Short-term variations in gene flow related to cyclic
density fluctuations in the common vole
BERTRAND GAUFFRE,* † KARINE BERTHIER, ‡ PABLO INCHAUSTI, § YANNICK CHAVAL, ¶
VINCENT BRETAGNOLLE † andJEAN-FRANC ß OIS COSSON ¶
*INRA, USC 1339 (CEBC-CNRS), F-79360 Beauvoir sur Niort, France, †CEBC-CNRS (UMR 7372), F-79360 Beauvoir sur
Niort, France, ‡Pathologie V eg etale, INRA UR407, Domaine Saint-Maurice, PB 94, 84143 Montfavet Cedex, France, §Centro
Universtario Regional de Este, Universidad de Republica, Maldonado, Uruguay, ¶INRA, UMR 1062 CBGP, F-34988
Montferrier-sur-Lez Cedex, France
Abstract
In highly fluctuating populations with complex social systems, genetic patterns are
likely to vary in space and time due to demographic and behavioural processes. Cyclic
rodents are extreme examples of demographically instable populations that often exhi-
bit strong social organization. In such populations, kin structure and spacing behav-
iour may vary with density fluctuations and impact both the composition and spatial
structure of genetic diversity. In this study, we analysed the multiannual genetic struc-
ture of a cyclic rodent, Microtus arvalis, using a sample of 875 individuals trapped
over three complete cycles (from 1999 to 2007) and genotyped at 10 microsatellite loci.
We tested the predictions that genetic diversity and gene flow intensity vary with den-
sity fluctuations. We found evidences for both spatial scale-dependant variations in
genetic diversity and higher gene flow during high density. Moreover, investigation of
sex-specific relatedness patterns revealed that, although dispersal is biased toward
males in this species, distances moved by both sexes were lengthened during high
density. Altogether, these results suggest that an increase in migration with density
allows to restore the local loss of genetic diversity occurring during low density. We
then postulate that this change in migration results from local competition, which
enhances female colonization of empty spaces and male dispersal among colonies.
Keywords: cyclic rodent populations, gene flow, genetic diversity, Microtus arvalis, migration,
spatial genetic structure
Received 9 November 2012; revision received 12 May 2014; accepted 14 May 2014
Introduction
Under demographically stable conditions, neutral
genetic patterns are expected to be stable over time as a
result of an equilibrium between genetic drift and
migration (Wright 1931, 1943). However, numerous nat-
ural populations, in particular fluctuating populations,
exhibit important spatio-temporal variations in size. In
such populations, both the composition and spatial
structure of neutral genetic diversity are likely to vary
in space and time. Quantifying temporal changes in
neutral genetic patterns in relation to density fluctua-
tions has emerged as an important topic to better
understand demographic and microevolutionary pro-
cesses in natural populations (Schwartz et al. 2007). In
this field, genetic comparative studies, between popula-
tions being in different demographic states or temporal
demo-genetic monitoring, have proved to be very use-
ful approaches to better understand the role of dispersal
in the maintenance of genetic diversity in populations
regularly affected by low numbers (Østergaard et al.
2003; Berthier et al. 2006; Ehrich et al. 2009; Rikalainen
et al. 2012) and in spatial synchrony and spread of out-
breaks (Berthier et al. 2005, 2013; Chapuis et al. 2008,
2009). Comparing patterns for both neutral and adap-
tive genetic variation may also provide insight on den-
sity-dependent changes in selection pressures such as
Correspondence: Bertrand Gauffre, Fax: +33 5 49 09 35 16;
E-mail: gauffre@cebc.cnrs.fr
© 2014 John Wiley & Sons Ltd
Molecular Ecology (2014) 23, 3214–3225 doi: 10.1111/mec.12818