MHC diversity of endemic Malagasy rodents in relation to geographic range and social system

Abstract.

The major histocompatibility complex (MHC) encodes a group of closely linked genes that play a central role in the vertebrate immune system. Most natural mammal populations studied so far possess high levels of diversity within the MHC. However, recent investigations in the MHC class II gene DQA of the critically endangered Malagasy giant jumping rat (Hypogeomys antimena) revealed very low variability compared to other mammalian species. The low genetic variability was confirmed in the present study through analyses of the MHC class II gene DRB exon 2. This codes for the antigen-binding site and is therefore considered as one of the most important parts of the MHC. The species' geographic distribution has been reduced recently to a fragmented area of suitable habitat within a geographic range of less than 20×40 km of dry deciduous forest at the west coast of Madagascar. H. antimena has some unusual life history characteristics for a rodent species, such as living in obligate monogamy, with pairs staying together until one mate dies, a low reproduction rate (one to two offspring/couple per year), high site and mate fidelity, short dispersal distances, almost no adult migration, and therefore a constant gene pool with very limited gene flow. Current hypotheses usually interpret low MHC polymorphism either as a consequence of reduced selection pressure, bottleneck effects or by constraints of the mating system. To differentiate between these hypotheses, the MHC variability of the DQA and DRB gene of two additional sympatric, but widely distributed rodent species, Macrotarsomys bastardi and Eliurus myoxinus, were studied by using universal primers and single-strand conformation polymorphism. The two species differ in their mating systems: M. bastardi also lives in pairs but E. myoxinus is a promiscuous species. Whereas the investigated MHC class II genes DQA and DRB had low levels of polymorphism in the pair-living species H. antimena and M. bastardi (DQA: 2 and 3 alleles, DRB: 5 and 6 alleles, respectively), higher levels of variation (DQA: 11 alleles, DRB: 9 alleles) were recorded in the promiscuous species, E. myoxinus. Gene diversity was also higher in E. myoxinus (DQA: 0.85, DRB: 0.86) than in the two pair-living species (DQA: 0.41–0.45, DRB: 0.55–0.63). The results suggest that low MHC variability might not only result from bottleneck effects due to recent declines in population size, but also from a monogamous mating system.