Extreme mtDNA divergences in a terrestrial slug (Gastropoda, Pulmonata, Arionidae): accelerated evolution, allopatric divergence and secondary contact

Abstract

Extremely high levels of intraspecific mtDNA differences in pulmonate gastropods have been reported repeatedly and several hypotheses to explain them have been postulated. We studied the phylogeny and phylogeography of 51 populations (n = 843) of the highly polymorphic terrestrial slug Arion subfuscus (Draparnaud, 1805) across its native distribution range in Western Europe. By combining the analysis of single stranded conformation polymorphisms (SSCP) and nucleotide sequencing, we obtained individual sequence data for a fragment of the mitochondrial 16S rDNA and a fragment of the nuclear ITS1. Additionally, five polymorphic allozyme loci were scored. Based on the 16S rDNA phylogeny, five monophyletic haplotype groups with sequence divergences of 9–21% were found. Despite this deep mitochondrial divergence, the haplotype groups were not monophyletic for the nuclear ITS1 fragment and haplotype group‐specific allozyme alleles were not found. Although there is evidence for an accelerated mtDNA clock, the divergence among the haplotype groups is older than the Pleistocene and their current allopatric ranges probably reflect allopatric divergence and glacial survival in separate refugia from which different post‐glacial colonization routes were established. A range‐overlap of two mtDNA groups (S1 and S2, 21% sequence divergence) stretched from Central France and Belgium up to the North of the British Isles. The nuclear data suggest that this secondary contact resulted in hybridization between the allopatrically diverged groups. Therefore, it seems that, at least for two of the groups, the deep mtDNA divergence was only partially accompanied by the formation of reproductive isolation.

Evidence for population fragmentation within a subterranean aquatic habitat in the Western Australian desert

“…Either fragmentation has not persisted long enough to provide sufficient time to achieve reciprocal monophyly or, as suggested earlier, there has been longterm fragmentation of populations with recent secondary contact (Taberlet et al, 1998;Hewitt, 2000). This latter hypothesis of post-isolation colonisation, in which a population is fragmented by a geographic barrier (vicariance) and subsequently rejoined, has been demonstrated in many epigean species (Zamudio and Savage, 2003;Phillips et al, 2004;Hoskin et al, 2005;Pinceel et al, 2005). Such a scenario has also been documented from a broad range of cavernicolous habitats and is a plausible hypothesis for the taxa within the LDC aquifer system (Cobolli Sbordoni et al, 1990;Crouau-Roy and Bakalowicz, 1993;Buhay and Crandall, 2005;Hunter et al, 2008).…”

Congruence and Conflict Between Molecular and Reproductive Characters When Assessing Biological Diversity in the Western Fanshell Cyprogenia aberti (Bivalvia, Unionidae)1

“…Fluctuations in climate, water levels, and reorganization of drainage patterns within the Highlands could isolate and displace populations of aquatic fauna, while creating opportunity for recolonization and range expansion at a later time. The post-glacial secondary contact hypothesis has been used to explain similar genetic patterns in other molluscan taxa, including slugs (Pinceel et al, 2005) and terrestrial gastropods (Davidson, 2000).…”

The ovotestis: an underdeveloped organ of evolution

“…It has been noted frequently that molluscs may have exceptionally high rates of molecular evolution, especially of mitochondrial DNA, (54)(55)(56)(57)(58)(59) but probably also at some nuclear loci. (60)(61)(62)(63)(64) Within species, mitochondrial divergence in many land snails is of the order of 5 to 30%, depending upon the species and gene fragment used.…”