Abstract
Simple SummaryDisease prevention and appropriate wildlife management are among the major challenges in wildlife conservation. In the present study, we made a first assessment of the variability of major histocompatibility complex (MHC) genes in roe deer in Slovenia and evaluated local population adaptation by comparing MHC variability with neutral microsatellites. We discovered three new MHC DRB exon 2 alleles in addition to seven previously described in the literature. Moreover, we found evidence of historical positive selection, as selection analysis indicated that approx. 10% of the encoded amino acids were subjected to episodic positive selection. This study provides the basis for further research on immunogenetic variation in roe deer and highlights opportunities to incorporate genetic data into science-based population management.Disease control and containment in free-ranging populations is one of the greatest challenges in wildlife management. Despite the importance of major histocompatibility complex (MHC) genes for immune response, an assessment of the diversity and occurrence of these genes is still rare in European roe deer, the most abundant and widespread large mammal in Europe. Therefore, we examined immunogenetic variation in roe deer in Slovenia to identify species adaptation by comparing the genetic diversity of the MHC genes with the data on neutral microsatellites. We found ten MHC DRB alleles, three of which are novel. Evidence for historical positive selection on the MHC was found using the maximum likelihood codon method. Patterns of MHC allelic distribution were not congruent with neutral population genetic findings. The lack of population genetic differentiation in MHC genes compared to existing structure in neutral markers suggests that MHC polymorphism was influenced primarily by balancing selection and, to a lesser extent, by neutral processes such as genetic drift, with no clear evidence of local adaptation. Selection analyses indicated that approx. 10% of amino acids encoded under episodic positive selection. This study represents one of the first steps towards establishing an immunogenetic map of roe deer populations across Europe, aiming to better support science-based management of this important game species.
Highlights
We found no evidence for population genetic differentiation at major histocompatibility complex (MHC) DRB exon 2 alleles (Figure S2); for further analysis, we pooled individuals based on the location of their death into (i) ten predefined groups based on the different historical management of roe deer and geographical characteristics of Slovenia and (ii) three genetically differentiated clusters revealed by neutral genetic markers
We found 10 functional alleles for MHC DRB exon 2 coding for different amino acid sequences among tested individuals
Our conclusion is supported by several facts that showed weaker patterns of genetic structuring for MHC compared with microsatellite loci: (i) Cluster analyses revealed no structure in the MHC (Figure S2, Table S5), whereas three evident genetic clusters were found using microsatellites (Figure S1). (ii) Only one of the pairwise FST comparisons was significant for MHC, while FST values were much higher for microsatellites and were significant in 22 cases, i.e., 52% (Table S4, Table S8). (iii) We found no evidence of isolation by geographic distance for MHC (p = 0.41), while a strong and significant pattern was confirmed for neutral microsatellite loci (p < 0.001; see [44])
Summary
Polymorphism in the major histocompatibility complex (MHC), a family of highly variable genes, plays a key role in populations’ resilience against pathogens [8–10] as well as in sexual selection, mate choice [11–13], fitness, and survival rates [14–19] For this reason, MHC diversity reflects the genetic health of populations [20]. Since the molecular variation among MHC alleles is mainly adaptive and maintained by natural and/or sexual selection [21], these alleles can be considered as non-neutral markers They have been evaluated in conjunction with neutral genetic markers (e.g., [22–26]) to understand the evolutionary forces (especially the effects of drift vs selection) acting on populations, and it is this interplay of neutral and nonneutral markers that shapes genetic diversity. Neutral genetic markers and genes under selections often provide different insights relevant to predicting adaptive/evolutionary potential; a combined view may be the most informative [2,27]
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