Endemic species may have complex histories: within‐refugium phylogeography of an endangered Iberian vole

Abstract

Glacial refugia protected and promoted biodiversity during the Pleistocene, not only at a broader scale, but also for many endemics that contracted and expanded their ranges within refugial areas. Understanding the evolutionary history of refugial endemics is especially important in the case of endangered species to recognize the origins of their genetic structure and thus produce better informed conservation practices. The Iberian Peninsula is an important European glacial refugium, rich in endemics of conservation concern, including small mammals, such as the Cabrera vole (Microtus cabrerae). This near-threatened rodent is characterized by an unusual suite of genetic, life history and ecological traits, being restricted to isolated geographic nuclei in fast-disappearing Mediterranean subhumid herbaceous habitats. To reconstruct the evolutionary history of the Cabrera vole, we studied sequence variation at mitochondrial, autosomal and sex-linked loci, using invasive and noninvasive samples. Despite low overall mitochondrial and nuclear nucleotide diversities, we observed two main well-supported mitochondrial lineages, west and east. Phylogeographic modelling in the context of the Cabrera vole's detailed fossil record supports a demographic scenario of isolation of two populations during the Last Glacial Maximum from a single focus in the southern part of the Iberian Peninsula. In addition, our data suggest subsequent divergence within the east, and secondary contact and introgression of the expanding western population, during the late Holocene. This work emphasizes that refugial endemics may have a phylogeographic history as rich as that of more widespread species, and conservation of such endemics includes the preservation of that genetic legacy.

Agricultural intensification during the Late Holocene rather than climatic aridification drives the population dynamics and the current conservation status ofMicrotus cabrerae, an endangered Mediterranean rodent

“…Aridity does not have a constraining role in the distribution of this rodent (Table ) because distribution changes from MHPC to APC and from APC to AC reveal a continuous shift from low aridity regions (Pirenaic‐Occitanan) to others of greater aridity (Betic, Montiberican and Luso‐Carpetanian; see aridity map in Figure S3 in Appendix S3 and current versus Mid‐Holocene climate comparison in Appendix S4). This conclusion is corroborated by phylogenetic data of the species (Barbosa et al., ; Figure ), which do not show any evidence of demographic reduction linked to the 5.3 ka BP (Atlantic‐Subboreal transition) climatic crisis but, instead, a constant population increase throughout the Holocene with a more sudden decline at 1.5–2.0 ka. Furthermore, a recent archaeological review questions the ecologic effects of the 5.3 ka BP climatic crisis in the Iberian Peninsula, indicating that this degradation may not be related to an increase in aridity but to a geographical redistribution of human populations and changes in their systems of exploitation of resources (Almagro‐Gorbea, ).…”

“…Overall, our study suggests that, without human pressure, the expansion of M. cabrerae 's distribution area that started after the LGM could continue (and intensify) during the Holocene, associated with a concomitant increase in population size (Barbosa et al., ) . We note that Araújo, Guilhaumon, Rodrogues Neto, Pozo Ortego, and Gómez Calmaestra () and Mestre et al.…”

“…A recent genetic study at the population level that determined the effective female population sizes ( N ef ) during the Holocene (Barbosa et al., ) suggest that its populations (number of individuals) increased until 1.0–2.0 ka BP. This result is consistent for the two phylogenetic lineages of the species (west and east lineages) and for the species as a whole (see Figure , extracted from Barbosa et al., ). Although this chronology supports the hypothesis of decline due to expansion and intensification of agriculture and animal husbandry, it does not directly address the potential drivers of such change.…”

“…Main historic events pinpointed after Almagro‐Gorbea (). Lines are simplified versions of the Bayesian skyline plots based on cyt‐ b data (Barbosa et al., ). The evolution of the total population shows a continuous growth until the 2nd millennium BP , and a subsequent reduction (expansive and decline phases indeed over the X axis).…”

Integrative approaches to guide conservation decisions: Using genomics to define conservation units and functional corridors

“…In this context, the protection of these sparsely distributed habitat patches that appear and disappear through both space and time is likely to reduce the susceptibility of more isolated metapopulations to extinction and prevent a generalized loss of genetic diversity (Frankham et al., ; Mills, ). Previous phylogeographic studies identified two main mitochondrial lineages that likely diverged during and after the last glacial maximum and that are now in secondary contact (Barbosa et al., ). However, the observed nuclear differentiation (based on the analysis of a few autosomal and sex‐linked loci) was very low and inadequate to define CUs .…”