skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


Title: 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.  more » « less
Award ID(s):
1942252 1754834
PAR ID:
10319956
Author(s) / Creator(s):
; ;
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
More Like this
  1. ; ; ; (, Journal of Evolutionary Biology)
    Abstract Most supergenes discovered so far are young, occurring in one species or a few closely related species. An ancient supergene in the ant genusFormicapresents 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. francoeuriexhibits polymorphism in colony social organization and that the phenotypic polymorphism is strongly associated with genotypes within theFormicasocial supergene region. The distribution of supergene haplotypes inF. francoeuridiffers from that of related speciesFormica selysiin 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 theFormicasupergene is conserved within the genus, the mechanisms that maintain the supergene and its associated polymorphisms differ among species. 
    more » « less
  2. ; ; ; (, Current Biology)
    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. 
    more » « less
  3. ; ; ; ; (, Molecular Ecology)
    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). TheFormicasupergene 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 theFormicaphylogeny. Within the nonrecombining region, the geneknockoutcontains 22 single nucleotide polymorphisms (SNPs) that are consistently differentiated between two alternative supergene haplotypes in divergent EuropeanFormicaspecies, and we show that these same SNPs are present in mostFormicaclades. In these clades, including an early diverging NearcticFormicaclade, individuals with alternative genotypes atknockoutalso have higher differentiation in other portions of this chromosome. We identify hotspots of SNPs along this chromosome that are present in multipleFormicaclades 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 ofFormicaand that just a few loci in this large region of suppressed recombination retain strongly differentiated alleles across contemporaryFormicalineages. 
    more » « less
  4. ; ; (, Proceedings of the National Academy of Sciences)
    Genes and the environment jointly shape individual traits, but the influence of indirect genetic effects (IGEs), arising from the genetic composition of interacting conspecific individuals, is often ignored or underemphasized. Moreover, because of practical challenges in characterizing IGEs, empirical research has fallen behind theoretical advancement. The fire antSolenopsis invictaoffers a uniquely suitable study system due to its distinct colony-level phenotypic variation (monogyne and polygyne social forms) attributed to IGEs of a social-supergene variant (ballele). A minority ofb-carrying workers (Bbgenotype) can trigger colony-level conversion from monogyne (single queen per colony) to polygyne (multiple queens per colony) behavior. This study investigated the mechanisms underlying this process via 400-ant microcolonies. We first showed that assimilatedBbworkers reduce aggression by hostBBworkers towardBbqueens, thus inducing polygyny, at rates observed earlier in experiments that used full-size (>20,000 ants) colonies. We then demonstrated that social conversion is facilitated by cuticular contact between the worker types, and verified the presence of nonvolatile cuticular pheromones that are necessary but not sufficient components underpinning this process. Follow-up experiments suggested that a second, polygyne worker-produced pheromone that is only released once such workers detect aBbqueen is also necessary but again insufficient, for full expression of the conversion phenomenon. Thus, multiple pheromonal components linked to presence of thebsupergene allele in colony workers appear to be involved in shaping social environments and thereby inducing, via IGEs, the transformation from monogyne to polygyne fire ant societies. 
    more » « less
  5. ; ; ; ; (, Insect Science)
    Females of many species are polyandrous. However, polyandry can give rise to conflict among individuals within families. We examined the level of polyandry and paternity skew in the common eastern yellowjacket wasp,Vespula maculifrons, in order to gain a greater understanding of conflict in social insects. We collected 10 colonies ofV. maculifronsand genotyped workers and prereproductive queens at highly variable microsatellite markers to assign each to a patriline. Genotypic data revealed evidence of significant paternity skew among patrilines. In addition, we found that patrilines contributed differentially to caste production (worker vs. queen), suggesting an important role for reproductive conflict not previously discovered. We also investigated if patterns of paternity skew and mate number varied over time. However, we found no evidence of changes in levels of polyandry when compared to historical data dating back almost 40 years. Finally, we measured a suite of morphological traits in individuals from the most common and least common patrilines in each colony to test if males that showed highly skewed reproductive success also produced offspring that differed in phenotype. Our data revealed weak correlation between paternity skew and morphological phenotype of offspring sired by different males, suggesting no evidence of evolutionary tradeoffs at the level investigated. Overall, this study is the first to report significant paternity and caste‐associated skew inV. maculifrons, and to investigate the phenotypic consequences of skew in a social wasp. Our results suggest that polyandry can have important consequences on the genetic and social structure of insect societies. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email