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Journal ArticleDOI

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.

AbstractSexually 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.

Topics: Sexual dimorphism (62%), Sexual selection (57%)

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Citations
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Journal ArticleDOI
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.

29 citations


Journal ArticleDOI
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. This article is protected by copyright. All rights reserved.

25 citations


Journal ArticleDOI
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.

24 citations


Journal ArticleDOI
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.

17 citations


Journal ArticleDOI
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...

12 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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References
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Book
24 Feb 1871
Abstract: Part II. Sexual Selection (continued): 12. Secondary sexual characters of fishes, amphibians and reptiles 13. Secondary sexual characters of birds 14. Birds (continued) 15. Birds (continued) 16. Birds (concluded) 17. Secondary sexual characters of mammals 18. Secondary sexual characters of mammals (continued) 19. Secondary sexual characters of man 20. Secondary sexual characters of man (continued) 21. General summary and conclusion Index.

11,295 citations


Journal ArticleDOI
06 Apr 1871-Nature
Abstract: I. IF Mr. Darwin had closed his rich series of contributions to Science by the publication of the “Origin of Species,“he would have made an epoch in Natural History like that which Socrates made in philosophy, or Harvey in medicine. The theory identified with his name has stimulated ethnological and anatomical inquiries in every direction; it has been largely adopted and followed out by naturalists in this country and America, but most of all in the great work-room of modern science, whence a complete literature on “Darwinismus“has sprung up, and there disciples have appeared who stand in the same relation to their master as Muntzer and the Anabaptists did to Luther. Like most great advances in knowledge, the theory of Evolution found everything ripe for it. This is shown by the well-known fact that Mr. Wallace arrived at the same conclusion as to the origin of species while working in the Eastern Archipelago, and scarcely less so by the manner in which the theory has been worked out by men so distinguished as Mr. Herbert Spencer and Prof. Haeckel. But it was known when the “Origin of Species “was published, that instead of being the mere brilliant hypothesis of a man of genius, of which the proofs were to be furnished and the fruits gathered in by his successors, it was really only a summary of opinions based upon the most extensive and long-continued researches. Its author did not simply open a new province for future travellers to explore, he had already surveyed it himself, and the present volumes show him still at the head of his followers. They are written in a more popular style than those on "Animals and Plants under Domestication,“as they deal with subjects of more general interest; but all the great qualities of industry and accuracy in research, of fertility in framing hypotheses, and of impartiality in judgment, are as apparent in this as in Mr. Darwin's previous works. To one who bears in mind the too frequent tone of the controversies these works have excited, the turgid rhetoric and ignorant presumption of those "who are not of his school -or any school,“and the still more lamentable bad taste which mars the writings of Vogt and even occasionally of Haeckel, it is very admirable to see the calmness and moderation (for which philosophical would be too low an epithet) with which the author handles his subject. If prejudice can be conciliated, it will surely be by a book like this. The Descent of Man, and Selection in relation to Sex. By Charles Darwin, &c. In two volumes. Pp. 428, 475. (Murray, 1871.)

4,382 citations


"Experimental evidence of condition‐..." refers background in this paper

  • ...While sexually antagonistic selection may arise from ecological interactions such as intersexual resource competition (Darwin, 1871), sexual selection is often thought to be involved because it is persistent and the divergent reproductive interests of males and females cause it to be sex-specific,…...

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  • ...While sexually antagonistic selection may arise from ecological interactions such as intersexual resource competition (Darwin, 1871), sexual selection is often thought to be involved because it is persistent and the divergent reproductive interests of males and females cause it to be sex-specific, often being present in one sex yet weak or absent in the other (Price, 1984; Fairbairn & Preziosi, 1996)....

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Journal ArticleDOI
01 Jan 1987-The Auk
TL;DR: The correct calculation of repeatability is outlined, a common mistake is pointed out, how the incorrectly calculated value relates to repeatable values is shown, and a method for checking published values and calculating approximate repeatability values from the F ratio is provided.
Abstract: -Repeatability is a useful tool for the population geneticist or genetical ecologist, but several papers have carried errors in its calculation We outline the correct calculation of repeatability, point out the common mistake, show how the incorrectly calculated value relates to repeatability, and provide a method for checking published values and calculating approximate repeatability values from the F ratio (mean squares among groups/ mean squares within groups) Received 6 February 1986, accepted 25 August 1986 REPEATABILITY is a measure used in quantitative genetics to describe the proportion of variance in a character that occurs among rather than within individuals Repeatability, r, is given by: r = (VG + VEg)/ VP, (1) where VG is the genotypic variance, VEg the general environmental variance, and Vp the phenotypic variance (Falconer 1960, 1981) In addition to its use in assessing the reliability of multiple measurements on the same individual, repeatability may be used to set an upper limit to the value of heritability (Falconer 1960, 1981) and to separate, for instance, the effects of "self" and "mate" on a character such as clutch size (van Noordwijk et al 1980) Repeatability is therefore a useful statistic for population geneticists and genetical ecologists Recently, we have noticed an increasing number of published papers and unpublished manuscripts in which repeatability was miscalculated Our purpose is fivefold: (1) to outline the correct method of calculating repeatability; (2) to point out a common mistake in calculating repeatability; (3) to show how much this mistake affects values of repeatability; (4) to provide a quick way of checking published estimates, and to calculate an approximate value of repeatability from published F ratios and degrees of freedom; and (5) to make recommendations for authors, referees, editors, and readers to prevent the promulgation and propagation of incorrect repeatability values in the literature CALCULATION OF REPEATABILITY Repeatability is the intraclass correlation coefficient (Sokal and Rohlf 1981), which is based on variance components derived from a one-way analysis of variance (ANOVA) The intraclass correlation coefficient is given by some statistical packages; otherwise it can be calculated from an ANOVA ANOVA is described in most statistics textbooks (eg Sokal and Rohlf 1981; Kirk 1968 gives a detailed treatment of more complex designs of ANOVA), so we will not repeat it here, but give the general form of the results from such an analysis in Table 1 Repeatability, r, is given by r = sA / (S + SA)' (2) where S2A is the among-groups variance component and s2 is the within-group variance component These variance components are calculated from the mean squares in the analysis of variance as:

2,802 citations


"Experimental evidence of condition‐..." refers background in this paper

  • ...For traits subject to persistent directional selection, a component of fitness is an increasing function of investment in them, favouring increased allocation to their expression (Andersson, 1982; Nur & Hasson, 1984)....

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Journal ArticleDOI
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

1,607 citations


"Experimental evidence of condition‐..." refers methods in this paper

  • ...Repeatabilities were estimated as the ANOVA-based intraclass correlation coefficient (Lessels & Boag, 1987) and were ≥ 0.9 for all traits (Table S1)....

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Journal ArticleDOI
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.

1,250 citations


"Experimental evidence of condition‐..." refers background in this paper

  • ...…probably alter condition, both for morphological traits (David et al., 1994, 2000; Post et al., 1999; Karan et al., 2000; Bonduriansky & Rowe, 2005; Weladji et al., 2005; Bonduriansky, 2007a; Boughman, 2007; Punzalan et al., 2008) and, in a study in Drosophila melanogaster, for gene expression…...

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