Fitness and the level of homozygosity in a social insect

Abstract

To date very few studies have addressed the effects of inbreeding in social Hymenoptera, perhaps because the costs of inbreeding are generally considered marginal owing to male haploidy whereby recessive deleterious alleles are strongly exposed to selection in males. Here, we present one of the first studies on the effects of queen and worker homozygosity on colony performance. In a wild population of the ant Formica exsecta, the relative investment of single‐queen colonies in sexual production decreased with increased worker homozygosity. This may either stem from increased homozygosity decreasing the likelihood of diploid brood to develop into queens or a lower efficiency of more homozygous workers at feeding larvae and thus a lower proportion of the female brood developing into queens. There was also a significant negative association between colony age and the level of queen but not worker homozygosity. This association may stem from inbreeding affecting queen lifespan and/or their fecundity, and thus colony survival. However, there was no association between queen homozygosity and colony size, suggesting that inbreeding affects colony survival as a result of inbred queens having a shorter lifespan rather than a lower fecundity. Finally, there was no significant association between either worker or queen homozygosity and the probability of successful colony founding, colony size and colony productivity, the three other traits studied. Overall, these results indicate that inbreeding depression may have important effects on colony fitness by affecting both the parental (queen) and offspring (worker) generations cohabiting within an ant colony.

Natal Dispersal, Mating Patterns, and Inbreeding in the AntFormica exsecta

“…The study population is genetically structured, and previous population genetics analyses suggest sex-biased dispersal, with males mediating gene flow over longer distance than queens (Sundström et al 2003). As a result, the population is inbred, with extensive variation in inbreeding both at the queen and the colony level (Haag-Liautard et al 2009). …”

“…The study population of the narrow-headed ant Formica exsecta is located on five islands close to Tvärminne Zoological station in Hanko, on the SW coast of Finland, and has been surveyed for demography, colony kin structure, colony size, productivity and sex ratio since 1994 (Sundström et al 2003, Haag-Liautard 2009). The yearly standing population comprises on average 100 colonies, the majority of which are headed by a single reproductive queen (monogyny), which is either singly or multiply mated.…”

“…The incipient colony queens, 8-16 workers from 222 established colonies, and 5-10 males from 104 colonies where available were genotyped at 10 highly variable microsatellite loci, as described in Haag- Liautard et al 2009). We used the homozygosity measure of Aparicio et al (2006), HL, as proxy for inbreeding in queens and the workers.…”

“…For incipient colonies we directly genotyped the queens and the sperm they had stored during mating, to assess the genotypes of their male mates and to construct worker genotypes. The average HL of the deduced worker genotypes was then used as measure of colony / worker homozygosity of the incipient colonies, following Haag- Liautard et al (2009). In short, the dissected spermatheca was placed in ethanol and sperm extracted using sterile needles under a stereomicroscope with 50x magnification.…”

“…Diploid males are typically unviable and/or infertile, and are produced instead of workers or reproductive females in inbred colonies (Tarpy and Page 2002). In addition to diploid male production, inbreeding depression has also been shown to impair colony productivity and lifespan in ants (Whitehorn et al 2009, Haag-Liautard et al 2009; but see Kureck et al 2013).…”