Sex determination and inbreeding depression in an ant with regular sib-mating

Abstract

Haplodiploidy is one of the most widespread mechanisms of sex determination in animals. In many Hymenoptera, including all hitherto investigated social species, diploid individuals, which are heterozygous at the sex locus, develop as females, whereas haploid, hemizygous individuals develop as males (single-locus complementary sex determination, sl-CSD). Inbreeding leads to homozygosity at the sex locus, resulting in the production of diploid males, which are usually sterile and constitute a considerable fitness cost. Nevertheless, regular inbreeding without diploid male production is known from several solitary wasps, suggesting that in these species sex is not determined by sl-CSD but alternative mechanisms. Here, we examine sex determination in an ant with regular inbreeding, Cardiocondyla obscurior. The almost complete absence of diploid males after 10 generations of brother-sister mating in the laboratory documents for the first time the absence of sl-CSD and CSD with two or a few unlinked sex loci in a species of social Hymenoptera. Queens, which mated with a brother, appeared to decrease the number of males in their brood, as expected from the relatedness relationships under inbreeding. In contrast, some colonies began to show signs of an inbreeding depression after several generations of sib-mating, such as shortened queen life span, higher brood mortality, and a shift to more male-biased sex ratios in some colonies, presumably due to lower insemination capability of sperm.

Experimental Support for Multiple-Locus Complementary Sex Determination in the Parasitoid Cotesia vestalis

“…Several studies suggested their results might be better explained by ml-CSD rather than sl-CSD (Garofolo 1973;Kerr 1974;Naito et al 2000), while others found no support for ml-CSD in a range of other species (Skinner and Werren 1980;Cook 1993a;Periquet et al 1993;Butcher et al 2000;Niyibigira et al 2004a;Schrempf et al 2006). Here, we show that inbreeding the braconid wasp C. vestalis for eight generations results in increasing proportions of DM and an increasingly male-biased sex ratio (Figures 3 and 4).…”

“…A similar diversity of sex determining systems can be found more broadly in the Braconidae as well (Beukeboom et al 2000;Wu et al 2005;van Wilgenburg et al 2006). Another interesting group is the ant family, Formicidae, because many species are believed to have sl-CSD (van Wilgenburg et al 2006), but it appears to be absent in the inbreeding ant Cardiocondyla batesii (Schrempf et al 2006). Also, a number of socially parasitic ants engage in inbreeding, bringing into question whether they have sl-CSD (Crozier and Pamilo 1996).…”

Multiple mating in the ant Cataglyphis cursor: testing the sperm limitation and the diploid male load hypotheses

“…First, genetic mechanisms may prevent homozygosity at the CSD loci, such as multiple-loci complementary sex determination (ml-CSD) (Crozier, 1971) or genomic imprinting (Beukeboom, 1995). To date, ml-CSD has not been directly shown in a social Hymenoptera, but good evidence against single-locus complementary sex determination has recently been published for Cardiocondyla elegans (Schrempf et al, 2006). Genomic imprinting cannot be tested without appropriate cytogenetic markers, such as the paternal sex-ratio chromosome (PSR) in Nasonia vitripennis (Dobson and Tanouye, 1998;Beukeboom and Werren, 2000), which are not available for any ant species.…”

Bee genetics and conservation

“…Both authors showed that haplodiploids without complementary sex determination experience substantial inbreeding depression, although lower than that experienced by diploids. Furthermore, even some haplodiploid species with systematically-inbreeding mating systems still experience inbreeding depression (Luna and Hawkins, 2004;Schremph et al, 2006). These results indicate that haplodiploidy does not offer complete immunity from inbreeding depression, and that both overdominance and dominance in female-limited genes likely constitute a significant source of inbreeding depression in haplodiploids.…”