Sex-specific dominance reversal of genetic variation for fitness

Grieshop, Karl; Arnqvist, Göran

doi:10.1371/journal.pbio.2006810

Cited by 70 publications

(137 citation statements)

References 77 publications

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“…Our data still suggests that, in C. frigida, dominance at the inversion locus does vary in strength and direction between survival and fertility, as well as between sexes. These findings are in line with recent studies in other species showing that dominance can vary depending on the sex (14,15,61), and that multivariate traits, such as total fitness or complex traits, often involve the combination of trait-specific dominance (62)(63)(64). Overdominance may also emerge from the genetic architecture of the trait under antagonistic pleiotropy: inversions are frequently associated with deleterious or lethal effects, either because the breakpoints disrupt a gene, or because they contain recessive deleterious mutations which can only be purged by recombination and purifying selection when they occur at the homozygous state (33,(65)(66)(67).…”

Section: Discussionsupporting

confidence: 92%

Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly

Mérot

Llaurens

Normandeau

et al. 2019

Preprint

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How genetic diversity is maintained in natural populations is an evolutionary puzzle. Over time, genetic variation within species can be eroded by drift and directional selection, leading to the fixation or elimination of alleles. However, some loci show persistent variants at intermediate frequencies for long evolutionary time-scales, implicating a role of balancing selection, but studies are seldom set up to uncover the underlying processes. Here, we identify and quantify the selective pressures involved in the widespread maintenance of an inversion polymorphism in the seaweed fly Coelopa frigida, using an experimental evolution approach to estimate fitness associated with different allelic combinations. By precisely evaluating reproductive success and survival rates separately, we show that the maintenance of the polymorphism is governed by a life-history trade-off, whereby each inverted haplotype has opposed pleiotropic effects on survival and reproduction. Using numerical simulations, we confirm that this uncovered antagonism between natural and sexual selection can maintain inversion variation in natural populations of C. frigida. Moreover, our experimental data highlights that inversion-associated fitness is affected differently by sex, dominance and environmental heterogeneity. The interaction between these factors promotes polymorphism maintenance through antagonistic pleiotropy. Taken together, our findings indicate that combinations of natural and sexual selective mechanisms enable the persistence of diverse trait in nature. The joint dynamics of life history trade-offs and antagonistic pleiotropy documented here is likely to apply to other species where large phenotypic variation is controlled by structural variants. Significance statementPersistence of chromosomal rearrangements is widespread in nature and often associated with divergent life-history traits. Understanding how contrasted life-history strategies are maintained in wild populations has implications for food production, health and biodiversity in a changing environment. Using the seaweed fly Coelopa frigida, we show that a polymorphic chromosomal inversion is maintained by a trade-off between survival and reproduction, and thus provide empirical support for a role of balancing selection via antagonistic pleiotropy. This mechanism has long been overlooked because it was thought to only apply to a narrow range of ecological scenarios. These findings empirically reinforce the recent theoretical predictions that co-interacting factors (dominance, environment and sex) can lead to polymorphism maintenance by antagonistic pleiotropy and favour life-history variation.

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Section: Discussionsupporting

confidence: 92%

Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly

Mérot

Llaurens

Normandeau

et al. 2019

Preprint

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“…Recent studies have suggested dominance reversals, e.g. in Drosophila melonagaster (Chen et al 2015) and beetles (Grieshop and Arnqvist 2018). Specifically, we assume that the fitness of homozygote genotypes fluctuates temporally.…”

Section: Methodsmentioning

confidence: 99%

Models for Eco-evolutionary Extinction Vortices and their Detection

Nabutanyi

Wittmann

2020

Preprint

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1The smaller a population is, the faster it looses genetic variation due to genetic drift. Loss 2 of genetic variation can reduce population growth rate, making populations even smaller and 3 more vulnerable to loss of genetic variation, and so on. Ultimately, the population can be driven 4 to extinction by this "eco-evolutionary extinction vortex". So far, extinction vortices due to 5 loss of genetic variation have been mainly described verbally. However, quantitative models are 6 needed to better understand when such vortices arise and to develop methods for detecting 7 them. Here we propose quantitative eco-evolutionary models, both individual-based simulations 8 and analytic approximations, that link loss of genetic variation and population decline. Our 9 models assume stochastic population dynamics and multi-locus genetics with different forms 10 of balancing selection. Using mathematical analysis and simulations, we identify parameter 11 combinations that exhibit strong interactions between population size and genetic variation as 12 populations decline to extinction and match our definition of an eco-evolutionary vortex, i.e. 13 the per-capita population decline rates and per-locus fixation rates increase with decreasing 14 population size and number of polymorphic loci. We further highlight cues and early warning 15 signals that may be useful in identifying populations undergoing an eco-evolutionary extinction 16 vortex.

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“…, ; Martinossi‐Allibert et al. ; Grieshop and Arnqvist ), artificial selection experiments (Berger et al. ), and experimental evolution (Martinossi‐Allibert et al.…”

Section: Methodsmentioning

confidence: 99%

Sexual selection and the evolution of male and female cognition: A test using experimental evolution in seed beetles*

2019

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The mating system is thought to be important in shaping animal intelligence and sexual selection has been depicted as a driver of cognitive evolution, either directly by promoting superior cognitive ability during mate competition, or indirectly via genic capture of sexually selected traits. However, it remains unclear if intensified sexual selection leads to general improvements in cognitive abilities. Here, we evaluated this hypothesis by applying experimental evolution in seed beetles. Replicate lines, maintained for 35 generations of either enforced monogamy (eliminating sexual selection) or polygamy, were challenged to locate and discriminate among mates (male assays) or host seeds (female assays) in a spatial chemosensory learning task. All lines displayed learning between trials. Moreover, polygamous males outperformed monogamous males, providing evidence that sexual selection can lead to the evolution of improved male cognition. However, there were no differences between regimes in rates of male learning, and polygamous females showed no improvement in host search and even signs of reduced learning. Hence, sexual selection increased performance in cognitively demanding mate search, but it did not lead to general increases in cognitive abilities. We discuss the possibility that sexually antagonistic selection is an important factor maintaining abundant genetic variation in cognitive traits.

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Sex-specific dominance reversal of genetic variation for fitness

Cited by 70 publications

References 77 publications

Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly

Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly

Models for Eco-evolutionary Extinction Vortices and their Detection

Sexual selection and the evolution of male and female cognition: A test using experimental evolution in seed beetles*

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