Antagonistic selection has long been considered a major driver of the formation and expansion of sex chromosomes. For example, sexually antagonistic variation on an autosome can select for suppressed recombination between that autosome and the sex chromosome, leading to a neo-sex chromosome. Autosomal supergenes, chromosomal regions containing tightly linked variants affecting the same complex trait, share similarities with sex chromosomes, raising the possibility that sex chromosome evolution models can explain the evolution of genome structure and recombination in other contexts. We tested this premise in a Formica ant species wherein we identified four supergene haplotypes on chromosome 3 underlying colony social organization and sex ratio. We discovered a novel rearranged supergene variant (9r) on chromosome 9 underlying queen miniaturization. The 9r is in strong linkage disequilibrium with one chromosome 3 haplotype (P2) found in multi-queen (polygyne) colonies. We suggest that queen miniaturization is strongly disfavored in the single queen (monogyne) background, and thus socially antagonistic. As such, divergent selection experienced by ants living in alternative social ‘environments’ (monogyne and polygyne) may have contributed to the emergence of a genetic polymorphism on chromosome 9 and associated queen-size dimorphism. Consequently, an ancestral polygyne-associated haplotype may have expanded to include the polymorphism on chromosome 9, resulting in a larger region of suppressed recombination spanning two chromosomes. This process is analogous to the formation of neo-sex chromosomes and consistent with models of expanding regions of suppressed recombination. We propose that miniaturized queens, 16-20% smaller than queens without 9r, could be incipient intraspecific social parasites.
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Linked supergenes underlie split sex ratio and social organization in an ant
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 cooperative breeding. 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 predicted that worker control of sex ratio and variation in relatedness asymmetry among colonies would cause each colony to specialize in the production of one sex. While some empirical tests supported theoretical predictions, others deviated from them, leaving many questions about how split sex ratio emerges. One factor yet to be investigated is whether colony sex ratio may be influenced by the genotypes of queens or workers. 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 future research on the evolutionary drivers of split sex ratio.
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- NSF-PAR ID:
- 10319956
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 118
- Issue:
- 46
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Most supergenes discovered so far are young, occurring in one species or a few closely related species. An ancient supergene in the ant genus
Formica presents an unusual opportunity to compare supergene‐associated phenotypes and the factors that influence the persistence of polymorphism in different species. We investigate the genetic architecture of social organization inFormica francoeuri , an ant species native to low‐ and mid‐elevation semiarid regions of southern California, and describe an efficient technique for estimating mode of social organization using population genomic data. Using this technique, we show thatF. francoeuri exhibits polymorphism in colony social organization and that the phenotypic polymorphism is strongly associated with genotypes within theFormica social supergene region. The distribution of supergene haplotypes inF. francoeuri differs from that of related speciesFormica selysi in that colonies with multiple queens contain almost exclusively workers that are heterozygous for alternative supergene haplotypes. Moreover, heterozygous workers exhibit allele‐specific expression of the polygyne‐associated haplotype at the candidate geneKnockout, which is thought to influence social organization. We also report geographic population structure and variation in worker size across a large fraction of the species range. Our results suggest that, although theFormica supergene is conserved within the genus, the mechanisms that maintain the supergene and its associated polymorphisms differ among species. -
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Abstract Supergenes, regions of the genome with suppressed recombination between sets of functional mutations, contribute to the evolution of complex phenotypes in diverse systems. Excluding sex chromosomes, most supergenes discovered so far appear to be young, being found in one species or a few closely related species. Here, we investigate how a chromosome harbouring an ancient supergene has evolved over about 30 million years (Ma). The
