Land Bridge Calibration of Rates of Molecular Evolution in a Widespread Rodent

Abstract

There is mounting evidence that rates of molecular evolution decay over recent timescales. Care is needed, therefore, to apply appropriate rates whenever molecular variation is analysed within a temporal context. Given their focus on recent events, intraspecific phylogeographic and demographic studies are particularly vulnerable to erroneous application of rates appropriate to longer periods of evolution and divergence. Rates for recent molecular evolution can be inferred directly from the DNA sequences themselves, but external geophysical events may also be used for calibration. In particular, the formation and loss of land bridges can provide an opportunity to calibrate intraspecific genealogies, estimate molecular rates and infer the absolute timing or scale of demographic changes. The Eurasian field vole Microtus agrestis is an exceptional system with which to examine recent demographic change and divergence in a wild mammal, because of its clear-cut pattern of molecular variation, being composed of three evolutionarily significant units (ESUs) that are reciprocally monophyletic for mitochondrial, sex-chromosome and autosomal markers. These three lineages are confined to northern Eurasia, southern Europe and western Iberia. The northern ESU is in turn comprised of six parapatric mitochondrial lineages, one of them confined to northern Britain. The restricted distribution of this lineage can be associated with the Holocene land bridge connecting Britain with mainland Europe, which permits the temporal calibration of the genealogy and the association of demographic changes with specific climatic episodes. The resulting estimate of the mitochondrial protein-coding substitution rate is very high (ca. 4 × 10⁻⁷ substitutions/site/year), similar to mutation rates measured from pedigrees, i.e. contemporary evolution. The reliability of this estimate is considered.