Sexual selection, environmental robustness and evolutionary demography of maladapted populations: a test using experimental evolution in seed beetles

Martinossi‐Allibert, Ivain; Thilliez, Emma; Arnqvist, Göran; Berger, David

doi:10.1101/426056

Cited by 4 publications

(1 citation statement)

References 89 publications

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“…A canalized response for female reproductive traits may be selected for, given that population growth is mainly dependent on female fertility in many sexually reproducing species (Caswell, 2006 ), but this cannot completely overcome the male‐biased reduction. However, for traits with a shared genetic basis and that are condition dependent, male‐biased thermal sensitivity may help purge deleterious mutations without negative effects on population fitness (Martinossi‐Allibert et al, 2019 ; Manning, 1984 ; Rowe & Houle, 1996 ). It is important to note, however, that males are not universally more sensitive to thermal stress (Walsh, Parratt, Hoffmann, et al, 2019 ) and that interactions between the sexes shape realized thermal sensitivity of reproduction (Baur et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

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: 99%

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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Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

Bagchi

Corbel

Khan

et al. 2020

Preprint

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Sexual dimorphism in immunity is believed to reflect sex-differences in trade-offs between competing life history demands. Sexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex-differences in immunity as well as associated host-pathogen dynamics. Yet, experimental data linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females. We demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males as a result of sex-biased expression of genes in the proPO activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (relative to natural polygamy) rapidly decreases female (but not male) PO activity. The evolution of decreased PO in monogamous females was accompanied by increased tolerance to bacterial infection unrelated to mating. This implies that female responses to costly mating may trade off with other aspects of immune defence. Finally, female (but not male) PO activity show correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects. Our results thus provide a proximate and ultimate understanding of the links between sexual selection and sexual dimorphism in immunity.

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The ecology of sexual conflict: behaviorally plastic responses to temperature variation in the social environment can drastically modulate male harm to females

García‐Roa

Chirinos

C³

2018

Preprint

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Sexual conflict is a fundamental driver of male/female adaptations, an engine of biodiversity, and a crucial determinant of population viability. For example, sexual conflict frequently leads to behavioural adaptations that allow males to displace their rivals, but in doing so harm those same females they are competing to access. Sexual conflict via male harm hence not only deviates females from their fitness optimum, but can decrease population viability and facilitate extinction. Despite this prominent role, we are far from understanding what factors modulate the intensity of sexual conflict, and particularly the role of ecology in mediating underlying behavioural adaptations. In this study we show that, in Drosophila melanogaster, variations in environmental temperature of ±4ºC (within the natural range in the wild) decrease male harm impact on female fitness by between 45-73%. Rate-sensitive fitness estimates indicate that such modulation results in an average rescue of population productivity of 7% at colder temperatures and 23% at hotter temperatures. Our results: a) show that the thermal ecology of social interactions can drastically modulate male harm via behaviourally plasticity, b) identify a potentially crucial ecological factor to understand how sexual conflict operates in nature, and c) suggest that behaviourally plastic responses can lessen the negative effect of sexual conflict on population viability in the face of rapid environmental temperature changes.

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Sexual selection, environmental robustness and evolutionary demography of maladapted populations: a test using experimental evolution in seed beetles

Cited by 4 publications

References 89 publications

The genetic basis and adult reproductive consequences of developmental thermal plasticity

The genetic basis and adult reproductive consequences of developmental thermal plasticity

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

The ecology of sexual conflict: behaviorally plastic responses to temperature variation in the social environment can drastically modulate male harm to females

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