Single-Locus Recessive Inheritance of Asexual Reproduction in a Parasitoid Wasp

Abstract

The evolutionary maintenance of sex is one of the big unresolved puzzles in biology. All else being equal, all-female asexual populations should enjoy a two-fold reproductive advantage over sexual relatives consisting of male and female individuals. However, the "all else being equal" assumption rarely holds in real organisms because asexuality tends to be confounded with altered genomic constitutions such as hybridization and polyploidization or to be associated with parthenogenesis-inducing microbes. This limits the ability to draw general conclusions from any particular system. Here we describe a new system that permits unbiased comparisons of sexual and asexual reproduction: the parasitic wasp Lysiphlebus fabarum. Crossing experiments demonstrated that asexual reproduction has a simple genetic basis in this species and is consistently inherited as a single-locus recessive trait. We further show that the asexuality-inducing allele exhibits complete linkage to a specific allele at a microsatellite marker: all asexual lines in the field were homozygous for this allele, and the allele cosegregated perfectly with asexual reproduction in our experimental crossings. This novel system of contagious asexuality allows the production of closely related individuals with different reproductive modes, as well as the monitoring of the asexuality-inducing allele in natural and experimental populations.

The genetics of obligate parthenogenesis in an aphid species and its consequences for the maintenance of alternative reproductive modes

“…Moreover, repeated transitions to OP maintain a high level of genetic diversity in OP populations, allowing their persistence in the long term owing to higher evolvability (Simon et al, 2003;Sandrock and Vorburger, 2011). Despite the high potential of this contagious mechanism to generate obligate parthenogens, its actual incidence in the wild is largely unknown (Simon et al, 2003;Halkett et al, 2008;Sandrock and Vorburger, 2011). To date, for S. avenae, we have only indirect evidence of its occurrence in field populations (Simon et al, 1999;Dedryver et al, 2001Dedryver et al, , 2008.…”

“…It also allows asexuality-inducing alleles to be protected locally during harsh winters when extreme frost kills most obligate parthenogens, and to spread very quickly after winter. Moreover, repeated transitions to OP maintain a high level of genetic diversity in OP populations, allowing their persistence in the long term owing to higher evolvability (Simon et al, 2003;Sandrock and Vorburger, 2011). Despite the high potential of this contagious mechanism to generate obligate parthenogens, its actual incidence in the wild is largely unknown (Simon et al, 2003;Halkett et al, 2008;Sandrock and Vorburger, 2011).…”

“…Contagious asexuality has been reported in a wide range of arthropods (Delmotte et al, 2001;Lattorff et al, 2005;Paland et al, 2005;Halkett et al, 2008;Sandrock and Vorburger, 2011). When studied, inheritance of obligate asexuality has been found to be mono-or oligogenic in most cases.…”

“…In the rotifer Brachyonus calyciflorus, OP clones are homozygous for a recessive allele op, which renders them unable to respond to the chemical signals that usually induce sexual reproduction in this species (Scheuerl et al, 2011), whereas heterozygotes and homozygotes for the wild type are CP (Stelzer et al, 2010). In insects, all-female parthenogenesis (thelytoky) has been found to be inherited as a single-locus recessive trait in two hymenopterans, the Cape honeybee Apis mellifera capensis (Lattorff et al, 2005), and a solitary aphid endoparasitoid wasp, Lysiphlebus fabarum (Sandrock and Vorburger, 2011).…”

“…Contagious asexuality refers to a process whereby parthenogenesisinducing alleles are spread by rare males produced in parthenogenetic lineages and that convert sexual into asexual lineages (Simon et al, 2003;Sandrock and Vorburger, 2011). The effects of the meiosissuppressing loci are most often limited to the female genetic pathway and a variable quantity of males in addition to asexual females can be produced by OP clones.…”