Living together but remaining apart: comparative phylogeography of Anolis poncensis and A. cooki, two lizards endemic to the aridlands of Puerto Rico

Comparative phylogeography is a powerful method for testing hypotheses of evolutionary diversification in ecological communities. Caribbean lizards of the genus Anolis are a species-rich group and a well-known example of adaptive radiation. In 1983, Ernest Williams suggested that species of Anolis that belong to the same ‘climate type’ (taxa that occur sympatrically in either xeric, mesic or very wet habitats) probably evolved under similar ecological conditions, and thus have experienced a parallel evolutionary history. This hypothesis implies that the phylogeographical patterns of such species can be expected to be concordant, a prediction that has not been tested. We conducted a comparative phylogeographical and population genetic study of Anolis poncensis and Anolis cooki, two sympatric lizards restricted to the aridlands of southwestern Puerto Rico, to determine whether there are similarities in the genetic architecture of the two anoles that may have resulted from a parallel response to the same historical events, or whether each taxon displays a distinct pattern of geographical distribution of intraspecific genealogical lineages. Our dataset consisted of approximately 2120 base pairs of the ND2 and cytochrome b genes from specimens from the known extant populations of the two species. The average haplotype diversity in A. poncensis (0.36) was considerably lower than that in A. cooki (0.62), whereas the average nucleotide diversity in A. cooki was ten times higher than that in A. poncensis. Both anoles showed pronounced phylogeographical structure, with no shared haplotypes among populations. The gene genealogy of A. poncensis recovered three strongly supported clades: the westernmost population, the easternmost deme and the three intermediate populations. In A. cooki, the populations from the western part of the species' range formed a well-supported group, to the exclusion of the eastern demes. Pairwise FST values revealed significant genetic differentiation among all conspecific populations of both anoles. Coalescent simulations indicated that A. poncensis could have evolved under a scenario of simple population fragmentation during the Pleistocene, but that A. cooki did not. The estimate of the effective population size of A. cooki was an order of magnitude larger than that of A. poncensis. Because time to the most recent common ancestor is dependent on effective population size, this tenfold difference implies that the time to the most recent common ancestor of A. cooki is much longer than that of A. poncensis, which indicates that A. cooki diversified earlier than A. poncensis. Collectively, these findings suggest that, although A. poncensis and A. cooki are syntopic throughout much of their current distribution, intraspecific diversification in the two species has not proceeded in parallel, which does not support the hypothesis that Anolis lizards that occupy the same climate-type region possess spatially and temporally congruent genetic architectures. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 617–634.