Absence of complementary sex determination in twoLeptopilinaspecies (Figitidae, Hymenoptera) and a reconsideration of its incompatibility with endosymbiont‐induced thelytoky

Abstract

Complementary sex determination (CSD) is a widespread sex determination mechanism in haplodiploid Hymenoptera. Under CSD, sex is determined by the allelic state of one or multiple CSD loci. Heterozygosity at one or more loci leads to female development, whereas hemizygosity of haploid eggs and homozygosity of diploid eggs results in male development. Sexual (arrhenotokous) reproduction normally yields haploid male and diploid female offspring. Under asexual reproduction (thelytoky), diploidized unfertilized eggs develop into females. Thelytoky is often induced by bacterial endosymbionts that achieve egg diploidization by gamete duplication. As gamete duplication leads to complete homozygosity, endosymbiont‐induced thelytokous reproduction is presumed to be incompatible with CSD, which relies on heterozygosity for female development. Previously, we excluded CSD in four Asobara (Braconidae) species and proposed a two‐step mechanism for Wolbachia‐induced thelytoky in Asobara japonica. Here, we conclusively reject CSD in two cynipid wasp species, Leptopilina heterotoma and Leptopilina clavipes. We further show that thelytoky in L. clavipes depends on Wolbachia titer but that diploidization and feminization steps cannot be separated, unlike in A. japonica. We discuss what these results reveal about the sex determination mechanism of L. clavipes and the presumed incompatibility between CSD and endosymbiont‐induced thelytoky in the Hymenoptera.

Infection dynamics of endosymbionts that manipulate arthropod reproduction

“…Examples were derived with T 0.95, and, for MK, Φ 0.85. a), b) and f) show results for diplodiploid hosts, and c), d), e), g) and h) for haplodiploid hosts. For all parameter combinations that do not fulfil the CI invasion condition (equations 16, 19 and 22), invasion is not possible and hence the equilibrium frequency is zero, which in these examples applies to all cases where F <= 1 (f, g, h). For these cases, the corresponding threshold frequencies are shown (dashed lines).…”

“…PI can be achieved via either a one- or a two-step mechanism (Verhulst et al ., 2023). In the two-step mechanism, endosymbiont-induced diploidization and feminization are two separate steps (Ma et al ., 2015), whereas in the one-step mechanism, they co-occur in a manner that cannot be separated (Chen et al ., 2022; Wang & Verhulst, 2022). The two-step mechanism seems to be necessary whenever diploidization does not automatically lead to feminization, and here, the feminization of diploid males is conceptually identical to the essential role that it plays in FE.…”

The feedback loop of thetransformergene results in proper feminization under multiple sex determination signals in the ant,Vollenhovia emeryi

“…The haplodiploid sex determination system allows females to control the sex ratio [15,16]; however, involvement of the CSD locus imposes a high inbreeding cost (up to 50%; Figure 1A), since diploid males resulting from homozygosity at the CSD locus are typically sterile or inviable, and small populations can fall into an extinction vortex [8,[17][18][19][20]. On the other hand, some hymenopterans (ants and wasps) have evolved a CSD-independent sex-determination system [21][22][23][24][25] or multi-locus CSD (ml-CSD) systems [26][27][28][29][30][31]. As a result, diploid male production is avoided or reduced under inbreeding.…”