The legacy of ice ages in mountain species: post-glacial colonization of mountain tops rather than current range fragmentation determines mitochondrial genetic diversity in an endemic Pyrenean rock lizard

Abstract

Aim The genetic impact of Quaternary climatic fluctuations on mountain endemic species has rarely been investigated. The Pyrenean rock lizard (Iberolacerta bonnali) is restricted to alpine habitats in the Pyrenees where it exhibits a highly fragmented distribution between massifs and between habitats within massifs. Using mitochondrial DNA markers, we set out: (1) to test whether several evolutionary units exist within the species; (2) to understand how the species persisted through the Last Glacial Maximum and whether the current range fragmentation originates from distribution shifts after the Last Glacial Maximum or from more ancient events; and (3) to investigate whether current mitochondrial diversity reflects past population history or current habitat fragmentation. Location The Pyrenees in south-western France and northern Spain. Methods We used variation in the hypervariable left domain of the mitochondrial control region of 146 lizards collected in 15 localities, supplemented by cytochrome b sequences downloaded from GenBank to cover most of the species’ distribution range. Measures of population genetic diversity were contrasted with population isolation inferred from topography. Classical (F-statistics) and coalescence-based methods were used to assess the level of gene flow and estimate divergence time between populations. We used coalescence-based simulations to test the congruence of our genetic data with a scenario of simultaneous divergence of current populations. Results Coalescence-based analyses suggested that these peripheral populations diverged simultaneously at the end of the last glacial episode when their habitats became isolated on mountain summits. High mitochondrial diversity was found in peripheral, isolated populations, while the populations from the core of the species’ range were genetically impoverished. Where mitochondrial diversity has been retained, populations within the same massif exhibited high levels of genetic differentiation. Main conclusions As suggested for many other mountain species, the Pyrenean rock lizard survived glacial maxima through short-distance range shifts instead of migration or contraction in distant southern refugia. Most of the main Pyrenean range has apparently been re-colonized from a single or a few source populations, resulting in a loss of genetic diversity in re-colonized areas. As a result, current levels of intra-population mitochondrial diversity are better explained by post-glacial population history than by current habitat fragmentation. Genetic population differentiation within massifs implies severe reduction in female-mediated gene flow between patches of habitats.