggesting a more general trend in Diptera.
4. To examine the generality of this pattern in holometabolous insects, we combine our data with data from the literature in a meta-analysis. Again, male body size tends to be more plastic than female size when males are the larger sex, though female size is now also generally more plastic when females are larger.
5. Our findings indicate that primarily selection on size, rather than the reproductive role per se, drives the evolution of sex-specific body size plasticity. However, sepsid flies, and possibly Diptera in general, show a clear sexual asymmetry with greater male than female plasticity related to SSD, likely driven by strong sexual selection on males. Although further research controlling for phylogenetic and ecological confounding effects is needed, our findings are congruent with theory in suggesting that condition dependence plays a pivotal role in the evolution of sexual size dimorphism.
Citations
More filters
TL;DR: Studies of adaptive evolution under rapid environmental change should consider the possibility that phenotypic plasticity of sexually selected male traits, even if it elevates male fitness, could have a negative effect on female reproductive output, thereby increasing the risk of population extinction.
Abstract: In a rapidly changing environment, does sexual selection on males elevate a population's reproductive output? If so, does phenotypic plasticity enhance or diminish any such effect? We outline two routes by which sexual selection can influence the reproductive output of a population: a genetic correlation between male sexual competitiveness and female lifetime reproductive success; and direct effects of males on females' breeding success. We then discuss how phenotypic plasticity of sexually selected male traits and/or female responses (e.g. plasticity in mate choice), as the environment changes, might influence how sexual selection affects a population's reproductive output. Two key points emerge. First, condition-dependent expression of male sexual traits makes it likely that sexual selection increases female fitness if reproductively successful males disproportionately transfer genes that are under natural selection in both sexes, such as genes for foraging efficiency. Condition-dependence is a form of phenotypic plasticity if some of the variation in net resource acquisition and assimilation is attributable to the environment rather than solely genetic in origin. Second, the optimal allocation of resources into different condition-dependent traits depends on their marginal fitness gains. As male condition improves, this can therefore increase or, though rarely highlighted, actually decrease the expression of sexually selected traits. It is therefore crucial to understand how condition determines male allocation of resources to different sexually selected traits that vary in their immediate effects on female reproductive output (e.g. ornaments versus coercive behaviour). In addition, changes in the distribution of condition among males as the environment shifts could reduce phenotypic variance in certain male traits, thereby reducing the strength of sexual selection imposed by females. Studies of adaptive evolution under rapid environmental change should consider the possibility that phenotypic plasticity of sexually selected male traits, even if it elevates male fitness, could have a negative effect on female reproductive output, thereby increasing the risk of population extinction. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.
36 citations
TL;DR: A comparative, interdisciplinary approach is taken to explore various hypotheses about how sex differences in aging arise and discusses genomic, morphological, and environmental differences between the sexes and how these relate to sex Differences in aging.
Abstract: Sex differences in aging occur in many animal species, and they include sex differences in lifespan, in the onset and progression of age‐associated decline, and in physiological and molecular markers of aging. Sex differences in aging vary greatly across the animal kingdom. For example, there are species with longer‐lived females, species where males live longer, and species lacking sex differences in lifespan. The underlying causes of sex differences in aging remain mostly unknown. Currently, we do not understand the molecular drivers of sex differences in aging, or whether they are related to the accepted hallmarks or pillars of aging or linked to other well‐characterized processes. In particular, understanding the role of sex‐determination mechanisms and sex differences in aging is relatively understudied. Here, we take a comparative, interdisciplinary approach to explore various hypotheses about how sex differences in aging arise. We discuss genomic, morphological, and environmental differences between the sexes and how these relate to sex differences in aging. Finally, we present some suggestions for future research in this area and provide recommendations for promising experimental designs.
27 citations
TL;DR: It is found that studying several traits simultaneously at minimum permits better interpretation in case of multiple, potentially conflicting trends or hypotheses concerning the macroecology of insects, and little support for confounding interrelations between body size, wing loading and range size in this taxon is found.
