Phylogeography of an Italian endemic salamander (genus Salamandrina): glacial refugia, postglacial expansions, and secondary contact

Abstract

The Italian endemic genus Salamandrina has been historically regarded as monotypic but, recently, studies based on both mitochondrial and nuclear markers have indicated the existence of two distinct species of spectacled salamanders: Salamandrina perspicillata, in central and northern Italy, and Salamandrina terdigitata, in southern Italy. We analyzed nucleotide variation at mitochondrial and nuclear genes [cytochrome b, 12S and 16S rRNA, recombination activating gene (RAG 1)] in 223 individuals from 56 locations, aiming to investigate their genetic structure and recent evolutionary histories. Phylogenetic and phylogeographical analyses revealed the existence of three and two genetically distinct groups of populations in northern and southern salamander, respectively. Historical demographic analyses led to the inference of range expansion for both species in the late Pleistocene. During the last glacial stage, each salamander survived in a single refugium, namely the southern in Calabria and the northern in central Italy. At the end of this period, both lineages expanded northward and established secondary contact. Spatial distribution of RAG 1 haplotype variation revealed two differentiated population groups corresponding to the major mitochondrial (mt)DNA clades. Nuclear pattern of introgressive hybridization was more extensive than the highly limited introgression of mtDNA markers. From a conservation standpoint, southern Latium and Calabria proved to be the major genetic diversity reservoirs, thus deserving particular conservation effort

Extensive unidirectional introgression between two salamander lineages of ancient divergence and its evolutionary implications

“…This pattern supports the idea that the S. terdigitata alleles have become integral to the gene pool of southern S. perspicillata populations, and it also suggests that these populations could have achieved some degree of evolutionary ‘independence' from conspecific populations to the north. Further support for this interpretation comes from the lack of HW and linkage disequilibria, as well as from previous findings35 that have indicated that the southern S. perspicillata populations belong to a distinct albeit weakly differentiated mtDNA haplogroup.…”

“…Once regarded as a single species ( S. terdigitata ), they were recently identified as two deeply divergent species based on both nuclear and mitochondrial genetic data313233 and their divergence time was estimated to largely predate the onset of the Pleistocene epoch3233 (but see also34). Recently, a small area was found where both the highly divergent mitochondrial DNA (mtDNA) lineages come into sympatry35, and a preliminary analysis of the hybridization was carried out (based on one sampling location, one mtDNA marker, and one diagnostic and one uninformative nuclear markers)36.…”

Integrative Phylogeography of Calotriton Newts (Amphibia, Salamandridae), with Special Remarks on the Conservation of the Endangered Montseny Brook Newt (Calotriton arnoldi)

“…Direct sequencing of PCR products for RAG-1 revealed a single nucleotide site at which individuals were heterozygous. Diploid amplified sequences were represented by two alleles [16], [31].…”

“…Amphibians are good models to explore the influence of historical aspects on the genetic structure at different geographic scales ([13], [14], [15], [16], among others). This can be explained by the retention of strong phylogeographic signal due to the low dispersal capacity [17], and sensibility to small environmental changes [6].…”

Late Pleistocene fossils and the future distribution of Rana temporaria (Amphibia, Anura) along the Apennine Peninsula (Italy)

“…In recent years, phylogeographic studies have used genetic and molecular methods for investigating the history of the distribution of various taxa of amphibians (among others: Duellman 1999; Riberon et al 2001;Zeisset and Beebee 2001;Bonnet and Chippindale 2004;Vences et al 2004;Alexandrino et al 2007;Crottini et al 2007;Recuero et al 2007;Vences and Wake 2007;Stöck et al 2008;Shepard and Burbrink 2009;Mattoccia et al 2011;Chiari et al 2012). As far as Europe is concerned, Rana temporaria has been the subject of several papers (Veith et al 2003;Palo et al 2004;Gómez and Lunt 2006;Zeisset and Beebee 2008;Teacher et al 2009;Stefani et al 2012), probably because its current broad range (Gasc et al 1997;Kuzmin 1999;Sillero et al 2014) and the fact that it is adapted to relatively cold environments render this species a good model for evaluating the range changes that occurred during and after the Pleistocene coolings.…”