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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.
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Unexpected absence of a multiple-queen supergene haplotype from supercolonial populations of Formica ants
Abstract Ants exhibit many complex social organization strategies. One particularly elaborate strategy is supercoloniality, in which a colony consists of many interconnected nests (= polydomy) with many queens (= polygyny). In many species of Formica ants, an ancient queen number supergene determines whether a colony is monogyne (= headed by single queen) or polygyne. The presence of the rearranged P haplotype typically leads colonies to be polygyne. However, the presence and function of this supergene polymorphism have not been examined in supercolonial populations. Here, we use genomic data from species in the Formica rufa group to determine whether the P haplotype leads to supercoloniality. In a Formica paralugubris population, we find that nests are polygyne despite the absence of the P haplotype in workers. We find spatial genetic ancestry patterns in nests consistent with supercolonial organization. Additionally, we find that the P haplotype is also absent in workers from supercolonial Formica aquilonia and Formica aquilonia × polyctena hybrid populations but is present in some Formica polyctena workers. We conclude that the P haplotype is not necessary for supercoloniality in the Formica rufa group, despite its long-standing association with non-supercolonial polygyny across the Formica genus.
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- Award ID(s):
- 2215705
- PAR ID:
- 10656461
- Editor(s):
- Rogers, Rebekah; Larson, Erica
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Evolutionary Biology
- Volume:
- 38
- Issue:
- 4
- ISSN:
- 1420-9101
- Page Range / eLocation ID:
- 543 to 553
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/jeb/voaf023
