Exploring the relationship between tychoparthenogenesis and inbreeding depression in the Desert Locust, Schistocerca gregaria

Abstract

Tychoparthenogenesis, a form of asexual reproduction in which a small proportion of unfertilized eggs can hatch spontaneously, could be an intermediate evolutionary link in the transition from sexual to parthenogenetic reproduction. The lower fitness of tychoparthenogenetic offspring could be due to either developmental constraints or to inbreeding depression in more homozygous individuals. We tested the hypothesis that in populations where inbreeding depression has been purged, tychoparthenogenesis may be less costly. To assess this hypothesis, we compared the impact of inbreeding and parthenogenetic treatments on eight life‐history traits (five measuring inbreeding depression and three measuring inbreeding avoidance) in four laboratory populations of the desert locust, Schistocerca gregaria, with contrasted demographic histories. Overall, we found no clear relationship between the population history (illustrated by the levels of genetic diversity or inbreeding) and inbreeding depression, or between inbreeding depression and parthenogenetic capacity. First, there was a general lack of inbreeding depression in every population, except in two populations for two traits. This pattern could not be explained by the purging of inbreeding load in the studied populations. Second, we observed large differences between populations in their capacity to reproduce through tychoparthenogenesis. Only the oldest laboratory population successfully produced parthenogenetic offspring. However, the level of inbreeding depression did not explain the differences in parthenogenetic success between all studied populations. Differences in development constraints may arise driven by random and selective processes between populations.

First case of parthenogenesis in ladybirds (Coleoptera: Coccinellidae) suggests new mechanisms for the evolution of asexual reproduction

“…A more widespread phenomenon is tychoparthenogenesis, an accidental spontaneous hatch of unfertilized eggs that develop into females (Bullini, —“spontaneous theory”). In this accidental parthenogenesis, the proportion of unfertilized eggs and their hatching rates are very low, but could be magnified by mate limitation (the “mate scarcity hypothesis,” Rhainds, ; Schwander, Vuilleumier, Dubman, & Crespi, ) in small effective populations or after bottleneck events (Little, Chapuis, Blondin, Chapuis, & Jourdan‐Pineau, ). This could explain the well‐known relationship between parthenogenesis and certain habitats such as islands (“geographical parthenogenesis” Vandel, ).…”

Parthenogenesis and developmental constraints

“…Here ploidy is restored at the end of meiosis by the fusion of the generally large oocyte with the closest polar body (second, in the row of four meiotic products). These ploidy restoration mechanisms that do not, or only marginally, interfere with meiosis are, thus, characterized by a loss of heterozygosity and in sporadic parthenogenesis by extremely low viability and fertility rates (Cassar et al, 1998;Corley & Moore, 1999;Eisman & Kaufman, 2007;Little, Chapuis, Blondin, Chapuis, & Jourdan-Pineau, 2017;Murdy & Carson, 1959;Olsen, 1974;Riparbelli & Callaini, 2003;Sprackling, 1960;White, 1973). Heterozygosity is lost, except for some caused by crossing over.…”

“…Sporadic parthenogenesis has been hypothesized to represent another route to obligate parthenogenesis, via mutations for better ploidy restoration, more efficient centrosome assembly, and retention of heterozygosity (e.g., Bell, 1982;Lenormand, Engelstädter, Johnston, Wijnker, & Haag, 2016;Seiler, 1961;White, 1973). Reproductive success in sporadic parthenogenesis is generally extremely low, with hardly any offspring surviving as fertile adults (e.g., Corley & Moore, 1999;Little et al, 2017;Murdy & Carson, 1959;Olsen, 1974;Sprackling, 1960;White, 1973). Reproductive success in sporadic parthenogenesis is generally extremely low, with hardly any offspring surviving as fertile adults (e.g., Corley & Moore, 1999;Little et al, 2017;Murdy & Carson, 1959;Olsen, 1974;Sprackling, 1960;White, 1973).…”

“…Terminal fusion occurs for instance in sporadic parthenogenesis in vertebrates and also in Wolbachiainduced parthenogenesis in hymenopterans (Booth et al, 2014;Lampert, 2008;Werren, Baldo, & Clark, 2008). These ploidy restoration mechanisms that do not, or only marginally, interfere with meiosis are, thus, characterized by a loss of heterozygosity and in sporadic parthenogenesis by extremely low viability and fertility rates (Cassar et al, 1998;Corley & Moore, 1999;Eisman & Kaufman, 2007;Little, Chapuis, Blondin, Chapuis, & Jourdan-Pineau, 2017;Murdy & Carson, 1959;Olsen, 1974;Riparbelli & Callaini, 2003;Sprackling, 1960;White, 1973). Furthermore, the homozygosity enforcing mechanisms imply that in species with a ZZ, ZW sex determination system, where the females are the heterogamous sex (ZW), only males (ZZ) can be produced parthenogenetically and no females, that is, a genetic constraint against parthenogenesis (e.g., in hammerhead sharks, several snakes, Komodo dragons, chickens, and turkeys; Booth et al, 2014;Cassar et al, 1998;Chapman et al, 2007;Watts et al, 2006).…”

“…However, it is uncertain whether the drastic changes of meiosis associated with obligate parthenogenesis can be achieved by gradual evolution. Reproductive success in sporadic parthenogenesis is generally extremely low, with hardly any offspring surviving as fertile adults (e.g., Corley & Moore, 1999;Little et al, 2017;Murdy & Carson, 1959;Olsen, 1974;Sprackling, 1960;White, 1973). For instance, in wild strains of D. parthenogenetica 1.5% of eggs laid by unfertilized females develop into viable adults (Stalker, 1954) and only three viable adults were produced from 50,000 unfertilized eggs of D. mercatorum (Kramer, Templeton, & Miller, 2002), compared to 50% in the obligate parthenogenetic D. mangabeirai (60% of eggs hatches of which 80% survive as adults; Carson, Wheeler, & Heed, 1957;Markow, 2013;Murdy & Carson, 1959;Sprackling, 1960;White, 1973).…”