Introduction history overrides social factors in explaining genetic structure of females in Mediterranean mouflon

Abstract

Fine‐scale spatial genetic structure of populations results from social and spatial behaviors of individuals such as sex‐biased dispersal and philopatry. However, the demographic history of a given population can override such socio‐spatial factors in shaping genetic variability when bottlenecks or founder events occurred in the population. Here, we investigated whether socio‐spatial organization determines the fine‐scale genetic structure for both sexes in a Mediterranean mouflon (Ovis gmelini musimon × Ovis sp.) population in southern France 60 years after its introduction. Based on multilocus genotypes at 16 loci of microsatellite DNA (n = 230 individuals), we identified three genetic groups for females and two for males, and concurrently defined the same number of socio‐spatial units using both GPS‐collared individuals (n = 121) and visual resightings of marked individuals (n = 378). The socio‐spatial and genetic structures did not match, indicating that the former was not the main driver of the latter for both sexes. Beyond this structural mismatch, we found significant, yet low, genetic differentiation among female socio‐spatial groups, and no genetic differentiation in males, with this suggesting female philopatry and male‐biased gene flow, respectively. Despite spatial disconnection, females from the north of the study area were genetically closer to females from the south, as indicated by the spatial analysis of the genetic variability, and this pattern was in accordance with the common genetic origin of their founders. To conclude, more than 14 generations later, genetic signatures of first introduction are not only still detectable among females, but they also represent the main factor shaping their present‐time genetic structure.

Both candidate gene and neutral genetic diversity correlate with parasite resistance in female Mediterranean mouflon

“…philopatry, founder events) induce both local adaptation and inbreeding in the population [111]. Due to high female philopatry in the study population [113, 114], moderate inbreeding (a low number of individuals exhibiting low sMLH) is likely to occur in females. On the other hand, the release of founders originating from three diverse origins [115] is likely to have generated outbreeding depression that still persists as observed in this population for other genetic signals [114].…”

“…Due to high female philopatry in the study population [113, 114], moderate inbreeding (a low number of individuals exhibiting low sMLH) is likely to occur in females. On the other hand, the release of founders originating from three diverse origins [115] is likely to have generated outbreeding depression that still persists as observed in this population for other genetic signals [114]. Outbreeding depression might result from underdominance, disruption of epistatic interactions leading to break-down of co-adapted gene complexes and/or loss of local adaptations by disruption of advantageous gene × environment interactions [102].…”

Does host socio-spatial behavior lead to a fine-scale spatial genetic structure in its associated parasites?

“…In the present study, we hypothesized the socio-spatial behavior of Mediterranean mouflon (Supplementary Data 1, [32,57,66]) to limit H. contortus gene flow, resulting in a significant genetic structure in the parasite population. We, however, did not evidence any spatial patterns in the distribution of parasite genetic variability.…”

“…Finally, although Mediterranean mouflon are spatially structured, some overlap persists between socio-spatial unit home ranges (see Fig. 1 in [56], Supporting information G in [66]). Taken together, these host behavioral characteristics might favor step by step parasite exchanges between sub-populations of hosts, and be sufficient to ensure parasite gene flow across the entire study area.…”

“…We aimed here to help answer this question by studying the spatial genetic structure of a H. contortus population parasitizing an isolated wild Mediterranean mouflon population. In this population, males and females have been shown to be spatially structured (Supplementary Data 1 and [32,57,66]) and to have stable home ranges from year to year (see [54], Appendix S2 in [55]). Because H. contortus has a direct life cycle (monoxenous parasite), for which free-living infesting larvae remain close to the host feces [59], we expected the socio-spatial behavior to generate a spatial genetic signature in the population of H. contortus.…”