Genie and karyotypic selection on an inversion polymorphism in the seaweed fly, Coelopa frigida

Butlin, Roger K.; Day, Thomas H.

doi:10.1038/hdy.1985.36

Cited by 24 publications

(33 citation statements)

References 19 publications

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“…Here, ββ and αβ relative survival rate did not differ significantly (mean difference 2%, p = 0.99), suggesting a dominance effect of the β allele on egg-to-adult survival. This contrasts with the general finding of overdominance in European populations of C. frigida, where αβ heterozygotic larvae survive better than both homozygotes (36,37,42). Yet, the high αβ relative survival is known to be enhanced by increased competitive conditions and, therefore, the performance of homozygotes in our data may be explained by the low-density conditions maintained in our experiment.…”

Section: The β Allele Confers a Viability Advantage During The Larvalmentioning

confidence: 69%

“…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). The generally higher egg-to-adult viability of heterozygotes, which is enhanced in stressful (high-density) conditions, suggests that the two haplotypic rearrangements of C. frigida may contain different clusters of deleterious mutations, a result supported by intra-and inter-population crosses (36). Such a linked genetic load may explain why the rarest αα genotype exhibits the highest deficit compared to Hardy-Weinberg expectations in nature (30) and why the αα genotype has the lowest viability in laboratory conditions.…”

Section: Discussionmentioning

confidence: 99%

“…In C. frigida, the two alleles, referred to as α and β, differ by more than 2.5% sequence divergence in coding regions and are observed at intermediate frequencies in both European and North American C. frigida populations, suggesting that the haplotypic rearrangements diverged a long time ago and were maintained ever since by balancing selection (30)(31)(32). The widespread excess of αβ heterozygotes and the higher egg-to-adult survival of heterozygotes compared to αα and ββ homozygotes implicates that this polymorphism is partly maintained by overdominance, possibly due to deleterious alleles captured by the inversion (36,37). Moreover, inversion frequencies correlate with environmental factors such as temperature and local substrate characteristics, suggesting that spatially-varying selection combined with migration also contributes to maintain this polymorphism (30,31,38).…”

Section: Introductionmentioning

confidence: 99%

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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: The β Allele Confers a Viability Advantage During The Larvalmentioning

confidence: 69%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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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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“…In the case of C. frigida, none of the homokaryotypes is lethal but the parallel, repeatedly striking deficit of the homokaryotypes suggests the presence of moderately deleterious effects. This is supported by evidence for genic selection in a series of inter and intra-population crosses [77] and remains to be investigated at the genome level.…”

Section: Additional Mechanisms Of Balancing Selection Contributing Tomentioning

confidence: 80%

Karyotype-environment associations support a role for a chromosomal inversion in local adaptation in the seaweed flyCoelopa frigida

Mérot¹,

Berdan²,

Babin³

et al. 2018

Preprint

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Large chromosomal rearrangements are thought to facilitate adaptation to heterogeneous environments by limiting genomic recombination. Indeed, inversions have been implicated in adaptation along environmental clines and in ecotype specialisation. Here, we combine classical ecological studies and population genetics to investigate an inversion polymorphism previously documented in Europe among natural populations of the seaweed fly Coelopa frigida along a latitudinal cline in North America. We test if the inversion is present in North America and polymorphic, assess which environmental conditions modulate the inversion karyotype frequencies, and document the relationship between inversion karyotype and adult size. We sampled nearly 2,000 flies from 20 populations along several environmental gradients to quantify associations of inversion frequencies to heterogeneous environmental variables. Genotyping and phenotyping showed a widespread and conserved inversion polymorphism between Europe and America. Variation in inversion frequency was significantly associated with environmental factors, with parallel patterns between continents, indicating that the inversion may play a role in local adaptation. The three karyotypes of the inversion are differently favoured across micro-habitats and represent life-history strategies likely maintained by the collective action of several mechanisms of balancing selection. Our study adds to the mounting evidence that inversions are facilitators of adaptation and enhance within-species diversity.not peer-reviewed)

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“…There are two major alternative sources of widespread heterosis, both associated with reduced recombination in heterozygous individuals: positive epistatic interactions (co‐adaptation) among loci within the rearrangement or accumulation of deleterious recessive alleles independently in the two chromosomal populations. The contributions of these effects can be separated in appropriate crosses (Butlin & Day 1985). Whatever the original reason for the spread of a rearrangement, it is likely that heterosis will increase, so long as the rearrangement remains polymorphic, because deleterious recessive alleles and alleles that are advantageous in the background of one arrangement tend to accumulate.…”

Section: Role In Speciationmentioning

confidence: 99%

Recombination and speciation

2005

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Speciation can be viewed as the evolution of restrictions on the freedom of genetic recombination: new combinations of alleles can be generated within species, but alleles from different species cannot be brought together. Recently, there has been increasing realization that the role of chromosomal rearrangements in speciation might be primarily a result of their influence on recombination. I argue that ideas about the role of recombination in speciation should be considered in the context of the variability of recombination rates and patterns more generally and that genic as well as chromosomal causes of restricted recombination should be considered. I review patterns of variation in recombination rates and theoretical progress in understanding the conditions that favour increased or decreased rates. Although progress has been made in understanding conditions that alter overall rates of recombination, widespread variation in patterns of recombination remains largely unexplained. I consider three models for the role of locally restricted recombination in speciation and the evidence currently supporting them.

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Genie and karyotypic selection on an inversion polymorphism in the seaweed fly, Coelopa frigida

Cited by 24 publications

References 19 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

Karyotype-environment associations support a role for a chromosomal inversion in local adaptation in the seaweed flyCoelopa frigida

Recombination and speciation

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