A new cytogenetic mechanism for bacterial endosymbiont-induced parthenogenesis in Hymenoptera

Abstract

Vertically transmitted endosymbiotic bacteria, such as Wolbachia, Cardinium and Rickettsia, modify host reproduction in several ways to facilitate their own spread. One such modification results in parthenogenesis induction, where males, which are unable to transmit the bacteria, are not produced. In Hymenoptera, the mechanism of diploidization due to Wolbachia infection, known as gamete duplication, is a post-meiotic modification. During gamete duplication, the meiotic mechanism is normal, but in the first mitosis the anaphase is aborted. The two haploid sets of chromosomes do not separate and thus result in a single nucleus containing two identical sets of haploid chromosomes. Here, we outline an alternative cytogenetic mechanism for bacterial endosymbiont-induced parthenogenesis in Hymenoptera. During female gamete formation in Rickettsia-infected Neochrysocharis formosa (Westwood) parasitoids, meiotic cells undergo only a single equational division followed by the expulsion of a single polar body. This absence of meiotic recombination and reduction corresponds well with a non-segregation pattern in the offspring of heterozygous females. We conclude that diploidy in N. formosa is maintained through a functionally apomictic cloning mechanism that differs entirely from the mechanism induced by Wolbachia.

Figure 1

Different cytological mechanisms in apomictic and automictic parthenogenesis and their impact on the transition to homozygosity of a heterozygous locus whether crossing over between the locus and the centromere occurs or not (modified from Pearcy et al. 2006). Large and medium circles represent nuclei. Horizontal lines represent chromatids, with small circles showing the location of the centromere and letters representing alleles at a given locus. The parent is heterozygous (Aa) and the parthenogenesis causes inbreeding when its progeny becomes homozygote (AA or aa). (a(i)) Typical apomixis, (a(ii)) apomixis in Vavre et al. (2004), (b(i)) automixis, (b(ii)) automictic terminal fusion, (b(iii)) automictic central fusion, (b(iv)) automictic random fusion and (b(v)) automictic gamete duplication.

Figure 2

Meiosis and mitosis in unfertilized eggs of an arrhenotokous strain of N. formosa: (a) first metaphase, (b) first anaphase, (c) polar body (out of focus), divided first polar body and female pronucleus, (d,e) second polar body, divided first polar body and female pronucleus, (f) haploid telophase of first somatic mitosis and (g(i)(ii)) haploid telophase in embryo. Arrow head indicates polar nuclei. Scale bar represents 10 μm.

Figure 3

Meiosis and mitosis in a thelytokous strain of N. formosa: (a,b) first metaphase, (c) first telophase, (d(i)–(iii)) second metaphase and first polar body, (e(i)–(iii)) diploid telophase of first somatic mitosis and (f(i)–(v)) diploid telophase of second somatic mitosis. Arrow head indicates polar nuclei. Scale bar represents 10 μm.