Strong population structure in a species manipulated by humans since the Neolithic: the European fallow deer (Dama dama dama)

Abstract

Species that have been translocated and otherwise manipulated by humans may show patterns of population structure that reflect those interactions. At the same time, natural processes shape populations, including behavioural characteristics like dispersal potential and breeding system. In Europe, a key factor is the geography and history of climate change through the Pleistocene. During glacial maxima throughout that period, species in Europe with temperate distributions were forced south, becoming distributed among the isolated peninsulas represented by Anatolia, Italy and Iberia. Understanding modern patterns of diversity depends on understanding these historical population dynamics. Traditionally, European fallow deer (Dama dama dama) are thought to have been restricted to refugia in Anatolia and possibly Sicily and the Balkans. However, the distribution of this species was also greatly influenced by human-mediated translocations. We focus on fallow deer to better understand the relative influence of these natural and anthropogenic processes. We compared modern fallow deer putative populations across a broad geographic range using microsatellite and mitochondrial DNA loci. The results revealed highly insular populations, depauperate of genetic variation and significantly differentiated from each other. This is consistent with the expectations of drift acting on populations founded by small numbers of individuals, and reflects known founder populations in the north. However, there was also evidence for differentiation among (but not within) physically isolated regions in the south, including Iberia. In those regions we find evidence for a stronger influence from natural processes than may be expected for a species with such strong, known anthropogenic influence.

Figure 1

Map showing fallow deer sampling locations from across Europe. Locations are individually numbered to correspond with the samples presented in Table 1. Locations for samples representing each of the unique haplotypes found in Germany are detailed in Ludwig et al. (2012).

Figure 2

Graphical representation of the seven scenarios considered with approximate Bayesian computation using the software DIYABC. See Table 3 and Supplementary Table S7 and Supplementary Figures S4 and S5 for the results of the analysis.

Figure 3

Heatmap of pairwise F_ST values estimated from microsatellite data between all populations. Darker shading indicates higher F_ST values, as indicated by key to the right of the figure.

Figure 4

Assignment probabilities of individuals to putative population clusters at K=3, K=5 and K=10 using the program STRUCTURE 2.3.2. Locations where individuals were sampled are indicated below the graphs. Likelihood support values associated with these analyses are provided in Supplementary Figure S1.

Figure 5

Factorial correspondence analysis (FCA) of population multilocus scores computed using GENETIX based on a comparison of the first three factors.

Figure 6

Median joining network of phylogenetic relationships among fallow deer mitochondrial haplotypes where the size of the circle indicates relative frequency of the haplotype. Haplotypes represented are based on 683 base pairs of the mtDNA control region.