Genomic evidence that a sexually selected trait captures genome-wide variation and facilitates the purging of genetic load

Parrett, Jonathan M.; Chmielewski, Sebastian; Aydogdu, Eylem; Łukasiewicz, Aleksandra; Rombauts, Stéphane; Szubert-Kruszyńska, Agnieszka; Babik, Wiesław; Konczal, Mateusz; Radwan, Jacek

doi:10.1038/s41559-022-01816-w

Cited by 20 publications

(28 citation statements)

References 118 publications

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“…Some of these effects may be related to sexual con ict [29]. However, as the current study did not nd evidence for increased sexual con ict in the ghter-selected populations studied here (possibly due to large population sizes), most of these effects must be associated with indirect selection for better condition and increased purifying selection in ghter selected populations [21]. The association of these genes with oxidation-reduction processes and carbohydrate metabolism suggests that selection for an aggressive and highly competitive phenotype in males is re ected in metabolism of females.…”

Section: Transcriptomics Of Differences In Thermal Plasticity Between...contrasting

confidence: 53%

Transcriptomics of differences in thermal plasticity associated with selection for an exaggerated male sexual trait

Plesnar‐Bielak

Parrett

Chmielewski

et al. 2022

Preprint

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BackgroundThe information about the magnitude of between-individual differences in thermal plasticity and identification of the underlying molecular mechanisms are key to understand the evolution of thermal plasticity. In particular, genes underlying variation in the physiological response to temperature can provide raw material for selection acting on plastic traits. Using RNAseq, we investigate the transcriptional response to temperature in males and females from the bulb mite populations selected for the increased frequency of one of two discrete male morphs (fighter- and scrambler-selected populations) that differ in relative fitness depending on temperature.ResultsAt decreased temperature, males from fighter-selected populations showed higher transcriptomic plasticity, as indicated by a significant selection treatment by temperature (decreased vs. control) interaction effect on the expression of 40 genes, 38 of which were overexpressed in fighter-selected populations in response to temperature decrease. These genes were mostly associated with carbohydrate metabolism. At increased temperature, no selection-by-temperature interaction in gene expression was detected. Hence, between-morph differences in response to increased temperature are most likely determined by genes consistently differing in expression between morphs. These genes were associated with protein metabolism, ion transport, lipid metabolism and oxidoreductase activity among others. In females, we did not find genes with selection-treatment-specific response to temperature decrease or increase, but both sexes differed between selection treatments in expression of 79 genes. They can be treated as candidates for genes underlying temperature sensitivity of fitness differences between females from fighter- and scrambler-selected populations.ConclusionDifferent mechanisms underly the divergence in thermal response between populations differing in sexually selected traits prevalence at decreased vs. increased temperature. While temperature decrease was associated with higher transcriptomic plasticity of males with more elaborate armaments, differential response to temperature increase likely depended on genes associated with their distinct thermal tolerance. Selection on males drove gene expression patterns in females. These patterns could be associated with temperature-dependent fitness differences between females from fighter- vs. scrambler-selected populations reported in previous studies. Our study shows that selection for divergent male sexually selected morphologies and behaviors has a potential to drive divergence in metabolic pathways underlying plastic response to temperature in both sexes.

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Section: Transcriptomics Of Differences In Thermal Plasticity Between...contrasting

confidence: 53%

Transcriptomics of differences in thermal plasticity associated with selection for an exaggerated male sexual trait

Plesnar‐Bielak

Parrett

Chmielewski

et al. 2022

Preprint

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“…Nevertheless, our current model highlights that the presence of environmental variance in traits underlying male mating success critically affects the ability of phenotypic sexual selection to slow down the accumulation of genetic load, and that this effect arises because resulting variance in male mating success reduces N e and increases genetic drift to a degree that imposes an upper limit on the positive purging effects of increasing sexual selection. Accordingly, even when disregarding costs to sexually selected traits and/or the dynamics of sexual conflict, positive net contributions of strong sexual selection in reducing genetic load should not be taken for granted, partly explaining why empirical studies in laboratory and natural populations testing for positive net benefits of sexual selection may have shown mixed results (Chandler et al, 2020;Doherty et al, 2003;Parrett et al, 2019Parrett et al, , 2022. Future theoretical and empirical studies investigating the consequences of sexual selection on genetic load and population persistence should explicitly consider appropriate genetic and non-genetic components generating phenotypic variation under selection.…”

