Stepwise evolution of a butterfly supergene via duplication and inversion

Kim, Kang Wook; De‐Kayne, Rishi; Gordon, I.; Omufwoko, Kennedy Saitoti; Martins, Dino J.; ffrench-Constant, Richard H.; Martin, Simon H.

doi:10.1098/rstb.2021.0207

Cited by 35 publications

(38 citation statements)

References 54 publications

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“…An important message is that because different copies of the same arrangement can vary in content, the repeated use of the same inversion does not necessarily mean that the actual genetic basis of adaptation is the same. If inversions are old and geographically widespread, as has been shown in some cases (examples above, [ 66 ]), it is likely that such within-arrangement diversity has evolved. An example for within-supergene evolution after its initial formation is described for Heliconius butterflies in this issue [ 67 ].…”

Section: Factors That Facilitate or Hinder A Role Of Inversions In Pa...mentioning

confidence: 95%

Inversions and parallel evolution

Westram

Faria

Johannesson

et al. 2022

Phil. Trans. R. Soc. B

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Local adaptation leads to differences between populations within a species. In many systems, similar environmental contrasts occur repeatedly, sometimes driving parallel phenotypic evolution. Understanding the genomic basis of local adaptation and parallel evolution is a major goal of evolutionary genomics. It is now known that by preventing the break-up of favourable combinations of alleles across multiple loci, genetic architectures that reduce recombination, like chromosomal inversions, can make an important contribution to local adaptation. However, little is known about whether inversions also contribute disproportionately to parallel evolution. Our aim here is to highlight this knowledge gap, to showcase existing studies, and to illustrate the differences between genomic architectures with and without inversions using simple models. We predict that by generating stronger effective selection, inversions can sometimes speed up the parallel adaptive process or enable parallel adaptation where it would be impossible otherwise, but this is highly dependent on the spatial setting. We highlight that further empirical work is needed, in particular to cover a broader taxonomic range and to understand the relative importance of inversions compared to genomic regions without inversions. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.

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Section: Factors That Facilitate or Hinder A Role Of Inversions In Pa...mentioning

confidence: 95%

Inversions and parallel evolution

Westram

Faria

Johannesson

et al. 2022

Phil. Trans. R. Soc. B

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show abstract

“…Therefore, one expects a large variance in the tract length distribution under neutral admixture (Sachdeva and Barton 2018). Observing long haplotypes at intermediate frequency could thus be explained with purely neutral processes, especially if the hotspot corresponds to a region of reduced recombination (duplicated repeats may be an underestimated way to arrest recombination locally in the genomes, e.g., Kim et al 2022). Still, the singularity of such a region found in the genome of sympatric C. intestinalis individuals seems difficult to explain without invoking some sort of selection.…”

Section: Is There An Adaptive Breakthrough On Chromosome 5?mentioning

confidence: 99%

Introgression between highly divergent sea squirt genomes: an adaptive breakthrough?

Fraïssé¹,

Moan²,

Roux³

et al. 2022

Peer Community Journal

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Human-mediated introductions are reshuffling species distribution on a global scale. Consequently, an increasing number of allopatric taxa are now brought into contact, promoting introgressive hybridization between incompletely isolated species and new adaptive gene transfer. The broadcast spawning marine species, Ciona robusta, has been recently introduced in the native range of its sister taxa, Ciona intestinalis, in the English Channel and North-East Atlantic. These sea squirts are highly divergent, yet hybridization has been reported by crossing experiments and genetic studies in the wild. Here, we examined the consequences of secondary contact between C. intestinalis and C. robusta in the English Channel. We produced genomes phased by transmission to infer the history of divergence and gene flow, and analyzed introgressed genomic tracts. Demographic inference revealed a history of secondary contact with a low overall rate of introgression. Introgressed tracts were short, segregating at low frequency, and scattered throughout the genome, suggesting traces of past contacts during the last 30 ky. However, we also uncovered a hotspot of introgression on chromosome 5, characterized by several hundred kb-long C. robusta haplotypes segregating in C. intestinalis, that introgressed during contemporary times the last 75 years. Although locally more frequent than the baseline level of introgression, C. robusta alleles are not fixed, even in the core region of the introgression hotspot. Still, linkage-disequilibrium patterns and haplotype-based tests suggest this genomic region is under recent positive selection. We further detected in the hotspot an over-representation of candidate SNPs lying on a cytochrome P450 gene with a high copy number of tandem repeats in the introgressed alleles. Cytochromes P450 are a superfamily of enzymes involved in detoxifying exogenous compounds, constituting a promising avenue for functional studies. These findings support that introgression of an adaptive allele is possible between very divergent genomes and that anthropogenic hybridization can provide the raw material for adaptation of native lineages in the Anthropocene.

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“…A supergene usually arises when recombination is suppressed, often as a result of one or more inversions or other structural changes [ 12 ], so that a group of neighbouring genes becomes inherited as a single Mendelian element. The long-term fate of the novel haplotype will depend on drift and on the combined selective effects over multiple supergene elements.…”

Section: Introductionmentioning

confidence: 99%

Unbalanced selection: the challenge of maintaining a social polymorphism when a supergene is selfish

Tafreshi

Otto

Chapuisat

2022

Phil. Trans. R. Soc. B

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Supergenes often have multiple phenotypic effects, including unexpected detrimental ones, because recombination suppression maintains associations among co-adapted alleles but also allows the accumulation of recessive deleterious mutations and selfish genetic elements. Yet, supergenes often persist over long evolutionary periods. How are such polymorphisms maintained in the face of selection, drive and drift? We present a population genetic model that investigates the conditions necessary for a stable polymorphic equilibrium when one of the supergene haplotypes is a selfish genetic element. The model fits the characteristics of the Alpine silver ant, Formica selysi , in which a large supergene underlies colony social organization, and one haplotype distorts Mendelian transmission by killing progeny that did not inherit it. The model shows that such maternal-effect killing strongly limits the maintenance of social polymorphism. Under random mating, transmission ratio distortion prevents rare single-queen colonies from invading populations of multiple-queen colonies, regardless of the fitness of each genotype. A stable polymorphic equilibrium can, however, be reached when high rates of assortative mating are combined with large fitness differences among supergene genotypes. The model reveals that the persistence of the social polymorphism is non-trivial and expected to occur only under restrictive conditions that deserve further empirical investigation. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.

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Stepwise evolution of a butterfly supergene via duplication and inversion

Cited by 35 publications

References 54 publications

Inversions and parallel evolution

Inversions and parallel evolution

Introgression between highly divergent sea squirt genomes: an adaptive breakthrough?

Unbalanced selection: the challenge of maintaining a social polymorphism when a supergene is selfish

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