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Prior allozyme studies have indicated that populations of the asexual ostracode, Cypridopsis vidua (Müller), show extraordinary clonal diversity. Based on a joint examination of allozyme variation and sequence divergence at the mitochondrial cytochrome c oxidase I (COI) gene, the present analysis provides new insights concerning the origins of this variation. The results establish that populations of C. vidua in one recently deglaciated region of North America are not only allozymically diverse, but also include several divergent mitochondrial DNA (mtDNA) lineages. The extent of sequence divergence among these lineages is so large as to suggest their diversification over the past 7–8 million years. The patterning of genetic divergence among co-occurring clones makes it apparent that much of the mtDNA and allozyme diversity in local populations owes its origins to recurrent colonization events. However, in situ mutational diversification also appears to explain some variation. The mechanisms enabling the sustained coexistence of such a large array of closely allied genotypes remain unclear, but there is an apparent difference in equilibrium diversity between benthic and planktonic asexual organisms.