Embryo production in a parthenogenetic snail (Potamopyrgus antipodarum) is negatively affected by the presence of other parthenogenetic females

Stimuli associated with copulatory behavior are often needed to maximize reproductive output in internally fertilized sexual taxa. Although non-pseudogamous parthenogenetic females have no need for sperm, parthenogens descended from sexual ancestors may still require copulatory stimuli to reach their full reproductive potential. Retention of physiological dependence on copulation in parthenogens could facilitate the maintenance of sexual reproduction in species where sexual and parthenogenetic individuals coexist if parthenogens do not receive enough copulatory stimuli to achieve maximal daughter production. A laboratory experiment was conducted to determine whether embryo production in parthenogenetic female snails (Potamopyrgus antipodarum) is dependent on male presence. Rather than male presence, this experiment showed that embryo production is affected by the number of coexisting parthenogens. Specifically, parthenogens housed with fewer other parthenogens produced significantly more embryos than parthenogens housed with a greater number of other parthenogens, regardless of male presence and total population size. This result indicates that copulatory dependence is not likely to contribute to the maintenance of sex in P. antipodarum. Instead, it demonstrates that females of P. antipodarum negatively affect each other’s reproduction, and suggests that females of P. antipodarum may exert a larger competitive influence than males of P. antipodarum. Moreover, this finding raises the possibility that highly parthenogenetic and consequently female-dense populations of P. antipodarum may experience decreased reproductive output when population size is large and resources are limiting. Additional key words: asexual, sexual, reproduction, males, New Zealand Species that use internal fertilization often depend on the stimuli delivered by courtship behavior and copulation to initiate and coordinate reproductive function (reviewed in Arnqvist & Nilsson 2000; Neiman 2004). Consequently, parthenogens recently derived from sexual progenitors may retain dependence on the physiological response elicited by copulatory stimuli, a direct result of the phylogenetic inertia that couples copulation with priming of reproductive physiology (e.g., Crews et al. 1986). Retention of copulatory dependence in parthenogens could help explain why non-pseudogamous parthenogens from a variety of taxa still copulate although they have no need of sperm. Copulatory dependence could even aid in the maintenance of sex if parthenogens are unable to realize the two-fold advantage of parthenogenetic reproduction in the absence of adequate copulation. This situation may arise if, for example, males discriminate against copulating with parthenogens or if parthenogens do not encounter males very often because parthenogens and sexuals use slightly different resources or habitats (Neiman 2004). Fertility and fecundity in many sexual snail species is linked to copulation frequency (e.g., Clelland et al. 2001). Research directed at determining the mechanisms underlying the connection between copulation and egg production in snails has shown that substances transmitted by semen stimulate the production of female reproductive hormones (e.g., Bride et al. 1991; Koene & Chase 1998). Populations of the ovoviviparous New Zealand freshwater prosobranch snail Potamopyrgus antipodarum GRAY 1843 vary widely in the relative frequency of sexual and parthenogenetic individuals (Lively 1987). Although parthenogenetic females Invertebrate Biology 125(1): 45–50. r 2006, The Authors Journal compilation r 2006, The American Microscopical Society, Inc. DOI: 10.1111/j.1744-7410.2006.00038.x Author for correspondence. E-mail: [email protected] have no need for sperm per se (Wallace 1992), they Q2 copulate readily when housed with males (Neiman & Lively 2005). Two lines of evidence suggest that parthenogenetic females of P. antipodarum may benefit from copulation. First, as noted above, many sexual snail species are dependent on copulatory stimuli to achieve full reproductive potential. Second, parthenogenetic lineages of P. antipodarum are often recently descended (oB20,000 years) from sexual ancestors (Neiman et al. 2005), which means that their reproductive physiology may have much in common with the ancestral, sexual condition. A preliminary experiment demonstrated that parthenogenetic females produced significantly more brooded embryos when coexisting with a relatively high number of males than when housed alone or with few males (M. Neiman, unpubl. data). This experiment, however, did not control for a potentially confounding factor, the number of coexisting parthenogens within each treatment population. Here, I used an experimental design that tested for both the effects of female parthenogen number and male presence on brooded embryo production in parthenogenetic females of P. antipodarum. I predicted that if the parthenogens benefit from access to males, they would produce more embryos when housed with males than when housed without males, regardless of the number of other parthenogenetic females. On the other hand, if embryo production in parthenogenetic females is negatively affected by other parthenogens, I predicted that parthenogenetic females housed in populations with fewer other parthenogens, regardless of male presence, would produce more embryos.