Extreme divergence of mitochondrial DNA within species of pulmonate land snails

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Abstract
Mitochondrial DNA, inherited predominantly through the female line, has been exceptionally useful for reconstructing phylogenies (Avise, in Molecular markers, natural history and evolution. New York: Chapman and Hall (1994)). However, at the lowest taxonomic level, if there are polymorphisms within species the lineages of mitochondria need not correspond to the lineages of the species (Avise, in Phil. Trans. R. Soc. Lond. B 312, 325-342 (1986)). We find that a classic organism in ecological genetics, Cepaea nemoralis, has the most extreme intraspecific variation and polymorphism so far recorded, and that at least one other pulmonate land mollusc also has very high levels of mitochondrial diversity. Making the simplest assumptions, the data suggest times of divergence as long ago as 20 million years between haplotypes now coexisting within a single population. There are four overlapping explanations of the diversity: (i) that mitochondrial evolution in pulmonates is exceptionally fast; (ii) that the morphs have differentiated in isolated `refuges' and then come together; (iii) that natural selection has acted to preserve the variation; and (iv) that the population structure of pulmonates favours the persistence of ancient haplotypes. We argue for the importance of the last explanation.