Formica supergene underlies variation in colony queen number in at least five species. We expand previous analyses of sequence divergence on this chromosome to encompass about 90 species spanning theFormica phylogeny. Within the nonrecombining region, the geneknockout contains 22 single nucleotide polymorphisms (SNPs) that are consistently differentiated between two alternative supergene haplotypes in divergent EuropeanFormica species, and we show that these same SNPs are present in mostFormica clades. In these clades, including an early diverging NearcticFormica clade, individuals with alternative genotypes atknockout also have higher differentiation in other portions of this chromosome. We identify hotspots of SNPs along this chromosome that are present in multipleFormica clades to detect genes that may have contributed to the emergence and maintenance of the genetic polymorphism. Finally, we infer three gene duplications on one haplotype, based on apparent heterozygosity within these genes in the genomes of haploid males. This study strengthens the evidence that this supergene originated early in the evolution ofFormica and that just a few loci in this large region of suppressed recombination retain strongly differentiated alleles across contemporaryFormica lineages. -
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Abstract Invasive social insects rank among the most damaging of terrestrial species. They are responsible for extensive damage and severely threaten the biodiversity of environments where they are introduced. Variation in colony social form commonly occurs in introduced populations of yellowjacket wasps (genus
Vespula ). In particular, invasive colonies may contain multiple queens (i.e., polygyne) and persist several years, while in the native range, the colonies are usually annual and harbor a single queen (i.e., monogyne). In this study, we used genome‐wide loci obtained by double digest restriction site‐associated DNA sequencing (RADseq) to investigate the genetic structure and queen turnover in colonies of the western yellowjacket,Vespula pensylvanica , in their introduced range in Hawaii. Of the 27 colonies monitored over four months (October–January), 19 were polygyne and already contained multiple queens on the first day of sampling. Contrary to previous speculation, this finding suggests that polygyny often arises early in the annual colony cycle, before the production of new queens in the fall. Furthermore, polygyne colonies exhibited a prolonged average lifespan relative to those headed by a single queen. As a result, there is no clear window during which colony eradication efforts would be more effective than upon first discovery. The relatedness among nestmate queens was slightly above zero, indicating that these colonies are generally composed of nonrelatives. The queen turnover within each colony was low, and we detected some full‐sibling workers sampled up to four months apart. Finally, we did not detect any population structure among colonies, suggesting that queens disperse up to several kilometers. Taken together, our results provide the first insights into the requeening dynamics in this invasive and incipiently polygyne population and illuminate the early establishment of multiple long‐lasting queens in these damaging colonies. -
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Acromyrmex leaf-cutting ants are well-suited for investigating the evolution of complex mating strategies because both polygyny and polyandry co-occur in this genus. We used microsatellite markers and parentage inference in five South AmericanAcromyrmex species to study how different selective pressures influence the evolution of polygyny and polyandry. We show thatAcromyrmex species exhibit independent variation in mating biology and social structure, and polygyny and polyandry are not necessarily negatively correlated within genera. One species,Acromyrmex lobicornis , displays a significantly lower mating frequency compared to others, while another species,A. lundii , appears to have reverted to obligate monogyny. These variations appear to have a small impact on average intra-colonial relatedness, although the biological significance of such a small effect size is unclear. All species show significant reproductive skew between patrilines, but there was no significant difference in reproductive skew between any of the sampled species. We find that the evolution of social structure and mating biology appear to follow independent evolutionary trajectories in different species. Finally, we discuss the evolutionary implications that mating biology and social structure have on life history evolution inAcromyrmex leaf-cutting ants. Significance statement Many species of eusocial insects have colonies with multiple queens (polygyny), or queens mating with multiple males (polyandry). Both behaviors generate potentially beneficial genetic diversity in ant colonies as well as reproductive conflict. The co-occurrence of both polygyny and polyandry in a single species is only known from few ant species. Leaf-cutting ants have both multi-queen colonies and multiply mated queens, providing a well-suited system for studying the co-evolutionary dynamics between mating behavior and genetic diversity in colonies of eusocial insects. We used microsatellite markers to infer the socio-reproductive behavior in five South American leaf-cutter ant species. We found that variation in genetic diversity in colonies was directly associated with the mating frequencies of queens, but not with the number of queens in a colony. We suggest that multi-queen nesting and mating frequency evolve independently of one another, indicating that behavioral and ecological factors other than genetic diversity contribute to the evolution of complex mating behaviors in leaf-cutting ants.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2101427118
