Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae:Gyrinophilus) inferred from gene genealogies

Abstract

Cave organisms occupy a special place in evolutionary biology because convergent morphologies of many species demonstrate repeatability in evolution even as they obscure phylogenetic relationships. The origin of specialized cave-dwelling species also raises the issue of the relative importance of isolation vs. natural selection in speciation. Two alternative hypotheses describe the origin of subterranean species. The 'climate-relict' model proposes allopatric speciation after populations of cold-adapted species become stranded in caves due to climate change. The 'adaptive-shift' model proposes parapatric speciation driven by divergent selection between subterranean and surface habitats. Our study of the Tennessee cave salamander complex shows that the three nominal forms (Gyrinophilus palleucus palleucus, G. p. necturoides, and G. gulolineatus) arose recently and are genealogically nested within the epigean (surface-dwelling) species, G. porphyriticus. Short branch lengths and discordant gene trees were consistent with a complex history involving gene flow between diverging forms. Results of coalescent-based analysis of the distribution of haplotypes among groups reject the allopatric speciation model and support continuous or recurrent genetic exchange during divergence. These results strongly favour the hypothesis that Tennessee cave salamanders originated from spring salamanders via divergence with gene flow.

Molecular phylogeography of the troglobiotic millipede Tetracion Hoffman, 1956 (Diplopoda, Callipodida, Abacionidae)

“…In the three caves with two haplotypes, the haplotypes in those caves differed by a single nucleotide, which is consistent with in situ evolution through mutation, as opposed to migration from a genetically distinct population. These patterns are similar to those observed in other terrestrial troglobionts from the Cumberland Plateau (Snowman et al 2010;Dixon and Zigler 2011), but contrast with those of the cave crayfish and cave salamanders, where haplotypes were commonly shared among populations and across large distances (Buhay and Crandall 2005;Buhay et al 2007;Niemiller et al 2008). Aquatic subterranean habitats may be better connected than terrestrial subterranean habitats, or the longer lifespans of crayfish and salamanders may permit greater levels of migration and gene flow between populations.…”

“…For example, Snowman et al (2010) found high genetic variation (up to 4%) between populations of the cave spider Nesticus barri Gertsch, 1984, andDixon andZigler (2011) found high genetic variation in several cave species (including a fly, a beetle, and an isopod) on a small scale. High levels of genetic variation were also observed in the cave crayfish genera Orconectes Cope, 1872 and Cambarus Erichson, 1846 (Buhay and Crandall 2005;Buhay et al 2007), and in cave salamanders of the genus Gyrinophilus Cope, 1869 (Niemiller et al 2008). Although the differences between Tetracion populations were not great, populations were generally fixed for a single haplotype.…”

Post-glacial habitat release and incipient speciation in the genus Delphinus

“…Two putative hybrids were detected and both IMa and BayesAss suggested biased gene flow from the sbENP to the lbENP form at nonzero levels. This is not necessarily inconsistent with incipient speciation, as hybrids between recognized species are common for cetaceans (see Crossman et al, 2016), and incipient speciation is possible even in the face of recurrent or continuous gene flow (Hey, 2006;Niemiller et al, 2008), for example, among three divergent forms of Tennessee cave salamander, Gyrinophilus palleucus (Niemiller et al, 2008). Incomplete lineage sorting could explain some missassigned individuals based on a given marker, but the congruence of phenotype and different marker types for the same individuals makes this interpretation less likely.…”

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

“…The inherently parapatric and allopatric nature of the epigean-subterranean nexus (Niemiller et al, 2008) is indisputably a key speciation mechanism in cave environments; however, in situ speciation (that is, speciation within cavernicolous habitats) is also predicted to have had an impact . Speciation from an obligate subterranean-adapted ancestor within the cave environment has rarely and only recently been explored (Caccone, 1985;Buhay and Crandall, 2005;Guzik et al, 2009).…”

“…The shift from an epigean existence to cave life and subsequent isolation can typically lead to dramatic speciation events and morphological adaptation (Niemiller et al, 2008). This process of speciation by transition from surface to subterranean environments is suggested as the main mechanism for the evolution of subterranean species, although there is some debate about whether it requires extinction of the surface ancestral species (climate relict hypothesis; for example Peck and Finston (1993)) or can proceed in the presence of gene flow between the surface and subterranean populations (adaptive shift hypothesis; for example Desutter-Grandcolas and Grandcolas (1996)).…”