Male reproductive fitness and queen polyandry are linked to variation in the supergene Gp-9 in the fire ant Solenopsis invicta

Abstract

Supergenes are clusters of tightly linked loci maintained in specific allelic combinations to facilitate co-segregation of genes governing adaptive phenotypes. In species where strong selection potentially operates at different levels (e.g. eusocial Hymenoptera), positive selection acting within a population to maintain specific allelic combinations in supergenes may have unexpected consequences for some individuals, including the preservation of disadvantageous traits. The nuclear gene Gp-9 in the invasive fire ant Solenopsis invicta is part of a non-recombining, polymorphic supergene region associated with polymorphism in social organization as well as traits affecting physiology, fecundity and behaviour. We show that both male reproductive success and facultative polyandry in queens have a simple genetic basis and are dependent on male Gp-9 genotype. Gp-9(b) males are unable to maintain exclusive reproductive control over their mates such that queens mated to Gp-9(b) males remain highly receptive to remating. Queens mated to multiple Gp-9(B) males are rare. This difference appears to be independent of mating plug production in fertile males of each Gp-9 genotype. However, Gp-9(b) males have significantly lower sperm counts than Gp-9(B) males, which could be a cue to females to seek additional mates. Despite the reduced fitness of Gp-9(b) males, polygyne worker-induced selective mortality of sexuals lacking b-like alleles coupled with the overall success of the polygyne social form act to maintain the Gp-9(b) allele within nature. Our findings highlight how strong worker-induced selection acting to maintain the Gp-9(b) allele in the polygyne social form may simultaneously result in reduced reproductive fitness for individual sexual offspring.

Figure 1.

Regardless of social form or location, queens rarely mated with multiple Gp-9^B males, but were likely to be polyandrous if one partner was Gp-9^b. This difference corresponds to significantly different sperm counts of the two Gp-9 male haplotypes, but no differences in mating plug production. (a) Percentage of polyandrous queens and of Gp-9^b patrilines in each study population (light grey with dark outline, MS-P (Mississippi polygyne); black bars, FL-P (Florida polygyne); medium grey bars, FL-M (Florida monogyne)). Polyandry and proportion of insemination from Gp-9^b males covary regardless of social form. (b) Association of male Gp-9^b haplotype and polyandry. Polyandry (Gp-9^B males only) = (number of queens mated to two Gp-9^B males)/(number of queens mated to any Gp-9^B males). Polyandry (Gp-9^b males) = (number of queens mated to at least one Gp-9^b male)/(number of those queens with a second mate of any haplotype). (c) Total quantities of (i) mating plug fatty acids and (ii) sperm in Gp-9^b and Gp-9^B males.