An Ancient and Eroded Social Supergene Is Widespread across Formica Ants

Brelsford, Alan; Purcell, Jessica; Avril, Amaury; Van, Patrick Tran; Zhang, Junxia; Brütsch, Timothée; Sundström, Liselotte; Helanterä, Heikki; Chapuisat, Michel

doi:10.1016/j.cub.2019.11.032

Cited by 67 publications

(172 citation statements)

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“…Strikingly, in both systems a killer is hidden in the social supergene, and selfish drive by a nonrecombining haplotype favors the spread of multiple-queen colonies. Yet, in spite of drive, these supergene haplotypes did not reach fixation over extended evolutionary periods (34,38,39). The long-term persistence of these polymorphisms indicates that they are balanced by antagonistic selective pressures at the gene, individual and group levels.…”

Section: Discussionmentioning

confidence: 97%

“…shared across species separated by 20-40 MY of independent evolution(34).The unusual properties of the Sp haplotype, which drives without being lethal in homozygotes, raises the question of what balances the polymorphism and prevents the driving haplotype from going to fixation? Stable polymorphic equilibria can be maintained by overdominance, by various forms of negative frequency-dependent selection such as disassortative mating, or by selection in temporally or spatially heterogenous environments(35,36).…”

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confidence: 99%

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Maternal effect killing by a supergene controlling ant social organization

Avril

Purcell

Béniguel

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Supergenes underlie striking polymorphisms in nature, yet the evolutionary mechanisms by which they arise and persist remain enigmatic. These clusters of linked loci can spread in populations because they captured coadapted alleles or by selfishly distorting the laws of Mendelian inheritance. Here, we show that the supergene haplotype associated with multiple-queen colonies in Alpine silver ants is a maternal effect killer. All eggs from heterozygous queens failed to hatch when they did not inherit this haplotype. Hence, the haplotype specific to multiple-queen colonies is a selfish genetic element that enhances its own transmission by causing developmental arrest of progeny that do not carry it. At the population level, such transmission ratio distortion favors the spread of multiple-queen colonies, to the detriment of the alternative haplotype associated with single-queen colonies. Hence, selfish gene drive by one haplotype will impact the evolutionary dynamics of alternative forms of colony social organization. This killer hidden in a social supergene shows that large nonrecombining genomic regions are prone to cause multifarious effects across levels of biological organization.

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Section: Discussionmentioning

confidence: 97%

mentioning

confidence: 99%

Maternal effect killing by a supergene controlling ant social organization

Avril

Purcell

Béniguel

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…One half of the supergene, from 2-7.5 Mbp on chromosome 3, is associated with split sex ratio. The other half, from 7.5-12.5 Mbp, which includes the gene knockout identified as a candidate conserved gene influencing social structure in other Formica species (29), is associated with social structure (Fig. 2).…”

Section: Discussionmentioning

confidence: 99%

“…In an alternative scenario, a gene or supergene influencing sex ratio could predate the appearance of persistent social polymorphism; when alternative social structures emerged, selection for male-biased production in colonies with lower average relatedness and for gyne-biased production in colonies with higher average relatedness could have led to the appearance of linked genetic variants favoring one or more queens. The dual roles of linked supergenes in shaping social organization and sex ratio in Formica species could help to explain why this supergene has persisted for millions of years (29). Future studies could examine these speculative scenarios by seeking evidence of sex ratio supergenes in other, distantly related Formica species.…”

Section: Discussionmentioning

confidence: 99%

“…Formica selysi has a similar chromosome-spanning supergene underlying colony queen number, but there is no detectable overlap in gene content between the two (28). More recently, both ant social supergenes were shown to underlie colony queen number in other congeneric species (29,30). In both systems, the haplotype associated with multi-queen (= polygyne) social structure is a selfish transmission distorter (31)(32)(33).…”

Section: Introductionmentioning

confidence: 99%

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Linked supergenes underlie split sex ratio and social organization in an ant

Lagunas-Robles

Purcell

Brelsford

2021

Preprint

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Sexually reproducing organisms usually invest equally in male and female offspring. Deviations from this pattern have led researchers to new discoveries in the study of parent-offspring conflict, genomic conflict, and cooperation. Some social insect species exhibit the unusual population-level pattern of split sex ratio, wherein some colonies specialize in the production of future queens and others specialize in the production of males. Theoretical work focused on the relatedness asymmetries emerging from haplodiploid inheritance, whereby queens are equally related to daughters and sons, but their daughter workers are more closely related to sisters than to brothers, led to a series of testable predictions and spawned many empirical studies of this phenomenon. However, not all empirical systems follow predicted patterns, so questions remain about how split sex ratio emerges. Here, we sequence the genomes of 138 Formica glacialis workers from 34 male-producing and 34 gyne-producing colonies to determine whether split sex ratio is under genetic control. We identify a supergene spanning 5.5 Mbp that is closely associated with sex allocation in this system. Strikingly, this supergene is adjacent to another supergene spanning 5 Mbp that is associated with variation in colony queen number. We identify a similar pattern in a second related species, Formica podzolica. The discovery that split sex ratio is determined, at least in part, by a supergene in two species opens a new line of research on the evolutionary drivers of split sex ratio.Significance StatementSome social insects exhibit split sex ratio, wherein some colonies produce future queens and others produce males. This phenomenon spawned many influential theoretical studies and empirical tests, both of which have advanced our understanding of parent-offspring conflicts and cooperation. However, some empirical systems did not follow theoretical predictions, indicating that researchers lack a comprehensive understanding of the drivers of split sex ratio. Here, we show that split sex ratio is associated with a large genomic region in two ant species. The discovery of a genetic basis for sex allocation in ants provides a novel explanation for this phenomenon, particularly in systems where empirical observations deviate from theoretical predictions.

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Social structure of perennialVespula squamosawasp colonies

Dyson

Crossley

Ray

et al. 2022

Ecology and Evolution

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Many social species show variation in their social structure in response to different environmental conditions. For example, colonies of the yellowjacket wasp Vespula squamosa are typically headed by a single reproductive queen and survive for only a single season. However, in warmer climates, V. squamosa colonies sometimes persist for multiple years and can grow to extremely large size. We used genetic markers to understand patterns of reproduction and recruitment within these perennial colonies. We genotyped V. squamosa workers, pre‐reproductive queens, and males from perennial colonies in the southeastern United States at 10 polymorphic microsatellite loci and one mitochondrial DNA locus. We found that V. squamosa from perennial nests were produced by multiple reproductives, in contrast to typical annual colonies. Relatedness of nestmates from perennial colonies was significantly lower than relatedness of nestmates from annual colonies. Our analyses of mitochondrial DNA indicated that most V. squamosa perennial colonies represented semiclosed systems whereby all individuals belonged to a single matriline despite the presence of multiple reproductive females. However, new queens recruited into perennial colonies apparently mated with non‐nestmate males. Notably, perennial and annual colonies did not show significant genetic differences, supporting the hypothesis that perennial colony formation represents an instance of social plasticity. Overall, our results indicate that perennial V. squamosa colonies show substantial changes to their social biology compared to typical annual colonies and demonstrate variation in social behaviors in highly social species.

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An Ancient and Eroded Social Supergene Is Widespread across Formica Ants

Cited by 67 publications

References 68 publications

Maternal effect killing by a supergene controlling ant social organization

Maternal effect killing by a supergene controlling ant social organization

Linked supergenes underlie split sex ratio and social organization in an ant

Social structure of perennialVespula squamosawasp colonies

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