Alternated selection mechanisms maintain adaptive diversity in different demographic scenarios of a large carnivore

Different population trajectories are expected to impact the signature of neutral and adaptive processes at multiple levels, challenging the assessment of the relative roles of different microevolutionary forces. Here, we integrate adaptive and neutral variability patterns to disentangle how adaptive diversity is driven under different demographic scenarios within the Iberian wolf (Canis lupus) range. We studied the persistent, the expanding and a small, isolated group within the Iberian wolf population, using 3 MHC class II genes (DRB1, DQA1, and DQB1), which diversity was compared with 39 microsatellite loci.

Both the persistent and the expanding groups show evidence of balancing selection, revealed by a significant departure from neutrality at MHC loci, significant higher observed and expected heterozygosity and lower differentiation at MHC than at neutral loci, and signs of positive selection. However, despite exhibiting a significantly higher genetic diversity than the isolated group, the persistent group did not show significant excess of MHC heterozygotes. The expanding group, while showing a similar level of genetic diversity than the persistent group, displays by contrast a significant excess of MHC heterozygotes, which is compatible with the heterozygote advantage mechanism. Results are not clear regarding the role of drift and selection in the isolated group due to the small size of this population. Although diversity indices of MHC loci correspond to neutral expectations in the isolated group, accelerated MHC divergence, revealed by a higher differentiation at MHC than neutral loci, may indicate diversifying selection.

Different selective pressures were observed in the three different demographic scenarios, which are possibly driven by different selection mechanisms to maintain adaptive diversity.