No evidence for increased extinction proneness with decreasing effective population size in a parasitoid with complementary sex determination and fertile diploid males

BACKGROUND: In species with single locus complementary sex determination (sl-CSD), the sex of individuals depends on their genotype at one single locus with multiple alleles. Haploid individuals are always males. Diploid individuals are females when heterozygous, but males when homozygous at the sex-determining locus. Diploid males are typically unviable or effectively sterile, hence imposing a genetic load on populations. Diploid males are produced from matings of partners that share an allele at the sex-determining locus. The lower the allelic diversity at the sex-determining locus, the more diploid males are produced, ultimately impairing the growth of populations and jeopardizing their persistence. The gregarious endoparasitoid wasp Cotesia glomerata is one of only two known species with sl-CSD and fertile diploid males. RESULTS: By manipulating the relatedness of the founders, we established replicated experimental populations of the parasitoid C. glomerata differing in their genetic effective size, and thus in allelic richness at the sex-determining locus and in the expected magnitude of diploid male production. Our long-term survey of population welfare and persistence did not provide evidence for increased proneness to population extinction with decreasing initial genetic effective population size. Most recorded surrogates of fitness nevertheless decayed over time and most experimental populations eventually went extinct, suggesting that the negative effects of inbreeding outweighed any premium from the fertility of diploid males. CONCLUSIONS: The fertility of diploid males may have evolved as an adaptation prompted by the risk of extinction looming over small isolated populations of species with sl-CSD. However, fertility of diploid males does not negate the costs imposed by their production, and although it may temporarily stave off extinction, it is not sufficient to eradicate the negative effects of inbreeding.