Rapid evolution of sexual size dimorphism facilitated by Y-linked genetic variance

Kaufmann, Philipp; Wolak, Matthew E.; Husby, Arild; Immonen, Elina

doi:10.1038/s41559-021-01530-z

Cited by 17 publications

(59 citation statements)

References 61 publications

(77 reference statements)

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“…The Y chromosome is pivotal for male fertility (see references in Zhang et al, 2020 ), including for heat‐induced male sterility (Rohmer et al, 2004 ), but the Y chromosome is difficult to map and is not mapped in the DGRP. Additionally, the sexually dimorphic phenotypic response to developmental thermal plasticity points to a potential role in mediating phenotypes based on pervasive and genome‐wide sexually antagonistic genetic variation (Ruzicka et al, 2019 ) with recent work suggesting that the Y chromosome may be more important for sexually dimorphic phenotypes than previously assumed (Kaufmann et al, 2021 ). There will also be loci of small effect that we have not identified, as such loci that are difficult to detect even in large panels (Huang et al, 2014 ; Mackay et al, 2012 ).…”

Section: Discussionmentioning

confidence: 97%

The genetic basis and adult reproductive consequences of developmental thermal plasticity

Rodrigues

Zwoinska

Wiberg

et al. 2022

Journal of Animal Ecology

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Increasing temperature and thermal variability generate profound selection on populations. Given the fast rate of environmental change, understanding the role of plasticity and genetic adaptation in response to increasing temperatures is critical. This may be especially true for thermal effects on reproductive traits in which thermal fertility limits at high temperatures may be lower than for survival traits. Consequences of changing environments during development on adult phenotypes may be particularly problematic for core traits such as reproduction that begin early in development. Here we examine the consequences of developmental thermal plasticity on subsequent adult reproductive traits and its genetic basis. We used a panel of Drosophila melanogaster (the Drosophila Genetic Reference Panel; DGRP) in which male fertility performance was previously defined as either showing relatively little (status = ‘high’‐performing lines) or substantial (‘low’‐performing lines) decline when exposed to increasing developmental temperatures. We used a thermal reaction norm approach to quantify variation in the consequences of developmental thermal plasticity on multiple adult reproductive traits, including sex‐specific responses, and to identify candidate genes underlying such variation. Developmental thermal stress impacted the means and thermal reaction norms of all reproductive traits except offspring sex ratio. Mating success declined as temperature increased with no difference between high and low lines, whereas increasing temperature resulted in declines for both male and female fertility and productivity but depended on line status. Fertility and offspring number were positively correlated within and between the sexes across lines, but males were more affected than females. We identified 933 SNPs with significant evolved genetic differentiation between high and low lines. In all, 54 of these lie within genomic windows of overall high differentiation, have significant effects of genotype on the male thermal reaction norm for productivity and are associated with 16 genes enriched for phenotypes affecting reproduction, stress responses and autophagy in Drosophila and other organisms. Our results illustrate considerable plasticity in male thermal limits on several reproductive traits following development at high temperature, and we identify differentiated loci with relevant phenotypic effects that may contribute to this population variation. While our work is on a single population, phenotypic results align with an increasing number of studies demonstrating the potential for stronger selection of thermal stress on reproductive traits, particularly in males. Such large fitness costs may have both short‐ and long‐term consequences for the evolution of populations in response to a warming world.

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Section: Discussionmentioning

confidence: 97%

The genetic basis and adult reproductive consequences of developmental thermal plasticity

Rodrigues

Zwoinska

Wiberg

et al. 2022

Journal of Animal Ecology

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“…2018; Kaufmann et al. 2021; van der Bijl and Mank 2021). Furthermore, degrees of sexual dimorphism, mating and reproductive systems, and magnitudes of sexually antagonistic selection and sexual conflict can commonly vary markedly with ecological and environmental conditions (e.g., Post et al.…”

