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

Abstract

Despite its fundamental role in development, sex determination is highly diverse among animals. Approximately 20% of all animals are haplodiploid, with haploid males and diploid females. Haplodiploid species exhibit diverse but poorly understood mechanisms of sex determination. Some hymenopteran insect species exhibit single-locus complementary sex determination (sl-CSD), where heterozygosity at a polymorphic sex locus initiates female development. Diploid males are homozygous at the sex locus and represent a genetic load because they are inviable or sterile. Inbreeding depression associated with CSD is therefore expected to select for other modes of sex determination resulting in fewer or no diploid males. Here, we investigate an alternative, heretofore hypothetical, mode of sex determination: multiple-locus CSD (ml-CSD). Under ml-CSD, diploid males are predicted to develop only from zygotes that are homozygous at all sex loci. We show that inbreeding for eight generations in the parasitoid wasp Cotesia vestalis leads to increasing proportions of diploid males, a pattern that is consistent with ml-CSD but not sl-CSD. The proportion of diploid males (0.27 6 0.036) produced in the first generation of inbreeding (mother-son cross) suggests that two loci are likely involved. We also modeled diploid male production under CSD with three linked loci. Our data visually resemble CSD with linked loci because diploid male production in the second generation was lower than that in the first. To our knowledge, our data provide the first experimental support for ml-CSD.

Insect sex determination: it all evolves around transformer

“…Females are heterozygous and males hemizygous at this locus, but the biochemical details of CSD function are not yet completely known [39 ,45]. Interestingly, the csd primary signal can also be based on multiple loci (ml-csd) [64]. However, in all csd cases the paternally contributed genome provides the second csd allele that is required for female development.…”

Thelytoky and Sex Determination in the Hymenoptera: Mutual Constraints

“…In a sl-CSD system, al-ready the first generation of sib-matings should lead to the occurrence of diploid males in half of the broods. In a ml-CSD system, several generations of inbreeding may be required to observe diploid male production, depending on the number of loci involved [Cook, 1993;de Boer et al, 2008].…”

“…It has been argued that ml-CSD can evolve from sl-CSD by 1 or several duplications of the CSD locus and may be favored by selection, because it reduces the inbreeding load resulting from diploid male production [Crozier, 1971;van Wilgenburg et al, 2006;de Boer et al, 2008]. Analogously, it is argued above that ml-CSD may be conducive to the evolution of thelytoky with automixis because it increases the probability that at least 1 CSD locus occurs in a region of the genome that is sheltered from recombination.…”

“…It is worth considering whether such dynamics could possibly be used as a window of opportunity to study sex determination. It is difficult and labor-intensive, for example, to experimentally distinguish non-CSD mechanisms of sex determination from ml-CSD, because many generations of inbreeding are required to achieve a level of homozygosity that allows ruling out CSD involving several loci based on the lack of diploid males among inbred offspring [Cook, 1993;de Boer et al, 2008;Ma et al, 2013]. In principle, complete homozygosity could be achieved more quickly if it was possible to introduce a strain of PI-Wolbachia that induces thelytoky by gamete duplication in the species under investigation.…”

Análise da variabilidade genética de uma pequena população de Frieseomelitta varia (Hymenoptera, Apidae, Meliponini) por meio de análise do DNA mitocondrial, microssatélites e morfometria geométrica das asas

“…Em Hymenoptera o sistema de determinação sexual é governado pela composição alélica de um único loco, denominado Complementary Sex Determination (sl-CSD). (Beye et al, 2003;Hedrick et al, 2006;de Boer et al, 2007;de Boer et al, 2008). Os machos são hemizigotos enquanto que as fêmeas são heterozigotas para o loco CSD.…”