Glacial cycles drive rapid divergence of cryptic field vole species

Abstract

Understanding the factors that contribute to the generation of reproductively isolated forms is a fundamental goal of evolutionary biology. Cryptic species are an especially interesting challenge to study in this context since they lack obvious morphological differentiation that provides clues to adaptive divergence that may drive reproductive isolation. Geographical isolation in refugial areas during glacial cycling is known to be important for generating genetically divergent populations, but its role in the origination of new species is still not fully understood and likely to be situation dependent. We combine analysis of 35,434 single-nucleotide polymorphisms (SNPs) with environmental niche modeling (ENM) to investigate genomic and ecological divergence in three cryptic species formerly classified as the field vole (Microtus agrestis). The SNPs demonstrate high genomic divergence (pairwise F _ST values of 0.45-0.72) and little evidence of gene flow among the three field vole cryptic species, and we argue that genetic drift may have been a particularly important mechanism for divergence in the group. The ENM reveals three areas as potential glacial refugia for the cryptic species and differing climatic niches, although with spatial overlap between species pairs. This evidence underscores the role that glacial cycling has in promoting genetic differentiation and reproductive isolation by subdivision into disjunct distributions at glacial maxima in areas relatively close to ice sheets. Future investigation of the intrinsic barriers to gene flow between the field vole cryptic species is required to fully assess the mechanisms that contribute to reproductive isolation. In addition, the Portuguese field vole (M. rozianus) shows a high inbreeding coefficient and a restricted climatic niche, and warrants investigation into its conservation status.

Keywords: Microtus agrestis; environmental niche modeling; genetic drift; genotyping‐by‐sequencing; glacial refugia; speciation.

Figure 1

(a) Western European sampling localities for the three species included in SNP analyses. (b) Procrustes transformed genetic and geographic coordinates (details of procrustes transformation in methods). Portuguese (yellow), Mediterranean (red), and short‐tailed (blue) field voles

Figure 2

STRUCTURE plot showing K = 3 for short‐tailed (blue), Mediterranean (red), and Portuguese (yellow) field voles

Figure 3

PCA summarizing 35,434 SNP loci for Portuguese (yellow), Mediterranean (red), and short‐tailed (blue) field vole individuals

Figure 4

(a) Individuals used for parameterizing climatic niche models (N = 377) and the distribution of cryptic species of field vole [P: Portuguese (gray squares), M: Mediterranean (white circles), and St: short‐tailed (black diamonds)] in western Europe (our area for modeling; see text for details). Area in gray shows the field vole distribution in western Europe (Mitchell‐Jones et al., 1999). (b) Predicted cryptic species distribution in Europe according to environmental niche modeling (see text for details) and the species distribution recorded by Mitchell‐Jones et al. (1999). Hatching = short‐tailed, solid black = Mediterranean, and solid gray = Portuguese. Grid cells represent the UTM 50 × 50 km squares

Figure 5

Predicted probability of occurrence of the field vole during the Last Glacial Maximum (LGM) in western Europe according to climatic niche model 4 (individual cryptic species not identified). Hatched areas were excluded for model transferability according to a MESS analysis. Grid cells represent the UTM 50 × 50 km squares

Figure 6

Biogeographical relationships between the cryptic species of the field vole. (P: Portuguese, M: Mediterranean, and St: short‐tailed). Mean favorability scores (defined for each species) are plotted against gradients defined by the absolute local overlap values. The gradients were divided in natural intervals, and mean favorability values (±SD) are shown. The number of sampling sites at each interval is also shown in columns. Areas with higher local overlap of favorability scores between species increase on the x‐axis. Fixed intervals are defined (dotted vertical lines) in the charts and mapped, with light green being the lowest, orange and maroon being median, and dark green being the highest local overlap. Grid cells represent the UTM 50 × 50 km squares