Land-bridge calibration of molecular clocks and the post-glacial Colonization of Scandinavia by the Eurasian field vole Microtus agrestis.

Jeremy S Herman,Allan D Mcdevitt,Maarit Jaarola,Agata Kawałko,Jeremy B Searle,Jan M Wójcik,Valerio Ketmaier

doi:10.1371/journal.pone.0103949

Jeremy S Herman, Allan D Mcdevitt + Show 5 more

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https://doi.org/10.1371/journal.pone.0103949

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Abstract

Phylogeography interprets molecular genetic variation in a spatial and temporal context. Molecular clocks are frequently used to calibrate phylogeographic analyses, however there is mounting evidence that molecular rates decay over the relevant timescales. It is therefore essential that an appropriate rate is determined, consistent with the temporal scale of the specific analysis. This can be achieved by using temporally spaced data such as ancient DNA or by relating the divergence of lineages directly to contemporaneous external events of known time. Here we calibrate a Eurasian field vole (Microtus agrestis) mitochondrial genealogy from the well-established series of post-glacial geophysical changes that led to the formation of the Baltic Sea and the separation of the Scandinavian peninsula from the central European mainland. The field vole exhibits the common phylogeographic pattern of Scandinavian colonization from both the north and the south, however the southernmost of the two relevant lineages appears to have originated in situ on the Scandinavian peninsula, or possibly in the adjacent island of Zealand, around the close of the Younger Dryas. The mitochondrial substitution rate and the timescale for the genealogy are closely consistent with those obtained with a previous calibration, based on the separation of the British Isles from mainland Europe. However the result here is arguably more certain, given the level of confidence that can be placed in one of the central assumptions of the calibration, that field voles could not survive the last glaciation of the southern part of the Scandinavian peninsula. Furthermore, the similarity between the molecular clock rate estimated here and those obtained by sampling heterochronous (ancient) DNA (including that of a congeneric species) suggest that there is little disparity between the measured genetic divergence and the population divergence that is implicit in our land-bridge calibration.

Highlights

Phylogeography makes use of spatially ordered genetic data for biogeographical inference
There is growing realization of the need to take account of time-dependence in molecular rate estimates [9,12], as the application of clock rates derived from fixed genetic distances between species to intraspecific genetic data can lead to errors in orders of magnitude [8]
In the absence of dated ancient DNA sequences, calibration of intraspecific data can be achieved by aligning common ancestors with contemporaneous external events, deriving from geological [47] or archaeological [48] evidence

Summary

Introduction

Phylogeography makes use of spatially ordered genetic data for biogeographical inference. Intraspecific phylogeographic studies often rely on the application of published molecular clock rates, as in previous phylogeographic studies of northern Eurasian Microtus voles [4,5,6] These rates are generally derived from the genetic divergence between clearly-defined taxa whose separation can be dated from fossil evidence. It is inappropriate to apply such rates to recent genetic divergence among populations, given that they have been derived from fixed differences that have accumulated over millions of years [8] It has for some time been recognised that there is a decay in molecular evolutionary rates, when these are measured over increasing periods of time [9,10]. Evidence for time dependence and its influence on the inferred timing of evolutionary events are outlined in a recent review [10]

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