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Keywords:

  • clonal diversity;
  • coevolution;
  • frozen-niche variation;
  • maintenance of sex;
  • parthenogenesis;
  • Potamopyrgus antipodarum;
  • Red Queen hypothesis;
  • trematodes

Sexual reproduction within natural populations of most plants and animals continues to remain an enigma in evolutionary biology. That the enigma persists is not for lack of testable hypotheses but rather because of the lack of suitable study systems in which sexual and asexual females coexist. Here we review our studies on one such organism, the freshwater snail Potamopyrgus antipodarum (Gray). We also present new data that bear on hypotheses for the maintenance of sex and its relationship to clonal diversity. We have found that sexual populations of the snail are composed of diploid females and males, while clonal populations are composed of a high diversity of triploid apomictic females. Sexual and asexual individuals coexist in stable frequencies in many ‘mixed’ populations; genetic data indicate that clones from these mixed populations originated from the local population of sexual individuals without interspecific hybridization. Field data show that clonal and sexual snails have completely overlapping life histories, but individual clonal genotypes are less variable than individuals from the sympatric sexual population. Field data also show segregation of clones among depth-specific habitat zones within a lake, but clonal diversity remains high even within habitats. A new laboratory experiment revealed extensive clonal variation in reproductive rate, a result which suggests that clonal diversity would be low in nature without some form of frequency-dependent selection. New results from a long-term field study of a natural, asexual population reveal that clonal diversity remained nearly constant over a 10-year period. Nonetheless, clonal turnover occurs, and it occurs in a manner that is consistent with parasite-mediated, frequency-dependent selection. Reciprocal cross-infection experiments have further shown that parasites are more infective to sympatric host snails than to allopatric snails, and that they are also more infective to common clones than rare clones within asexual host populations. Hence we suggest that sexual reproduction in these snails may be maintained, at least in part, by locally adapted parasites. Parasite-mediated selection possibly also contributes to the maintenance of local clonal diversity within habitats, while clonal selection may be responsible for the distribution of clones among habitats. © 2003 The Linnean Society of London. Biological Journal of the Linnean Society 2003, 79, 165–181.