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The Underlying Genetics and Evolutionary History of a Sex Ratio Supergene in Formica Ants

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Abstract

In solitary sexually reproducing diploid organisms, frequency dependent selection maintains the population sex ratio at an equal proportion of male to female offspring. A 1:1 sex ratio equilibrium is expected because each sex contributes half of their ancestry to the following generation. Typically, selection occurs at the level of the parents. This contrasts sex ratio predictions in social Hymenoptera (ants, bees, and wasps), where there are two stark differences. 1) In social Hymenoptera, sex determination leads to a difference in ploidy level, where males are haploid, and females are diploid. 2) Selection on sex ratios is more complex in social Hymenoptera as brood care is primarily performed by sterile workers instead of the parents. As a result of these differences, reproductive queens and workers can be in conflict because diploid workers are more related to their diploid sisters than to their haploid brothers. Split sex ratio, where colonies produce only future queens (=gynes) or only males, is an extreme form of biased sex ratios and is observed throughout social Hymenoptera. But what leads to split sex ratios? A meta-analysis found the variance in split sex ratio can be explained, in part, by relatedness asymmetries (~20%) and colony queen number (~5%). A genetic polymorphism that predisposes colonies to produce only gynes or only males could explain some of the variance. In this dissertation, I aim to answer three overarching questions in Formica ants. In Chapter 1, I ask if a genetic polymorphism underlies colony sex ratio in two species. I find the presence of a non-recombining haplotype is associated with colony gyne-production in single-queen colonies. In Chapter 2, I ask how a gyne-producing haplotype originated within the genus. I find there are two origins for the gyne-producing haplotype that formed because of two different double-recombinant events. In Chapter 3, I expand to include multiple populations of the Chapter 1 species. I ask if multi-queen colonies also harbor the gyne-producing haplotype and whether population haplotype frequencies vary. I find species- and population-level variation exists in multi-queen colony sex ratios. I also find spatial variation in haplotype frequencies in one species but not the other. In summary, the presence of a non-recombining haplotype determines colony gyne production. The gyne-producing haplotype has at least two origins, one origin in Nearctic species and another origin in a Palearctic lineage. Intraspecific population frequency variation of the gyne-producing haplotype may lead to other colonies taking the role of gyne production.

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This item is under embargo until July 19, 2025.