Abstract

Gynogenetic organisms are asexual females of one species that require sperm from males of another species to initiate reproduction (but except in rare instances of ‘paternal leakage’, those sperm do not contribute to the genetic make-up of the gynogens’ offspring). Gynogenetic organisms seem to combine disadvantages of both sexual and asexual reproductive strategies (e.g., mating costs, reduced genetic diversity). We borrowed logic from the Red Queen Hypothesis (RQH) to help explain the persistence of gynogenetic species in nature, which is a paradox. The RQH is the most oft-cited explanation for the maintenance of sex. It states that evolving enemies generate a constantly changing environment, which provides the conditions that make sex advantageous. Under this scenario, asexual organisms cannot evolve fast enough to ‘keep up’ with co-evolving parasites and disease causing organisms, and ultimately show reduced fitness compared to sexual individuals. The RQH tends to view asexuality generally, ignoring important nuance in nature like gynogenetic species in mixed assemblages with closely related sexual species. We outline tests of the argument that sperm dependency prevents asexual gynogens from outcompeting sexuals in mixed species assemblages and that this further allows gynogens to escape evolving enemies.

Highlights

  • One key question that arises is why all the gynogenetic females do not just reproduce entirely asexually through parthenogenesis, i.e., evolve to forgo egg development that is dependent on attracting a heterospecific male? This question might be important to informing ideas about the evolution of (a)sex because it brings to the forefront a troubling situation: the gynogenetic mode of reproduction apparently combines disadvantages of both sexual and asexual strategies (Beukeboom and Vrijenhoek 1998; Schlupp 2005; Lamatsch and Stöck 2009)

  • We argue that sperm-dependency prevents the asexual species from outcompeting the sexual species, as previously suggested by Beukeboom and Vrijenhoek (1998), and that it is this obligate formation of mixed-species assemblages that prevents population crashes of asexuals by slowing down or averting parasite adaptation

  • Known commonly as the problem of recombination, states that sex can be detrimental to organisms that are adapted to their environment because it can break up beneficial gene associations (Nei 1967)

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Summary

The problem

Gynogenesis is a form of ‘sexual parasitism’ wherein one sex (the female) attracts a heterospecific mate for the purposes of mating, but not for reproduction (Hubbs 1964; Lehtonen et al 2013). This two-fold cost is the upper limit of the theoretical difference in reproduction for completely outbreeding individuals (Bell 1982) and is only expected under the unrealistic condition of “all else being equal” (i.e. niche, fitness, reproductive output) between the sexual and asexual lineages Another issue with sexuality, known commonly as the problem of recombination, states that sex can be detrimental to organisms that are adapted to their environment because it can break up beneficial gene associations (Nei 1967). Even if they do not produce males, gynogenetic females spend time and energy in mating, with all the potential risks that mating entails (e.g. aggression, predation risk, disease transmission, Daly 1978) Gynogens pay these costs or entail these risks while experiencing the costs of asexuality such as the accumulation of deleterious mutations within the genome or lower genetic diversity than sexuals, which is thought to compromise the asexual’s ability to evolve counteradaptations such as resistance to parasites and disease agents. This interpretation opens the door to a novel insight regarding gynogenetic individuals: could their presence in two-species assemblages, where one species is sexual, provide gynogens with some of the benefits of pure sexual groups in terms of escape from evolving enemies? Testing this idea requires more than comparing levels of parasiteism experienced concurrently by asexual and sexual individuals

Experimental approaches and key insights
Concluding remarks

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