Abstract: Support for macroecological rules in insects is mixed, with potential confounding interrelations between patterns rarely studied. We here investigate global patterns in body and wing size, sexual size dimorphism and range size in common fruit flies (Diptera: Drosophilidae) and explore potential interrelations and the predictive power of Allen's, Bergmann's, Rensch's and Rapoport's rules. We found that thorax length (r2 = 0.05) and wing size (r2 = 0.09) increased with latitude, supporting Bergmann's rule. Contrary to patterns often found in endothermic vertebrates, relative wing size increased towards the poles (r2 = 0.12), a pattern against Allen's rule, which we attribute to selection for increased flight capacity in the cold. Sexual size dimorphism decreased with size, evincing Rensch's rule across the family (r2 = 0.14). Yet, this pattern was largely driven by the virilis – repleta radiation and only weakly in other lineages. Finally, range size did not correlate with latitude, although a positive relationship with latitude was present in a subset of the species investigated, providing no convincing evidence for Rapoport's rule. We further found little support for confounding interrelations between body size, wing loading and range size in this taxon. Nevertheless, we demonstrate that studying several traits simultaneously at minimum permits better interpretation in case of multiple, potentially conflicting trends or hypotheses concerning the macroecology of insects.
23 citations
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...
22 citations
Cites background or methods from "The evolution of male-biased sexual..."
...S1, available online); it was therefore used as our best estimate of overall body size (as in previous studies; e.g., Martin and Hosken 2004; Blanckenhorn 2007; Rohner et al. 2018)....
[...]
...Moreover, previous studies have demonstrated considerable variation in mating systems among taxa that goes hand in hand with sex-specific directional selection and directional variation in sexual size dimorphism (SSD; Puniamoorthy et al. 2012a, 2012b; Rohner et al. 2016, 2018)....
[...]
...Sepsid flies consequently exhibit strongly plastic responses to food quantity and quality, involving both development time and adult body size (adult dry weight of siblings can vary by a factor of 10; Zerbe 1993; see also Blanckenhorn 1999; Dmitriew and Blanckenhorn 2014; Rohner et al. 2018)....
[...]
...As some taxa investigated here secondarily evolved malebiased sexual size dimorphism (Rohner et al. 2016, 2018), comparing absolute trait sizes between species does not necessarily reflect sex differences in the relative investment in a trait....
[...]
...Aligning with the overall sexspecific body-size plasticity, which generally correlates with the degree and direction of SSD across insects (Teder and Tammaru 2005; Stillwell et al. 2010; Rohner et al. 2018), we here found trait-specific support for this pattern across species....
[...]
TL;DR: This work raised fathead minnows, Pimephales promelas, under different levels of background predation risk in a split-clutch design and studied morphology in both juveniles and adults, finding no evidence for inducible morphological defences in females.
Abstract: Although comprehending the significance of phenotypic plasticity for evolution is of major interest in biology, the pre-requirement for that, the understanding of variance in plasticity, is still in its infancy. Most researchers assess plastic traits at single developmental stages and pool results between sexes. Here, we study variation among sexes and developmental stages in inducible morphological defences, a well-known instance of plasticity. We raised fathead minnows, Pimephales promelas, under different levels of background predation risk (conspecific alarm cues or distilled water) in a split-clutch design and studied morphology in both juveniles and adults. In accordance with the theory that plasticity varies across ontogeny and sexes, geometric morphometry analyses revealed significant shape differences between treatments that varied across developmental stages and sexes. Alarm cue-exposed juveniles and adult males developed deeper heads, deeper bodies, longer dorsal fin bases, shorter caudal peduncles and shorter caudal fins. Adult alarm cue-exposed males additionally developed a larger relative eye size. These responses represent putative adaptive plasticity as they are linked to reduced predation risk. Perhaps most surprisingly, we found no evidence for inducible morphological defences in females. Understanding whether similar variation occurs in other taxa and their environments is crucial for modelling evolution.
