Experimental evidence of condition‐dependent sexual dimorphism in the weakly dimorphic antler fly Protopiophila litigata (Diptera: Piophilidae)
01 Sep 2015-Biological Journal of The Linnean Society (John Wiley & Sons, Ltd)-Vol. 116, Iss: 1, pp 211-220
TL;DR: A shared developmental basis to condition dependence and sexual dimorphism can arise via sexual selection on males even in lineages lacking highly exaggerated male traits, as previously reported for highly dimorphic species.
Abstract: Sexually dimorphic traits have a history of directional selection for exaggeration in at least one sex. Theory suggests that traits targeted by persistent selection should evolve heightened condition dependence whereby their expression reflects the availability and processing efficiency of metabolic resources. This joint dependence of sexual dimorphism and condition dependence on directional selection should result in a positive correlation between the extent of sexual dimorphism and the strength of condition dependence. However, because direct phenotypic evidence is predominately from species with highly exaggerated male traits, it remains unclear whether condition-dependent sexual dimorphism is characteristic of species with more typical levels of dimorphism. We manipulated condition via larval diet and quantified sex-specific responses in adult body size and shape in a moderately dimorphic dipteran species, the antler fly Protopiophila litigata. While dimorphism did not increase with diet quality within any trait, among traits the extent of dimorphism was positively associated with the strength of condition dependence in males but not females, as previously reported for highly dimorphic species. This finding suggests that a shared developmental basis to condition dependence and sexual dimorphism can arise via sexual selection on males even in lineages lacking highly exaggerated male traits. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 116, 211–220.
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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.
44 citations
TL;DR: RNAseq analysis is used to build on recent work exploring mechanisms in the exaggerated weapons of beetles, by examining patterns of differential gene expression in exaggerated and non‐exaggerated traits in the Asian rhinoceros beetle, Trypoxylus dichotomus, to suggest that sexually dimorphic expression of weaponry involves large‐scale changes in gene expression, relative to other traits, while nutrition‐driven changes inGene expression in these same weapons are less pronounced.
Abstract: Among the most dramatic examples of sexual selection are the weapons used in battles between rival males over access to females. As with ornaments of female choice, the most "exaggerated" sexually selected weapons vary from male to male more widely than other body parts (hypervariability), and their growth tends to be more sensitive to nutritional state or physiological condition compared with growth of other body parts ("heightened" conditional expression). Here, we use RNAseq analysis to build on recent work exploring these mechanisms in the exaggerated weapons of beetles, by examining patterns of differential gene expression in exaggerated (head and thorax horns) and non-exaggerated (wings, genitalia) traits in the Asian rhinoceros beetle, Trypoxylus dichotomus. Our results suggest that sexually dimorphic expression of weaponry involves large-scale changes in gene expression, relative to other traits, while nutrition-driven changes in gene expression in these same weapons are less pronounced. However, although fewer genes overall were differentially expressed in high- vs. low-nutrition individuals, the number of differentially expressed genes varied predictably according to a trait's degree of condition dependence (head horn > thorax horn > wings > genitalia). Finally, we observed a high degree of similarity in direction of effects (vectors) for subsets of differentially expressed genes across both sexually dimorphic and nutritionally responsive growth. Our results are consistent with a common set of mechanisms governing sexual size dimorphism and condition dependence.
33 citations
TL;DR: Although it is shown weapons are highly condition dependent, and changes in weapon expression and dimorphism could alter evolutionary dynamics, populations are unlikely to experience further evolutionary changes under current conditions.
Abstract: Sexually-selected traits are often highly variable in size within populations due to their close link with the physical condition of individuals. Nutrition has a large impact on physical condition, and thus any seasonal changes in nutritional quality are predicted to alter the average size of sexually-selected traits as well as the degree of sexual dimorphism in populations. However, while traits affected by mate choice are well-studied, we have a surprising lack of knowledge of how natural variation in nutrition affects the expression of sexually-selected weapons and sexual dimorphism. Further, few studies explicitly test for differences in the heritability and mean-scaled evolvability of sexually-selected traits across conditions. Using the insect, Narnia femorata (Hemiptera: Coreidae), an insect where males use their hind legs as weapons and the femurs are enlarged, we studied the extent to which weapon expression, sexual dimorphism, and evolvability change across the actual range of nutrition available in the wild. We found that insects raised on a poor diet (cactus without fruit) are nearly monomorphic, while those raised on a high quality diet (cactus with ripe fruit) are distinctly sexually dimorphic via the expression of large hind leg weapons in males. Contrary to our expectations, we found little evidence of a potential for evolutionary change for any trait measured. Thus, although we show weapons are highly condition dependent, and changes in weapon expression and dimorphism could alter evolutionary dynamics, our populations are unlikely to experience further evolutionary changes under current conditions.
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31 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 from "Experimental evidence of condition‐..."
...…studies explicitly investigating the relationship between dimorphism and sex-specific condition dependence suggest a positive correlation (Bonduriansky and Rowe 2005; Bonduriansky 2007a; Punzalan et al. 2008; Johns et al. 2014; Oudin et al. 2015; but see Cayetano and Bonduriansky 2015)....
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TL;DR: It is shown that the developmental diet has profound effects on both weapon and testis expression and scaling, and normal, seasonal fluctuations in the nutritional environment may play a large role in the expression of sexually selected traits and the ability of these traits to respond to selection.
