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Abstract Selfish genetic elements subvert the normal rules of inheritance to unfairly propagate themselves, often at the expense of other genomic elements and the fitness of individuals carrying them. Social life provides diverse avenues for the propagation of such elements. In the fire ant Solenopsis invicta, polymorphic social organization is controlled by a social chromosome, one variant of which (Sb) enhances its own transmission in polygyne colonies through effects on caste development and queen acceptance by workers. Whether the selfish effects of Sb extend to haploid (reproductive) males in this system is less clear. Here, we demonstrate a strong overrepresentation of the Sb social chromosome haplotype in reproductive males, relative to Mendelian expectations, in both the pupal and adult stages. We tested for the presence of selective execution of adult SB males by workers but did not detect such behavior. Combined with the presence of a strong imbalance in the haplotype frequencies already early in the pupal stage, these results indicate that the Sb supergene may distort male haplotype frequencies during larval or embryonic development. These findings are significant because they demonstrate yet another mode by which the selfish tendencies of the Sb supergene are manifested, illuminate complex interactions between Sb and the fire ant breeding system, inform the development of models of the population dynamics of Sb, and illustrate how a selfish supergene can increase in frequency in a population despite harboring deleterious mutations. 

Abstract Characterizing molecular underpinnings of plastic traits and balanced polymorphisms represent 2 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 behaviour. 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 behaviour, 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 behaviour, 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 the 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 behavioural functions. Next, we compared plasticity-associated genes to those differentially expressed by supergene genotype, revealing a significant overlap of the 2 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.