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

Abstract

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.

SARS CoV2 infection _The longevity study perspectives

“…Very old people, including nonagenarians and centenarians, show a gathering of genetic variants in immune/inflammatory genes, mostly with anti-inflammatory biological effects, that confer them an optimal performance of immune system and might be included in the group of genes with beneficial redundancy ( Balistreri et al, 2012 ). In addition, the variants observed in long-lived people benefit from the effects of antagonist pleiotropy, that is consented as part of multi-controlled selection processes, enabling the persistence of genetic variations, including the immune/inflammatory genetic profiles peculiar in genetic background of long-lived people as evidenced in our and other studies ( Balistreri et al, 2012 ; Mérot et al, 2020 ). The aspects above reviewed lead us to suggest that the study of long-lived people that survived COVID, might facilitate identifying of the genetic basis of resistance to SARS-CoV-2 and provide a pharmacological target for preventing or reducing viral infection in other individuals.…”

Locally adaptive inversions modulate genetic variation at different geographic scales in a seaweed fly

“…The β arrangement provides quick growth and smaller size while the α arrangement provides high reproductive success linked to a larger size but at the expense of longer development time. This ecologically-related trade-off combined with heterozygote advantage results in strong balancing selection (Butlin 1983; Mérot, Llaurens, et al 2020). Conversely, the inversions Cf-Inv(4.1) and Cf-Inv(4.2/4.3) show no deviation from Hardy-Weinberg disequilibrium and display a strong geographic structure along a latitudinal cline.…”

“…The inversion Cf-Inv(1) encapsulates 10% of the genome and has two arrangements: α and β. These alternative Cf-Inv(1) arrangements have opposing effects on body size, fertility and development time, a combination of traits which results in different fitness depending on the local characteristics of the wrackbed (Butlin, Read, et al 1982; Day et al 1983; Butlin and Day 1985; Edward and Gilburn 2013; Wellenreuther et al 2017; Berdan et al 2018; Mérot, Llaurens, et al 2020). Almost nothing is known about the other inversions but, given that a large fraction of the C. frigida genome is impacted by polymorphic inversions, one can expect that these inversions play a significant role in structuring genetic variation and contribute to local adaptation.…”

Evolution and genetic architecture of disassortative mating at a locus under heterozygote advantage

“…Extreme examples of heterozygote advantage are observed for loci with reduced homozygote survival. In the seaweed fly Coelopa frigida heterozygotes (αβ) at the locus Adh have a higher fitness than homozygotes (αα or ββ) (RK Butlin et al, 1984;Mérot et al, 2019) and females prefer males with a genotype that differs from their own (Day and Butlin, 1987).…”