Abstract: The size of weapons and testes can be central to male reproductive success. Yet, the expression of these traits is often extremely variable. Studies are needed that take a more complete organism perspective, investigating the sources of variation in both traits simultaneously and using developmental conditions that mimic those in nature. In this study, we investigated the components of variation in weapon and testis sizes using the leaf-footed cactus bug, Narnia femorata (Hemiptera: Coreidae) on three natural developmental diets. We show that the developmental diet has profound effects on both weapon and testis expression and scaling. Intriguingly, males in the medium-quality diet express large weapons but have relatively tiny testes, suggesting complex allocation decisions. We also find that heritability, evolvability, and additive genetic variation are highest in the high-quality diet for testis and body mass. This result suggests that these traits may have an enhanced ability to respond to selection during a small window of time each year when this diet is available. Taken together, these results illustrate that normal, seasonal fluctuations in the nutritional environment may play a large role in the expression of sexually selected traits and the ability of these traits to respond to selection.
22 citations
References
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TL;DR: A quantitative test of the prediction that a multivariate sexual display consisting of a suite of contact pheromones termed “cuticular hydrocarbons” in Drosophila serrata was unusually condition dependent relative to other CHC combinations within the population, consistent with the evolution of heightened condition dependence of sexual displays in response to persistent sexual selection.
Abstract: Theory predicts that costly sexual displays should evolve condition dependence if the marginal fitness gain from trait exaggeration is greater for high- than for low-condition individuals and that the strength of condition dependence should increase with the strength of directional selection. While there is substantial support for the first prediction, evidence for the latter is much weaker. We undertook a quantitative test of this prediction for a multivariate sexual display consisting of a suite of contact pheromones termed “cuticular hydrocarbons” (CHCs) in Drosophila serrata. We performed a dietary manipulation of condition (i.e., the pool of metabolic resources available for allocation to fitness-enhancing traits) within a half-sibling breeding design, thereby also providing insight into the genetic basis of condition dependence. As predicted, the linear combination of CHCs under the strongest sexual selection from female mate preferences was unusually condition dependent relative to other CH...
42 citations
TL;DR: The results suggest that environmental variation may influence the extent of sexual dimorphism in antler length, as female calves more than males appear to prioritize their antler growth over body mass, especially when resources are limited.
Abstract: We analysed intercohort variability of live weight and antler length of 5,123 reindeer calves. We further assessed the influence of climate and density on the interannual variation in antler length, and discussed sex-specific resource allocation and response to climate variability. Antler length varied significantly among years and between sexes, with interaction between year and sex. Body weight and antler length were highly positively correlated, showed similar intercohort variability, and had a strong allometrical link, suggesting that antler length could be an equally reliable measure of calf condition as live weight. We found a relative measure of antler length (i.e. antler length corrected for the allometric effect of body mass) to be positively influenced by increasing density and May–June precipitation, and also decreasing May–June temperature. We attributed the effect of early summer weather to its influence on forage availability and quality as well as the level of parasitic insect harassment. Gender difference in both the allometric exponents and the interannual variability suggest that young males and females may have different tactics for relative resource allocation towards growth of antlers as compared to body mass. Because antlers are costly to produce, they may be an honest signal of individual quality for both sexes. However, we found gender-specific allometry, as female calves more than males appear to prioritize their antler growth over body mass, especially when resources are limited. Thus, our results suggest that environmental variation may influence the extent of sexual dimorphism in antler length.
32 citations
TL;DR: The antler fly Protopiophila litigata Bonduriansky forms large mating/oviposition aggregations on discarded moose antlers, where the strikingly aggressive males are strikingly aggressive.
Abstract: The antler fly Protopiophila litigata Bonduriansky (Diptera Piophilidae) forms large mating/oviposition aggregations on discarded moose (Alces alces) antlers, where the strikingly aggressive males engage in frequent combat. According to theory, costly fighting behaviour will be maintained by selection only if winners sire more progeny than losers. Through a field study of individually marked flies, we addressed the question “Why do male antler flies fight?“ by investigating what resources males compete for on antlers, whether or not large male body size and resulting advantage in agonistic encounters confers positional advantage in the mating aggregation, and whether the successful males experience greater survivorship or greater mating frequency. As expected, most agonistic contests were won by the larger male. Large males tended to live longer, mate more frequently, and achieve more matings over their lifetimes than small males. Males fought and defended territories primarily on the upward-facing (‘uppe...
28 citations
TL;DR: Evidence is found for a complex genetic architecture underlying the reaction norms and differences between males and females in Drosophila melanogaster, and for the extent of independence implies specific regulatory genes or only a specific allelic regulation of trait genes.
Abstract: We examined the genetic architecture of plasticity of thorax and wing length in response to temperature in Drosophila melanogaster. Reaction norms as a function of growth temperature were analyzed in 20 isofemale lines in a natural population collected from Grande Ferrade near Bordeaux (southern France) in two different years. We found evidence for a complex genetic architecture underlying the reaction norms and differences between males and females. Reaction norms were negative quadratics. Genetic correlations were moderately high between traits within environments. Among characteristic values, the magnitudes of genetic correlations varied among traits and sexes. We hypothesized that genetic correlations among environments would decrease as temperatures became more different. This expectation was upheld for only one trait, female thorax length. For males for both traits, the correlations were large for both very similar and very different temperatures. These correlations may constrain the evolution of the shape of the reaction norms. Whether the extent of independence implies specific regulatory genes or only a specific allelic regulation of trait genes can not be decided from our results.
26 citations
24 citations
"Experimental evidence of condition‐..." refers background in this paper
...Here, we investigate the relationship between sexual dimorphism and condition dependence in the antler fly Protopiophila litigata Bonduriansky (1995)....
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