Is MHC diversity a better marker for conservation than neutral genetic diversity? A case study of two contrasting dolphin populations

Abstract

Genetic diversity is essential for populations to adapt to changing environments. Measures of genetic diversity are often based on selectively neutral markers, such as microsatellites. Genetic diversity to guide conservation management, however, is better reflected by adaptive markers, including genes of the major histocompatibility complex (MHC). Our aim was to assess MHC and neutral genetic diversity in two contrasting bottlenose dolphin (Tursiops aduncus) populations in Western Australia—one apparently viable population with high reproductive output (Shark Bay) and one with lower reproductive output that was forecast to decline (Bunbury). We assessed genetic variation in the two populations by sequencing the MHC class II DQB, which encompasses the functionally important peptide binding regions (PBR). Neutral genetic diversity was assessed by genotyping twenty‐three microsatellite loci. We confirmed that MHC is an adaptive marker in both populations. Overall, the Shark Bay population exhibited greater MHC diversity than the Bunbury population—for example, it displayed greater MHC nucleotide diversity. In contrast, the difference in microsatellite diversity between the two populations was comparatively low. Our findings are consistent with the hypothesis that viable populations typically display greater genetic diversity than less viable populations. The results also suggest that MHC variation is more closely associated with population viability than neutral genetic variation. Although the inferences from our findings are limited, because we only compared two populations, our results add to a growing number of studies that highlight the usefulness of MHC as a potentially suitable genetic marker for animal conservation. The Shark Bay population, which carries greater adaptive genetic diversity than the Bunbury population, is thus likely more robust to natural or human‐induced changes to the coastal ecosystem it inhabits.

The inflated significance of neutral genetic diversity in conservation genetics

“…However, the current paradigm in conservation genetics would misleadingly suggest that the population with the most neutral diversity has the highest “adaptive potential” regarding future climatic change. Consequently, a recent study on bottlenose dolphin populations ( Tursiops aduncus ) has argued for an evaluation of the levels of diversity contained within the MHC region, rather genome-wide patterns of neutral genetic diversity, for conservation purposes ( 80 ).…”

Diversification of CD1 Molecules Shapes Lipid Antigen Selectivity

“…Moreover, the patterns of divergence in CD1, with amino acid variation enriched within the MHC-like domain, supports the hypothesis that lipid antigen recognition and presentation are the functional drivers of this divergence. These patterns are also observed in MHC genes (which are also undergoing positive selection), with elevated ω at hotspots in the MHC antigen recognition groove ( Hughes and Nei 1990 ; Manlik et al. 2019 ).…”

Diversification of CD1 molecules shapes lipid antigen selectivity

“…Moreover, the patterns of divergence in CD1, with amino acid variation largely restricted to the MHC-like domain, supports the hypothesis that lipid antigen recognition and presentation are the functional drivers of this divergence. These patterns are also observed in MHC genes (which are also undergoing positive selection), with elevated ω at hotspots in the MHC antigen recognition site (Hughes and Nei 1990;Manlik et al 2019). The electrostatic property variation in lipid ligands is found almost exclusively in the head-groups, with differences in the tail groups restricted to length and geometry of the hydrocarbon tails.…”