Genetic variation on islands: Mhc polymorphism in populations of the Australian bush rat

Jennifer  Mary Seddon

Island populations provide natural laboratories for testing the theories of population genetics. They provide a system in which the interplay of the forces governing the observed level of genetic variation can be examined. In this study, a series of relict populations of the Australian Bush Rat, Rattus fuscipes greyii, found on islands and the mainland of South Australia form an excellent framework to assess the effects of isolation and fragmentation on Major Histocompatibility Complex (Mhc) variation. Such a model provides a comparison of islands of varying size (60-400,000 hectares) with known and varying times of isolation (6,000-12,000 years). The dominant role of genetic drift in the reduction of genetic variation in these small island populations has been demonstrated previously for neutral (or near neutral) loci in allozyme studies and in the analysis of mitochondrial DNA. However, by examining the levels of polymorphism at an Mhc locus, we may gain an insight into the influence of strong balancing selection in the maintenance of genetic variation in small, isolated populations. Tail tips from rats in two mainland and 14 island populations of R. f greyii had previously been collected, with 25-28 rats sampled per population. Screening for genetic variation at exon 2 of the Mhc locus, RT1.Ba, was performed using Temperature Gradient Gel Electrophoresis (TGGE) in combination with DNA sequencing. Substantial overall variation was found with 36 alleles identified, many showing high allelic divergences. This study provides the first estimate of the amount of Mhc variation in these endemic Australian rats. Island populations generally show a reduction in genetic variation for neutral loci and this has been extended to this Mhc locus, a locus under balancing selection. Only the mainland and the largest island, Kangaroo Island, show high levels of genetic variation, retaining 7 10 alleles per population and showing within-population nucleotide diversity of 0.031 0.058. Most small islands are monomorphic. There is strong population differentiation (Fsr=0.78), with only three shared alleles and no obvious geographical nor temporal structuring. This study is one of the few large studies which confirms the complete absence of variation at an Mhc locus at the nucleotide level in a mammalian population. Comparisons of the observed levels of heterozygosity with those expected under the assumptions of neutrality or of overdominance suggest that fluctutations in population size causing a bottleneck effect may have occurred in some island populations. However, another explanation, a structured source population, is equally powerful in explaining the loss of variation in some populations. Other explanations, including the absence of balancing selection, the presence of directional selection and methodological artefacts, are also explored but found to be less able to explain the observed variation. Two populations, Williams Island and Waldegrave Island, maintain moderately high levels of heterozygosity (52-56%), despite the presence of only two alleles, suggesting the action of balancing selection in the maintenance of variation in these populations. The unusual evolutionary patterns of Mhc loci, including the presence of balancing selection, the retention of ancestral polymorphisms and gene conversion, are explored further in inter-specific comparisons. The evolutionary features evident in the second exon of RTl.Ba and its adjacent intron are examined in a range of species and subspecies of endemic Australian rats. The increase in variability in the functionally important peptide binding sites and, in particular, an increase in the number of non-synonymous substitutions at these sites, suggests the presence of balancing selection acting on the second exon. Clear evidence of the retention of ancestral polymorphism is provided by the presence of an identical exon 2 nucleotide sequence found in two divergent species, R. tunneyi culmorum and R. colletti. In addition, the presence of a retroposon sequence in the intron can be used to divide the species of Australian Rattus into two lineages, with both lineages identified in all major clades of the Australian rats. Finally, a phylogenetic analysis shows that the exon and its adjacent intron show substantial but not complete linkage. At the inter specific level, balancing selection has been sufficiently strong and the rate of recombination sufficiently low to result in an observed influence of this exon on its adjacent non-coding region. Therefore, this study presents the first examination of the amount of variation at an Mhc locus in the species of the endemic Australian rats. The presence of balancing selection and the retention of ancestral polymorphism is demonstrated in the inter-specific comparisons of this group. Furthermore, in an exploration of island populations of one species, R. f greyii, the ability of balancing selection to maintain variation in small, isolated populations is confirmed for three populations. However, there are several forces, such as fluctuations in population size and the influence of the founding population, which have a substantially greater influence on the level of variation observed in small and fragmented populations.

Genetic variation on islands: Mhc polymorphism in populations of the Australian bush rat

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Genetic variation on islands: Mhc polymorphism in populations of the Australian bush rat

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