Abstract
Two cyprinid species, Parachondrostoma toxostoma, an endemic threatened species, and Chondrostoma nasus, an invasive species, live in sympatry in southern France and form two sympatric zones where the presence of intergeneric hybrids is reported. To estimate the potential threat to endemic species linked to the introduction of invasive species, we focused on the DAB genes (functional MHC IIB genes) because of their adaptive significance and role in parasite resistance. More specifically, we investigated (1) the variability of MHC IIB genes, (2) the selection pattern shaping MHC polymorphism, and (3) the extent to which trans-species evolution and intergeneric hybridization affect MHC polymorphism.In sympatric areas, the native species has more diversified MHC IIB genes when compared to the invasive species, probably resulting from the different origins and dispersal of both species. A similar level of MHC polymorphism was found at population level in both species, suggesting similar mechanisms generating MHC diversity. In contrast, a higher number of DAB-like alleles per specimen were found in invasive species. Invasive species tended to express the alleles of two DAB lineages, whilst native species tended to express the alleles of only the DAB3 lineage. Hybrids have a pattern of MHC expression intermediate between both species. Whilst positive selection acting on peptide binding sites (PBS) was demonstrated in both species, a slightly higher number of positively selected sites were identified in C. nasus, which could result from parasite-mediated selection. Bayesian clustering analysis revealed a similar pattern of structuring for the genetic variation when using microsatellites or the MHC approach. We confirmed the importance of trans-species evolution for MHC polymorphism. In addition, we demonstrated bidirectional gene flow for MHC IIB genes in sympatric areas. The positive significant correlation between MHC and microsatellites suggests that demographic factors may contribute to MHC variation on a short time scale.
Highlights
The focus on genetic variation at the major histocompatibility complex (MHC) represents a new perspective in recent conservation studies to estimate the threat to native species due to habitat modification or destruction, the introduction of non-native species, and climate change
P. toxostoma and C. nasus differ in their levels of MHC polymorphism measured by a spectrum of MHC alleles per species when all ‘‘pure’’ specimens identified using mtDNA and microsatellite markers were taken into account
Concerning the alleles of the DAB1 lineage, 8 DAB1-like alleles were specific to P. toxostoma (7 of them were found in at least two specimens and one was a singleton), and only one DAB1-like allele was specific to C. nasus
Summary
The focus on genetic variation at the major histocompatibility complex (MHC) represents a new perspective in recent conservation studies to estimate the threat to native species due to habitat modification or destruction, the introduction of non-native (invasive) species, and climate change. The functional MHC genes playing a critical role in immune response are especially suitable for genetic studies in the area of conservation focusing on endangered species The high MHC polymorphism is most pronounced in the peptide-binding region (PBR), which is at specific amino-acid sites directly in contact with the bound peptides that mediate the recognition of the foreign antigens derived from pathogens and parasites. This polymorphism is maintained by several evolutionary mechanisms, such as balancing selection associated with the pressure exerted by pathogens and parasites MHC variability can be affected by genetic drift on a short timescale [20]
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