High levels of population subdivision in a morphologically conserved Mediterranean toad (Alytes cisternasii) result from recent, multiple refugia: evidence from mtDNA, microsatellites and nuclear genealogies

Abstract

Pleistocene glaciations often resulted in differentiation of taxa in southern European peninsulas, producing the high levels of endemism characteristic of these regions (e.g. the Iberian Peninsula). Despite their small ranges, endemic species often exhibit high levels of intraspecific differentiation as a result of a complex evolutionary history dominated by successive cycles of fragmentation, expansion and subsequent admixture of populations. Most evidence so far has come from the study of species with an Atlantic distribution in northwestern Iberia, and taxa restricted to Mediterranean-type habitats remain poorly studied. The Iberian Midwife toad (Alytes cisternasii) is a morphologically conserved species endemic to southwestern and central Iberia and a typical inhabitant of Mediterranean habitats. Applying highly variable genetic markers from both mitochondrial and nuclear genomes to samples collected across the species' range, we found evidence of high population subdivision within A. cisternasii. Mitochondrial haplotypes and microsatellites show geographically concordant patterns of genetic diversity, suggesting population fragmentation into several refugia during Pleistocene glaciations followed by subsequent events of geographical and demographic expansions with secondary contact. In addition, the absence of variation at the nuclear beta-fibint7 and Ppp3caint4 gene fragments suggests that populations of A. cisternasii have been recurrently affected by episodes of extinction and recolonization, and that documented patterns of population subdivision are the outcome of recent and multiple refugia. We discuss the evolutionary history of the species with particular interest in the increasing relevance of Mediterranean refugia for the survival of genetically differentiated populations during the Pleistocene glaciations as revealed by studies in co-distributed taxa.

The Confounding Effects of Population Structure, Genetic Diversity and the Sampling Scheme on the Detection and Quantification of Population Size Changes

“…While this effect has been known from a theoretical point of view (Wakeley 1999;Beaumont 2003bBeaumont , 2004; Nielsen and Beaumont 2009), it had not been quantified for data sets simulated with different levels of gene flow and diversity. We found that the effect was limited when genetic differentiation was low but that it could be observed for values of F ST that are typically reported in the literature (e.g., Gonc xalves et al 2009;Holsinger and Weir 2009;Quéméré et al 2009;Rosel et al 2009). We found that the effect was particularly strong with high values of u, which either correspond to highly variable markers or to species with large effective population sizes.…”

Salamandra salamandra (Amphibia: Caudata: Salamandridae) in Portugal: not all black and yellow

“…Yet, besides these impressive events during the Miocene more recent climatic changes also imprinted on the present-day distribution of genetic divergence. It seems clear that Pleistocene ice ages were probably responsible for the fragmentation of species and lineage splitting (Gonçalves et al 2009;Recuero and García-París 2011). As the temperatures declined throughout the last ice ages, most of Europe's common deciduous forests were confined to some secluded locations in the Mediterranean Peninsulas with large regions being turned to steppe-tundra land (Deffontaine et al 2005).…”

“…An exhaustive list can be found in Gómez and Lunt (2007, and references therein). Recently, further evidence supporting this theory included the rotifer Brachionus plicatilis (Campillo et al 2011), the grasshopper Chorthippus parallelus (Bella et al 2007), the Mediterranean toad (Alytes cisternasii) (Gonçalves et al 2009), the red-legged partridge (Alectoris rufa) (Ferrero et al 2011), the field vole, Microtus agrestis (Jaarola and Searle 2003), and the southern water vole (Arvicola sapidus) (Centeno-Cuadros et al 2009). …”

Extinction Resilience of Island Species: An Amphibian Case and a Predictive Model

“…This may be the case for a majority of non-marine species living on continents, whose distributions are often ecologically and geographically limited. Even the two alytines with larger ranges have a deep phylogeographic structure [44,133], warranting an urgent (re)evaluation of the status of their constituent subunits (whether recognized as subspecies or not).…”

“…In addition, the model includes an explicit identification of scale. This allows for considering large areas, such as whole biotic regions (as suggested by [9,167]), as well as smaller subdivisions, leading to diversification in ecological islands within islands [2,133,[168][169][170].…”