Causes of Spatial Genetic Structure in Mammals: A Case Study in the Atlantic Forest, Brazil
One of the fundamental links between ecological and evolutionary processes at fine spatial scales is the association between dispersal and gene flow. Population genetic theory predicts that the degree of genetic differentiation among subpopulations is inversely related to the amount of gene flow. Landscape ecology demonstrates that the degree of landscape connectivity among subpopulations is a function of the species’ dispersal capacity. Dispersal distance in mammals scales with both body size and trophic level, which suggests that these natural history characteristics could be good predictors of genetic structure in mammals. The actual dispersal distance is significantly dependent on the degree of heterogeneity of the surrounding landscape. Because dispersal and landscape connectivity, in most species, scale with body size and trophic level, it is plausible to think that genetic structure will also scale with these characteristics. To explore test this hypothesis, I studied the spatial distribution of genetic variation across species of mammals differing in both body size and trophic level within a single landscape.
Samples were collected in the fragmented landscape of the Pontal do Paranapanema, in the western tip of the State of São Paulo, Brasil. The area is contained within the Atlantic Forest of the Interior biome. Both dung and blood samples were collected from collared peccary (Tayassu tajacu), white-lipped peccary (Tayassu pecari), lowland tapir (Tapirus terrestris), ocelot (Leopardus pardalis), and jaguar (Panthera onca). For jaguars, blood samples were also obtained from two other locations, allowing for exploration of genetic variation at larger scales in this species. Samples for pumas (Puma concolor) were also collect, but they were in insufficient number for analysis, and the species was removed from this study. Genetic variation was evaluated using microsatellites.
Two different approaches were taken to analyze the data. First, I inferred genetic structure using a Bayesian model, which simulation data showed to be robust to the conditions present in this study. I then overlaid the inferred structure on a map of the landscape to infer barriers to gene flow. Second, I investigated scaling of genetic structure within an isolation-by-distance framework in the collared peccary, white-lipped peccary, lowland tapir and ocelot. Here, I examined the correlation of genetic relationships among individuals of each species with different measures of geographic distance
The results show significant genetic structure for all five remaining species. Habitat fragmentation affects all species, however, as expected, at different scales. The smaller collared and white-lipped peccaries show genetic partitions that are correlated with habitat fragmentation at smaller scales than the lowland tapir, or either of the two species of carnivores. Levels of genetic differentiation, when compared among species within the landscape, are higher for herbivores than carnivores. In addition, the scale of dispersal, as measured by the point of inflection in the isolation-by-distance curve, increases with body size being smaller for collared peccaries, intermediary for whitelipped peccaries and highest for lowland tapirs. And, current results suggest that the dispersal scale may be very similar for lowland tapirs (large herbivore) and ocelots (small carnivore). However, the social structure displayed by both species of peccaries could be inflating the degree of genetic differentiation in these species, due to the smaller effective population size that social structure implies. But, the fact that tapirs still display a higher degree of structure than carnivores suggests that social structure may not be an important factor in determining differences in degree of genetic differentiation among the examined species. And, the short period (measured in number of generations) since fragmentation occurred in this landscape probably means that some of the observed patterns of genetic structure are in transition, and therefore there is a lack genetic drift – gene flow equilibrium. As such, some of the observed patterns might be reflective of past rather than present levels of connectivity and fragmentation.
These results are in general agreement with the initial predictions and support the hypothesis that genetic structure is scalable with body size and trophic. Collectively, these results indicate that natural history characteristics may be good predictors of genetic structure. In principle, this would allow for studies undertaken in an experimental setting using smaller animals (e.g. insects or mice) at a finer scale to be generalized to larger scales. However, independent studies should be carried out to further corroborate the findings published here. This would allow for more controlled experiments to examine further the effects of body size, trophic level, and other factors such as social structure, degree of landscape heterogeneity, population size, and non-equilibrium among evolutionary forces on the scaling of genetic structure. From a conservation point of view, this study shows that a landscape genetic approach can generate useful and important information. However, the density of data needed for most analyses in landscape genetics still preclude the use of this approach in conservation settings were data are too scarce, and there is little prior ecological and historical information. I also make specific recommendations for the conservation of the Pontal do Paranapanema landscape.