Homozygosity at a class II MHC locus depresses female reproductive ability in European brown hares

Abstract

The link between adaptive genetic variation, individual fitness and wildlife population dynamics is fundamental to the study of ecology and evolutionary biology. In this study, a Bayesian modelling approach was employed to examine whether individual variability at two major histocompatibility complex (MHC) class II loci (DQA and DRB) and eight neutral microsatellite loci explained variation in female reproductive success for wild populations of European brown hare (Lepus europaeus). We examined two aspects of reproduction: the ability to reproduce (sterility) and the number of offspring produced (fecundity). Samples were collected from eastern Austria, experiencing a sub-continental climatic regime, and from Belgium with a more Atlantic-influenced climate. As expected, reproductive success (both sterility and fecundity) was significantly influenced by age regardless of sampling locality. For Belgium, there was also a significant effect of DQA heterozygosity in determining whether females were able to reproduce (95% highest posterior density interval of the regression parameter [-3.64, -0.52]), but no corresponding effect was found for Austria. In neither region was reproduction significantly associated with heterozygosity at the DRB locus. DQA heterozygotes from both regions also showed a clear tendency, but not significantly so, to produce a larger number of offspring. Predictive simulations showed that, in Belgium, sub-populations of homozygotes will have higher rates of sterile individuals and lower average offspring numbers than heterozygotes. No similar effect is predicted for Austria. The mechanism for the spatial MHC effect is likely to be connected to mate choice for increased heterozygosity or to the linkage of certain MHC alleles with lethal recessives at other loci.

Polarisation of Major Histocompatibility Complex II Host Genotype with Pathogenesis of European Brown Hare Syndrome Virus

“…Nevertheless, the hypothesis which postulates that polymorphism in the MHC might be maintained by a selective advantage of heterozygotes, is not supported by all population surveys of brown hares [45]. In a recent study of populations from Belgium and Austria, DQA heterozygosity was associated with other biological traits such as reproductive ability, where there was a clear tendency of heterozygotes, to produce a larger number of offspring [94]. Alternatively, the hypothesis of negative frequency-dependent selection could explain the maintenance of the observed high number of rare alleles.…”

Continentality affects body condition and size but not yearly reproductive output in female European hares (Lepus europaeus)

“…To determine the yearly individual reproductive output we counted the total number of placental scars (PSN) after staining (Hackländer et al 2001;Bray et al 2003). We excluded females whenever placental scar counts were ambiguous or when females did not reproduce at all (PSN = 0, see Smith et al 2010). Moreover, we excluded subadult females (born in the year of the hunt), with DLW less than 270 mg (see Suchentrunk These results reveal that there was no effect of study site on annual reproductive output in reproductively active adult female European hares.…”

Beyond splitting hares and rabbiting on about major histocompatibility complex complexity

“…The results from the studies of Smith et al (2010) and Oppelt et al (2010) reflect the reality that there is a consistent lack of consistency for evidence to support a particular mechanism driving MHC diversity. A lack of consensus across populations and taxa suggests that MHC diversity may be defined by an amalgam of effects, incorporating reproductive success, mating systems, antagonistic coevolution with parasites, fluctuating selection pressures, heterozygote advantage or copy number optimality, population demography and extrinsic environmental factors, all of which are likely to be context dependent.…”

“…The paper by Smith et al (2010) addresses one of the outstanding challenges of evolutionary biology -linking reproductive success and underlying genetic variation -by identifying an association between MHC variation and reproductive ability in European hares. Females that are heterozygous at the MHC-DQA locus have significantly higher reproductive ability than those that are homozygous, mediated primarily through reduced sterility, but with some evidence for increased fecundity among nonsterile individuals within the breeding population.…”

“…Linking high levels of MHC diversity to ecological factors in inherently complex natural populations requires a level of experimental design and analytical rigour that is extremely difficult to achieve owing to a plethora of potentially confounding and interacting variables. In this issue of Molecular Ecology, Smith et al (2010) elegantly overcome the challenge of detecting complex interactions in complex systems by using an intricate analytical approach to demonstrate a role for MHC in the reproductive ability of a natural population of the European hare Lepus europaeus (Fig. 1).…”