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Gaining Insight into the Formica Social Supergene: Variation in Function and Clues on Evolutionary History

Creative Commons 'BY-SA' version 4.0 license

Supergenes are chromosomal regions of tightly linked loci experiencing reduced recombination that are inherited as a single unit when heterozygous. Polygenic morphological or behavioral traits can be maintained as distinct morphs, polymorphisms, within a population due to alternative supergene haplotypes that rarely engage in recombination with one another. Supergenes have been found in a variety of organisms resulting in various types of polymorphisms including mimicry complexes in butterflies, mating morphs in birds, and alternative social organization in ants. Formica is a genus of ants known for having alternative supergene haplotypes on chromosome 3, resulting in either monogyne or polygyne colonies. Monogyne colonies are single family units headed by one queen, with the associated haplotype being Sm. Polygyne colonies can have multiple queens, with the alternative supergene haplotype, Sp, being associated with this form of social organization. This system, first described in Formica selysi, is now known to be present in multiple other Formica species. As we continue to expand our knowledge of the Formica supergene, two questions emerge: is the function of the supergene the same across the genus and what genomic events contributed to the evolution of the supergene? To answer the first question, I utilized SNP data from 280 workers of Formica neoclara, sampled from 32 colonies and 8 transect locations spanning from California to British Columbia. I determined that F. neoclara is socially polymorphic, with monogyne and polygyne colony assignment stemming from three metrics: inferred queen number, average colony relatedness, and opposing homozygosity. This social polymorphism is due to the supergene found in other Formica species through principal component analysis as well as a genome wide association study. Finally, I analyzed the population structure of F. neoclara, showing that populations from all sampled regions are experiencing limited gene flow with one another; a finding supported by expected heterozygosity values, principal component analysis, and isolation by distance analysis. Unlike F. selysi, in which all individuals within polygyne colonies must have an Sp haplotype, polygyne colonies of F. neoclara can consist of workers with all three genotypes (Sm/Sm, Sm/Sp, Sp/Sp), showing that the mode of action of the supergene is not identical across the genus. To answer the second question, regarding the evolution of the supergene, I performed comparative linkage mapping with F. selysi and an outgroup genus Polyergus. I constructed a linkage map for Polyergus using RADseq data from 83 workers from a single colony, with F. selysi serving as a reference. While Polyergus has synteny with F. selysi in many regions of the genome, including a large portion of chromosome 3, there are also many regions with inversions. By performing comparative linkage mapping between genera, we can better understand the timing and conditions surrounding the evolution of the supergene. This thesis, in exploring the elements of the supergene both within a genus and between genera, provides a glimpse into the function and evolution of this social supergene.

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