The Effect of Variable Frequency of Sexual Reproduction on the Genetic Structure of Natural Populations of a Cyclical Parthenogen

Abstract

Cyclical parthenogens are a valuable system in which to empirically test theoretical predictions as to the genetic consequences of sexual reproduction in natural populations, particularly if the frequency of sexual relative to asexual reproduction can be quantified. In this study, we used a series of lake populations of the cyclical parthenogen, Daphnia pulicaria, that vary consistently in their investment in sexual reproduction, to address the questions of whether the ecological variation in investment in sex is detectable at the genetic level, and if so, whether the genetic patterns seen are consistent with theoretical predictions. We show that there is variation in the genetic structure of these populations in a manner consistent with their investment in sexual reproduction. Populations engaging in a high frequency of sex were in Hardy–Weinberg and gametic phase equilibrium, and showed little genotypic differentiation across sampled years. In contrast, populations with a lower frequency of sex deviated widely from equilibrium, had reduced multilocus clonal diversity, and showed significant temporal genotypic deviation.

Effects of complex life cycles on genetic diversity: cyclical parthenogenesis

“…Our results indicate that the distribution of gametic phase disequilibrium, alone or in combination with the F IS distribution, represents an interesting tool with which to infer the level of clonality in a population. Genetic diversity of cyclical parthenogens R Rouger et al Sexuality in CA does not reset genetic diversity towards predictions made under full-sexuality conditions As anticipated in previous studies (Lynch and Deng, 1994;Pfrender and Lynch, 2000;De Meester et al, 2006;Allen and Lynch, 2012), our model confirms that a single generation of sexual reproduction following a low number of clonal generations rearranges genetic diversity at a single locus towards predictions made under a condition of full sexuality (CP after sex). Notably, this is not true in particular cases in which genetic drift dominates (Nμo1, for example, in very small populations) and the number of clonal generations preceding the sexual event is large enough to increase the probability of obtaining a high frequency of heterozygotes in the population.…”

“…Because of the absence of an explicit model describing the effect of clonality on the distribution of neutral genetic diversity in CP, many studies have relied on models describing predictions of genetic diversity under APC conditions in the discussion of their CP data (see, for example, Halkett et al, 2005a;Vorburger, 2006;Kanbe and Akimoto, 2009;Allen and Lynch, 2012). Specially designed to fit the CP lifecycle, our model refines these predictions and is particularly suited to testing precise hypotheses regarding genetic diversity in cyclical parthenogens.…”

“…To date, many studies have linked summary statistics such as F IS or linkage disequilibrium to the relative importance of sexual vs clonal reproduction within species displaying CP (Allen and Lynch, 2012;Delmotte et al, 2002;Halkett et al, 2005a;Ivens et al, 2012;Kanbe and Akimoto, 2009;Papura et al, 2003;Vorburger, 2006;Vorwerk and Forneck, 2006). Based on previous models and observations, a negative F IS and strong linkage disequilibrium have been interpreted as signatures of strong clonality.…”

“…Numerous field observations of partially clonal organisms have shown strong deviations from the predictions of intrapopulation genetic diversity resulting from strictly sexual models (Papura et al, 2003;Stoeckel et al, 2006;Kanbe and Akimoto, 2009;Allen and Lynch, 2012). The main observed effects of clonal reproduction are (1) decreased genotypic diversity within populations, (2) an excess of heterozygotes resulting in strongly negative F IS values and (3) an increased gametic phase disequilibrium due to the absence of recombination between loci (Halkett et al, 2005b).…”

The Exact Distributions of FIS under Partial Asexuality in Small Finite Populations with Mutation

“…Conversely, to explain why we can still observe populations that steadily reproduce through partial asexuality, we may suppose that the balance between the genetic benefits of mixis and the costs of sex should vary with different rates of asexuality [12]. Empirical and field studies observe that partially asexual species show lower negative F IS values at most loci when other direct evidences of asexuality argue for intermediate rates rather than full sexual species [17], [28]. This feature is thus commonly used to pragmatically detect asexual events in populations assumed to be sexual [16].…”