19 citations
References
More filters
Journal Article•
TL;DR: Copyright (©) 1999–2012 R Foundation for Statistical Computing; permission is granted to make and distribute verbatim copies of this manual provided the copyright notice and permission notice are preserved on all copies.
Abstract: Copyright (©) 1999–2012 R Foundation for Statistical Computing. Permission is granted to make and distribute verbatim copies of this manual provided the copyright notice and this permission notice are preserved on all copies. Permission is granted to copy and distribute modified versions of this manual under the conditions for verbatim copying, provided that the entire resulting derived work is distributed under the terms of a permission notice identical to this one. Permission is granted to copy and distribute translations of this manual into another language, under the above conditions for modified versions, except that this permission notice may be stated in a translation approved by the R Core Team.
272,030 citations
"The evolution of male-biased sexual..." refers methods in this paper
...All analyses were conducted in r (R Core Team, 2016) using the package lme4 (Bates, Machler, Bolker, & Walker, 2015)....
[...]
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
TL;DR: In this paper, a tool changer is disclosed for automatically removing a working tool after having been used from the spindle of a machine tool such as a vertical milling machine, transferring the used working tool to a rack which stores a plurality of working tools.
Abstract: A tool changer is disclosed for automatically removing a working tool after having been used from the spindle of a machine tool such as a vertical milling machine, transferring the used working tool to a rack which stores a plurality of working tools, picking up from the rack another working tool for the next machining operation, transferring such new working tool to the spindle, and operatively mounting such new working tool on the spindle.
1,887 citations
TL;DR: The common slope of the fecundity/size relationship is close to 1 and this indicates that female size is a principal constraint on insect potential FECundity.
Abstract: The relationship between intra-specific variation in female body size and potential fecundity was investigated using the published literature on 57 oviparous species of Coleoptera, Diptera, Ephemeroptera, Heteroptera, Homoptera, Hymenoptera, Lepidoptera, and Trichoptera, and 11 species of larviparous Aphidina and Diptera. Female body sizes were converted to dry body weight. Variation in body weight and fecundity was expressed as percentage deviation from the median values. The increase in fecundity with body weight was similar in most taxa, with only a few important exceptions. The common regression for oviparous and larviparous species predicts a 0.95% increase in median fecundity for each 1% increase in dry body weight. The number of ovarioles (in 10 species of Coleoptera, Diptera, Hymenoptera and Orthoptera) also increased with body weight. The general relationship predicted a 0.81% increase in ovariole number for each 1% increase in dry body weight. The slope of ovariole number versus weight relationship was greater in species with many ovarioles than in species with few. The common slope of the fecundity/size relationship is close to 1 and this indicates that female size is a principal constraint on insect potential fecundity.
1,504 citations
"The evolution of male-biased sexual..." refers background in this paper
...In insects, females are generally larger than males due to a strong size–fecundity relationship (Honek, 1993)....
[...]
...The strength and type of selection on body size often differ between males and females, owing to their distinct reproductive roles favouring divergent fitness optima (Blanckenhorn, 2000, 2005; Fairbairn, 2013; Fairbairn, Blanckenhorn, & Székely, 2007; Honek, 1993; Shine, 1989)....
[...]
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
"The evolution of male-biased sexual..." refers background in this paper
...Originally proposed to explain variation in ornament size via genic capture, condition dependence is predicted to link genome- wide genetic quality of an individual to the expression of its secondary sexual traits in a given environment (Rowe & Houle, 1996)....
[...]
...…the condition dependence hypothesis posits that plasticity increases by strong directional selection for resource- use efficiency and so captures interactive genetic and environmental effects (Amend et al., 2013; Bonduriansky, 2007a; Oudin, Bonduriansky, & Rundle, 2015; Rowe & Houle, 1996)....
[...]
...The evolution of stronger condition dependence in males compared to females, allowing to flexibly counterbalance costs depending on environmental circumstances, thus seems to have some adaptive value (Bonduriansky, 2007a, 2007b; Rowe & Houle, 1996)....
[...]