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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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Molecular underpinnings of plasticity and supergene-mediated polymorphism in fire ant queens
Characterizing molecular underpinnings of plastic traits and balanced polymorphisms represent two important goals of evolutionary biology. Fire ant gynes (pre-reproductive queens) provide an ideal system to study potential links between these phenomena because they exhibit both supergene-mediated polymorphism and nutritional plasticity in weight and colony-founding behavior. Gynes with the inversion supergene haplotype are lightweight and depend on existing workers to initiate reproduction. Gynes with only the ancestral, non-inverted gene arrangement accumulate more nutrient reserves as adults and, in a distinct colony-founding behavior, initiate reproduction without help from workers. However, when such gynes overwinter in the natal nest they develop an environmentally induced lightweight phenotype and colony-founding behavior, similar to gynes with the inversion haplotype that have not overwintered. To evaluate the extent of shared mechanisms between plasticity and balanced polymorphism in fire ant gyne traits, we assessed whether genes with expression variation linked to overwintering plasticity may be affected by evolutionary divergence between supergene haplotypes. To do so, we first compared transcriptional profiles of brains and ovaries from overwintered and non-overwintered gynes to identify plasticity-associated genes. These genes were enriched for metabolic and behavioral functions. Next, we compared plasticity-associated genes to those differentially expressed by supergene genotype, revealing a significant overlap of the two sets in ovarian tissues. We also identified sequence substitutions between supergene variants of multiple plasticity-associated genes, consistent with a scenario in which an ancestrally plastic phenotype responsive to an environmental condition became increasingly genetically regulated.
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- PAR ID:
- 10561753
- Publisher / Repository:
- Oxford University Press on behalf of the European Society of Evolutionary Biology
- Date Published:
- Journal Name:
- Journal of Evolutionary Biology
- ISSN:
- 1420-9101
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Parsch, John (Ed.)Abstract Supergenes underlying complex trait polymorphisms ensure sets of coadapted alleles remain genetically linked. Despite their prevalence in nature, the mechanisms of supergene effects on genome regulation are poorly understood. In the fire ant Solenopsis invicta, a supergene containing over 500 individual genes influences trait variation in multiple castes to collectively underpin a colony level social polymorphism. Here, we present results of an integrative investigation of supergene effects on gene regulation. We present analyses of ATAC-seq data to investigate variation in chromatin accessibility by supergene genotype and STARR-seq data to characterize enhancer activity by supergene haplotype. Integration with gene co-expression analyses, newly mapped intact transposable elements (TEs), and previously identified copy number variants (CNVs), collectively reveal widespread effects of the supergene on chromatin structure, gene transcription, and regulatory element activity, with a genome-wide bias for open chromatin and increased expression in the presence of the derived supergene haplotype, particularly in regions that harbor intact TEs. Integrated consideration of CNVs and regulatory element divergence suggests each evolved in concert to shape the expression of supergene encoded factors, including several transcription factors that may directly contribute to the trans-regulatory footprint of a heteromorphic social chromosome. Overall, we show how genome structure in the form of a supergene has wide-reaching effects on gene regulation and gene expression.more » « less
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Rogers, Rebekah; Larson, Erica (Ed.)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.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/jeb/voae159
