Microevolution of sympatry: landscape genetics of hedgehogs Erinaceus europaeus and E. roumanicus in Central Europe

Abstract

We used the mitochondrial control region and nuclear microsatellites to assess the distribution patterns, population structure, demography and landscape genetics for the hedgehogs Erinaceus europaeus and Erinaceus roumanicus in a transect of the mid-European zone of sympatry. E. roumanicus was less frequent and restricted to regions with lower altitudes. Demographic analyses suggested recent population growth in this species. A comparison of patterns in the spatial variability of mitochondrial and nuclear DNA indicated less sex-biased dispersal and higher levels of gene flow in E. roumanicus. No evidence of recent hybridisation or introgression was detected. We interpreted these results by comparing with phylogeographic and palaeontological studies as well as with the occurrence of hybridisation in the Russian contact zone. We propose that Central Europe was colonised by E. roumanicus by the beginning of the Neolithic period and that there was a subsequent reinforcement stage as well as the formation of a zone of sympatry after the complete reproductive isolation of both species.

Figure 1

Distribution range map of Erinaceus europaeus (blue), E. roumanicus (red) and E. concolor (green) in the western Palearctic (modified according to Reeve (1994) and Aulagnier et al. (2009)). The sympatry zones are violet. The arrows show colonisation routes from refuges after the last ice age (according to Hewitt (2000)). The white rectangle indicates the study area within the sympatric zone.

Figure 2

Sampling for the study in the sympatry zone of Erinaceus europaeus (blue) and E. roumanicus (red). In areas with dense sampling (Prague, Ostrava), not all individuals are displayed owing to space limitations. Country codes: AU, Austria; CZ, Czech Republic; GR, Germany; HU, Hungary; PL, Poland; SK, Slovak Republic. The map was created using the website http://www.mapy.cz.

Figure 3

Median-joining network of mitochondrial control region haplotypes for: (a) Erinaceus europaeus (E1–E17; N=154) from Czech Republic, Germany and Slovak republic; (b) E. roumanicus (ER1–ER7; N=55) from Czech Republic, Slovak Republic and Poland; and E. concolor (EC1–EC2; N=2) from Turkey and Lebanon. Haplotypes are denoted as circles with a size proportional to haplotype frequency. Numbers nearby the connecting lines represent how many mutation steps are between two connected haplotypes and are shown only if the number of steps was more than one. The hypothesised haplotype is represented by untitled dot.

Figure 4

Bayesian skyline plots based on partial sequences of the mitochondrial control region. Time is measured in mutation units per nucleotide position. The y axis represents a correlate of population size (Neμ). Black lines illustrate median Ne estimation, and grey areas show the 95% confidence interval. (a) Erinaceus europaeus (N=134) and (b) E. roumanicus (N=54).

Figure 5

Factorial correspondence analysis based on nine microsatellite loci, showing a multivariate relationship between individuals of Erinaceus europaeus (N=130) and E. roumanicus (N=49) in the Czech and Slovak Republics.

Figure 6

Tessellation maps illustrating the spatial distribution of subpopulations within Erinaceus europaeus and E. roumanicus, inferred by the Bayesian clustering method implemented in GeneLand. Black dots represent sample sites. (a) Microsatellites of E. europaeus, (b) microsatellites of E. roumanicus, (c) mtDNA of E. europaeus and (d) mtDNA of E. roumanicus.