Reconstructing the evolutionary history of the radiation of the land snail genus Xerocrassa on Crete based on mitochondrial sequences and AFLP markers

Abstract

BackgroundA non-adaptive radiation triggered by sexual selection resulted in ten endemic land snail species of the genus Xerocrassa on Crete. Only five of these species and a more widespread species are monophyletic in a mitochondrial gene tree. The reconstruction of the evolutionary history of such closely related species can be complicated by incomplete lineage sorting, introgression or inadequate taxonomy. To distinguish between the reasons for the nonmonophyly of several species in the mitochondrial gene tree we analysed nuclear AFLP markers.ResultsWhereas six of the eleven morphologically delimited Xerocrassa species from Crete are monophyletic in the mitochondrial gene tree, nine of these species are monophyletic in the tree based on AFLP markers. Only two morphologically delimited species could not be distinguished with the multilocus data and might have diverged very recently or might represent extreme forms of a single species. The nonmonophyly of X. rhithymna with respect to X. kydonia is probably the result of incomplete lineage sorting, because there is no evidence for admixture in the AFLP data and the mitochondrial haplotype groups of these species coalesce deeply. The same is true for the main haplotype groups of X. mesostena. The nonmonophyly of X. franciscoi might be the result of mitochondrial introgression, because the coalescences of the haplotypes of this species with some X. mesostena haplotypes are shallow and there is admixture with neighbouring X. mesostena.ConclusionThe most likely causes for the nonmonophyly of species in the mitochondrial gene tree of the Xerocrassa radiation on Crete could be inferred using AFLP data by a combination of several criteria, namely the depth of the coalescences in the gene tree, the geographical distribution of shared genetic markers, and concordance with results of admixture analyses of nuclear multilocus markers. The strongly subdivided population structure increases the effective population size of land snail species and, thus, the likelihood of a long persistence of ancestral polymorphisms. Our study suggests that ancestral polymorphisms are a frequent cause for nonmonophyly of species with a strongly subdivided population structure in gene trees.

High unexpected genetic diversity of a narrow endemic terrestrial mollusc

“…Moreover, Roucoux et al (2001) shows low but fluctuating tree pollen through the LGM, along with abundant grass and some herb pollen, indicating likely widespread suitability of the grassy habitats for Candidula species throughout the LGM. Similar events have already been detected for another land snail species (Harl et al, 2014; Sauer & Hausdorf, 2010; Shimizu & Ueshima, 2000). After the LGM, environmental conditions during deglaciation were such that promoted northward dispersal of land snails and the establishment of populations in locations of suitable isothermality and precipitation like Vale da Couda.…”

Animal Mitochondria, Positive Selection and Cyto-Nuclear Coevolution: Insights from Pulmonates

“…Furthermore, the potential importance of localized adaptations was demonstrated in Cepaea mtDNA [6]. Finally, in some studies it was shown that demographic factors (hypothesis iv), such as highly structured populations and limited capacity for active dispersal, are important both in conservation of mtDNA polymorphisms at a small-scale [39], [40] and in the long-term and large-scale structuring of populations [28], [30], [37], [41]. Moreover, it has been proposed [23], [40] that even in the face of adequate gene flow within demographically structured pulmonate populations, natural selection could favor specific associations between mtDNA and nuclear genes (associations developed whilst populations are separated) and that would radically slow the homogenization process of the mtDNA lineages, thus allowing several divergent mtDNA haplotypes to be maintained within a single pulmonate population.…”

Positive selection on panpulmonate mitogenomes provide new clues on adaptations to terrestrial life

“…However, a recent study has shown that mitochondrial DNA undergoes substantial amounts of adaptive evolution, especially in mollusks [41]. The particular demographic pattern of land snails that produces highly structured populations (hypothesis 4), i.e., “islands” of isolated demes, affects the probability of reciprocal monophyly of two samples and the chance that a gene tree matches the species tree [42], and explained the persistence of ancestral polymorphisms and the extreme divergence in Achatinella [43], Systrophia [44], and Xerocrassa [45]. In addition, in the case of Hygrophila, some studies found high divergence rates in Physella [46], and Radix [47], although no clear hypothesis has been proposed to explain this pattern.…”