Section: Discussionmentioning

confidence: 99%

“…While sexual conflict resulting from sexually antagonistic selection can in principle be resolved through evolution of sexual dimorphism, such outcomes depend on genetic architectures of focal traits, including sex-specific additive and nonadditive genetic effects and (co)variances (Lande 1980;Connallon and Clark 2010;Arnqvist et al 2014;Wyman and Rowe 2014). Accordingly, overarching objectives are to identify interacting processes and architectures that can jointly generate balancing selection and facilitate the emergence of sexual dimorphism and to understand how such processes and architectures can themselves arise or be constrained (Bonduriansky and Chenoweth 2009;Connallon andClark 2010, 2014;Connallon 2015;Llaurens et al 2017;Grieshop and Arnqvist 2018;Ruzicka et al 2019;Kaufmann et al 2021;van der Bijl and Mank 2021).…”

mentioning

confidence: 99%

Intrinsic emergence and modulation of sex‐specific dominance reversals in threshold traits

Reid

2022

Evolution

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Sex‐specific dominance reversals (SSDRs) in fitness‐related traits, where heterozygotes' phenotypes resemble those of alternative homozygotes in females versus males, can simultaneously maintain genetic variation in fitness and resolve sexual conflict and thereby shape key evolutionary outcomes. However, the full implications of SSDRs will depend on how they arise and the resulting potential for evolutionary, ecological and environmental modulation. Recent field and laboratory studies have demonstrated SSDRs in threshold(‐like) traits with dichotomous or competitive phenotypic outcomes, implying that such traits could promote the emergence of SSDRs. However, such possibilities have not been explicitly examined. I show how phenotypic SSDRs can readily emerge in threshold traits given genetic architectures involving large‐effect loci alongside sexual dimorphism in the mean and variance in polygenic liability. I also show how multilocus SSDRs can arise in line‐cross experiments, especially given competitive reproductive systems that generate nonlinear fitness outcomes. SSDRs can consequently emerge in threshold(‐like) traits as functions of sexual antagonism, sexual dimorphism and reproductive systems, even with purely additive underlying genetic effects. Accordingly, I identify theoretical and empirical advances that are now required to discern the basis and occurrence of SSDRs in nature, probe forms of (co‐)evolutionary, ecological and environmental modulation, and evaluate net impacts on sexual conflict.

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“…Given the fact that such effects were in many cases unexpected and unlooked for (e.g. [ 183 ]), it seems likely that we are currently only seeing the tip of the iceberg, and that many more examples of the genetic potential of NRSCs are waiting to be discovered.…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, a recent study in Callosobruchus seed beetles revealed that Y-linked genetic variation could explain the bulk of the response to artificial selection on body size in lines that were selected for increased sexual dimorphism [ 183 ]. This was a surprising finding since body size is a trait that is usually expected to be controlled by many small-effect autosomal loci, but is consistent with the results from live bearing fishes discussed above.…”

Section: Y Chromosomesmentioning

confidence: 99%

Sex-limited chromosomes and non-reproductive traits

2022

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Sex chromosomes are typically viewed as having originated from a pair of autosomes, and differentiated as the sex-limited chromosome (e.g. Y) has degenerated by losing most genes through cessation of recombination. While often thought that degenerated sex-limited chromosomes primarily affect traits involved in sex determination and sex cell production, accumulating evidence suggests they also influence traits not sex-limited or directly involved in reproduction. Here, we provide an overview of the effects of sex-limited chromosomes on non-reproductive traits in XY, ZW or UV sex determination systems, and discuss evolutionary processes maintaining variation at sex-limited chromosomes and molecular mechanisms affecting non-reproductive traits.

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Rapid evolution of sexual size dimorphism facilitated by Y-linked genetic variance

Abstract: This is the accepted version of a paper published in Nature Ecology & Evolution. This paper has been peer-reviewed but does not include the final publisher proof-corrections or journal pagination.

Cited by 17 publications

References 61 publications

The genetic basis and adult reproductive consequences of developmental thermal plasticity

The genetic basis and adult reproductive consequences of developmental thermal plasticity

Intrinsic emergence and modulation of sex‐specific dominance reversals in threshold traits

Sex-limited chromosomes and non-reproductive traits

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