Section: Discussionmentioning

confidence: 99%

“…Accordingly, considerable empirical work has tested whether sexual selection in males can indeed increase selection against deleterious mutations and thereby aid population persistence (Cally et al, 2019; Rowe & Rundle, 2021). Results are mixed: some experimental studies on a variety of species, for example, the fruit fly Drosophila melanogaster or the bulb mite Rhizoglyphus robini , report positive effects of sexual selection on population fitness (Almbro & Simmons, 2014; Godwin et al, 2020; Grieshop et al, 2016; Hollis et al, 2009; Jarzebowska & Radwan, 2010; Lumley et al, 2015; Parrett et al, 2022; Radwan, 2004), while other studies in the same or similar species did not find such effects (Allen et al, 2017; Arbuthnott & Rundle, 2012; Chenoweth et al, 2015; Hollis & Houle, 2011; Plesnar‐Bielak et al, 2011, 2020; Prokop et al, 2019). Meanwhile, studies of wild populations have mostly found negative effects of sexual selection on population persistence (Bro‐Jørgensen, 2014; Doherty et al, 2003; Martins et al, 2018; McLain et al, 1995; McLain & Vives, 1998; Morrow & Pitcher, 2003), but some studies report no effect (Morrow & Fricke, 2004; Prinzing et al, 2002) or positive effects (Parrett et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Environmental variance in male mating success modulates the positive versus negative impacts of sexual selection on genetic load

Tschol

Reid

Bocedi

2023

Journal of Evolutionary Biology

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Sexual selection on males is predicted to increase population fitness, and delay population extinction, when mating success negatively covaries with genetic load across individuals. However, such benefits of sexual selection could be counteracted by simultaneous increases in genome‐wide drift resulting from reduced effective population size caused by increased variance in fitness. Resulting fixation of deleterious mutations could be greatest in small populations, and when environmental variation in mating traits partially decouples sexual selection from underlying genetic variation. The net consequences of sexual selection for genetic load and population persistence are therefore likely to be context dependent, but such variation has not been examined. We use a genetically explicit individual‐based model to show that weak sexual selection can increase population persistence time compared to random mating. However, for stronger sexual selection such positive effects can be overturned by the detrimental effects of increased genome‐wide drift. Furthermore, the relative strengths of mutation‐purging and drift critically depend on the environmental variance in the male mating trait. Specifically, increasing environmental variance caused stronger sexual selection to elevate deleterious mutation fixation rate and mean selection coefficient, driving rapid accumulation of drift load and decreasing population persistence times. These results highlight an intricate balance between conflicting positive and negative consequences of sexual selection on genetic load, even in the absence of sexually antagonistic selection. They imply that environmental variances in key mating traits, and intrinsic genetic drift, should be properly factored into future theoretical and empirical studies of the evolution of population fitness under sexual selection.

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“…Male R. robini are dimorphic and develop into one of two morphs: fighters possess a sexually selected weapon in the form of a thickened and terminally pointed third pair of legs which are used in lethal combat with rivals, whereas scramblers have legs all approximately the same thickness and avoid direct competition. Male morph is largely heritable with considerable additive genetic variance (Radwan 1995, Parrett et al 2023a), but is also influenced by individual condition, itself determined by the amount of food available during development (Radwan 1995, Smallegange 2011) and genome‐wide variation of deleterious mutations (Łukasiewicz et al 2020, Parrett et al 2022). The expression and fitness of each morph has been shown to be influenced by thermal conditions, with fighter males having reduced fitness and selected against at increased temperatures (Plesnar‐Bielak et al 2013, 2018).…”

Section: Introductionmentioning

confidence: 99%

Fertility loss under thermal stress: males have lower fertility limits but no evidence of sex differences in sensitivity

Parrett,

Kulczak,

Szudarek‐Trepto

2024

Oikos

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Climate change models predict that the frequency and intensity of heatwaves are likely to increase, therefore understanding population responses to these extreme climatic events will be key in mitigating biodiversity loss. Here, using the male dimorphic bulb mite, Rhizoglyphus robini, we investigate and compare the impact of experimental heat stress on survival and fertility between females and male morphs that differ in the expression of a sexually selected weapon. We show that lethal limits are similar among all individuals, but find clear sex differences, although no difference between morphs, in sub‐lethal temperatures causing sterility: female fertility remains high close to lethal limits, whereas both male morphs suffer fertility loss at more than 2.5°C below their lethal limits. Contrastingly, when thermal stress was lower the sexes and morphs do not differ in their thermal sensitivity and declines in reproductive output are comparable. These declines appear to be additive as we observe the greatest declines when both sexes were exposed to thermal stress. In addition, during assays we included an extra treatment that allowed individuals two extra days to recover and found that fertility loss was almost fully recovered when thermal stress was low, but only partially recovered under the most extreme temperatures. The impact of heat stress on fertility therefore appears to be temporary with individuals rapidly recovering: whether recovery can negate negative population level effects remains to be investigated. Our experiments reveal the impact of heat stress on survival and fertility, finding sex‐specific fertility loss under the most extreme thermal conditions.

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Genomic evidence that a sexually selected trait captures genome-wide variation and facilitates the purging of genetic load

Cited by 20 publications

References 118 publications

Transcriptomics of differences in thermal plasticity associated with selection for an exaggerated male sexual trait

Transcriptomics of differences in thermal plasticity associated with selection for an exaggerated male sexual trait

Environmental variance in male mating success modulates the positive versus negative impacts of sexual selection on genetic load

Fertility loss under thermal stress: males have lower fertility limits but no evidence of sex differences in sensitivity

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