Massive genome inversion drives coexistence of divergent morphs in common quails

Sánchez-Donoso, Inés; Ravagni, Sara; Rodríguez‐Teijeiro, José Domingo; Christmas, Matthew J.; Huang, Yan; Maldonado-Linares, Andros; Puigcerver, M.; Jiménez-Blasco, Irene; Andrade, Pedro; Gonçalves, David; Friis, Guillermo; Roig, Ignasi; Webster, Matthew T.; Leonard, Jennifer A.; Vilà, Carles

doi:10.1016/j.cub.2021.11.019

Cited by 48 publications

(41 citation statements)

References 67 publications

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“…One hundred years after Alfred Sturtevant first provided evidence of chromosomal inversions in laboratory stocks of Drosophila (29) and, separately, forest-prairie ecotypes were first described in wild populations of Peromyscus (7), we found that a large chromosomal inversion is key to ecotype divergence in this classic system. Inversions have been identified in association with divergent ecotypes in diverse species, including plants (30)(31)(32)(33), invertebrates (34)(35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45), fish (46,47), and birds (48)(49)(50)(51)(52). In mammals, however, evidence for ecotype-defining inversions is limited [( 53), but see (54)].…”

Section: Discussionmentioning

confidence: 99%

A chromosomal inversion contributes to divergence in multiple traits between deer mouse ecotypes

Hager

Harringmeyer

Wooldridge

et al. 2022

Science

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How locally adapted ecotypes are established and maintained within a species is a long-standing question in evolutionary biology. Using forest and prairie ecotypes of deer mice ( Peromyscus maniculatus ), we characterized the genetic basis of variation in two defining traits—tail length and coat color—and discovered a 41-megabase chromosomal inversion linked to both. The inversion frequency is 90% in the dark, long-tailed forest ecotype; decreases across a habitat transition; and is absent from the light, short-tailed prairie ecotype. We implicate divergent selection in maintaining the inversion at frequencies observed in the wild, despite high levels of gene flow, and explore fitness benefits that arise from suppressed recombination within the inversion. We uncover a key role for a large, previously uncharacterized inversion in the evolution and maintenance of classic mammalian ecotypes.

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Section: Discussionmentioning

confidence: 99%

A chromosomal inversion contributes to divergence in multiple traits between deer mouse ecotypes

Hager

Harringmeyer

Wooldridge

et al. 2022

Science

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“…In that respect, it is interesting that many supergenes affect behaviour. For example, a supergene regulates male mating behaviour in the ruff [13], and supergenes regulate migration behaviour in the common quail and in rainbow trout [17,127]. Variation in behaviour allows individuals to select their environment, thereby increasing environmental predictability and providing conditions under which supergene evolution is favourable.…”

Section: Discussionmentioning

confidence: 99%

“…The best-known examples are sex chromosomes [6,7,11]. Others underpin alternative behaviour syndromes and plumage morphs in birds [12][13][14][15][16][17][18], mimetic colour morphs in butterflies [19,20], self-incompatibility in plants [21][22][23], mating types in fungi [24] and segregation distortion in various taxa [25,26]. Five supergenes have been recently discovered in ants (more than in any other animal family), and they all regulate the number of reproductive queens contained within a colony-a key aspect of the social organization of social insect colonies.…”

Section: Introductionmentioning

confidence: 99%

Iterative evolution of supergene-based social polymorphism in ants

Kay

Helleu

Keller

2022

Phil. Trans. R. Soc. B

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Species commonly exhibit alternative morphs, with individual fate being determined during development by either genetic factors, environmental cues or a combination thereof. Ants offer an interesting case study because many species are polymorphic in their social structure. Some colonies contain one queen while others contain many queens. This variation in queen number is generally associated with a suite of phenotypic and life-history traits, including mode of colony founding, queen lifespan, queen–worker dimorphism and colony size. The basis of this social polymorphism has been studied in five ant lineages, and remarkably social morph seems to be determined by a supergene in all cases. These ‘social supergenes’ tend to be large, having formed through serial inversions, and to comprise hundreds of linked genes. They have persisted over long evolutionary timescales, in multiple lineages following speciation events, and have spread between closely related species via introgression. Their evolutionary dynamics are unusually complex, combining recessive lethality, spatially variable selection, selfish genetic elements and non-random mating. Here, we synthesize the five cases of supergene-based social polymorphism in ants, highlighting interesting commonalities, idiosyncrasies and implications for the evolution of polymorphisms in general. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.

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“…Recent genome-scale studies have illuminated wide-ranging impacts of supergene evolution on complex phenotypes across diverse taxa (e.g. Schwander et al, 2014 ; Pearse et al, 2019 ; Hager et al, 2022 ; Joron et al, 2011 ; Kunte et al, 2014 ; Kess et al, 2019 ; Lundberg et al, 2017 ; Roberts et al, 2009 ; Sanchez-Donoso et al, 2022 ; Funk et al, 2021 ). Currently, the mechanisms by which functionally divergent supergene haplotypes evolve in the face of multiple evolutionary forces remain poorly understood, presenting a critical gap in knowledge.…”

Section: Introductionmentioning

confidence: 99%

Dynamic molecular evolution of a supergene with suppressed recombination in white-throated sparrows

Jeong

Baran

Sun

et al. 2022

eLife

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In white-throated sparrows, two alternative morphs differing in plumage and behavior segregate with a large chromosomal rearrangement. As with sex chromosomes such as the mammalian Y, the rearranged version of chromosome two (ZAL2m) is in a near-constant state of heterozygosity, offering opportunities to investigate both degenerative and selective processes during the early evolutionary stages of ‘supergenes.’ Here, we generated, synthesized, and analyzed extensive genome-scale data to better understand the forces shaping the evolution of the ZAL2 and ZAL2m chromosomes in this species. We found that features of ZAL2m are consistent with substantially reduced recombination and low levels of degeneration. We also found evidence that selective sweeps took place both on ZAL2m and its standard counterpart, ZAL2, after the rearrangement event. Signatures of positive selection were associated with allelic bias in gene expression, suggesting that antagonistic selection has operated on gene regulation. Finally, we discovered a region exhibiting long-range haplotypes inside the rearrangement on ZAL2m. These haplotypes appear to have been maintained by balancing selection, retaining genetic diversity within the supergene. Together, our analyses illuminate mechanisms contributing to the evolution of a young chromosomal polymorphism, revealing complex selective processes acting concurrently with genetic degeneration to drive the evolution of supergenes.

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Massive genome inversion drives coexistence of divergent morphs in common quails

Cited by 48 publications

References 67 publications

A chromosomal inversion contributes to divergence in multiple traits between deer mouse ecotypes

A chromosomal inversion contributes to divergence in multiple traits between deer mouse ecotypes

Iterative evolution of supergene-based social polymorphism in ants

Dynamic molecular evolution of a supergene with suppressed recombination in white-throated sparrows

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