Reconstructing the Evolutionary History of the Australian Magpie (Gymnorhina Tibicen): Patterns of Molecular Variation in a Widespread Passerine and Two Species of Obligate Feather Ectoparasites

Abstract

During the Pleistocene, fluctuating climates led to cycles of glacial/arid activity interspersed with pluvial periods across continents in both northern and southern hemispheres. Many studies in the northern hemisphere have used genetic analysis to document the important role that glacial activity has played in structuring avian populations at high latitudes. However, few have attempted to study the associated effect of aridification at low latitudes in the southern hemisphere. I investigated the past effects that cyclic aridification may have had on the population structure and history of a widespread endemic Australian bird species, the Australian magpie (Gymnorhina tibicen) and two species of obligate feather ectoparasites. 1166 samples from across the native range of G. tibicen were analysed for mitochondrial control region sequence variation and variation at six microsatellite loci. Analysis of mitochondrial control region sequence data indicated monophyletic clades that were geographically congruent with an eastern and western region. Analysis of mitochondrial variation at the sites sampled in this study suggested the contemporary distribution of eastern and western clades is non-overlapping but in close proximity. Analysis of microsatellite variation suggested that secondary contact may have occurred between eastern and western clades in north-western Australia. From AMOVA analysis and Bayesian analysis of population structure (BAPS) it was indicated that contemporary nuclear gene flow preceded mitochondrial gene flow from eastern populations through to north-western Australia. Most eastern, northern and north-western sites showed little geographic structure for microsatellite variation. BAPS analysis of microsatellite variation however, suggested there was as much structure among south-west populations as there was between eastern and western populations. For a majority of population comparisons, estimates of gene flow based on coalescent analyses (LAMARC) suggested higher gene flow rates for males than predicted by differences in effective population size of nuclear DNA compared to mitochondrial DNA. This result coupled with the spread of nuclear DNA preceding mitochondrial DNA supports earlier studies that suggest dispersal in magpies in male biased. Using the program IM, eastern and western mainland clades were estimated to have diverged in the Pleistocene around 36, 000 years ago. The island population of Tasmania was even more recent in origin, possibly since sea levels rose 16,000 years ago, inundating Bass Strait. The putative Carpentarian and possibly Canning barriers in the north and the Nullarbor-Eyrean arid barriers in the south appear to be associated with the divergence between eastern and western mainland populations. Nested clade analysis indicated a signature of range expansion in the eastern region suggesting movement possibly inland and northward subsequent to the last period of aridity. Although not significant, north-eastern and south-eastern populations appeared to show some evidence of a population expansion from mitochondrial DNA. Collectively, phylogeographic analyses suggested that increasing aridity during the Pleistocene played an important role in structuring the Australian magpie. The east to west pattern of mtDNA divergence that was identified contrasts with the striking north to south pattern in morphological (back colour) variation in magpies. Over a large proportion of northern Australia, magpies are black backed (BB) and over a smaller area in southern Australia, magpies are white backed (WB). Between BB’s and WB’s a contact zone is present where both parental forms and magpies with an intermediate black band occur. The discordance between back colour and mtDNA structure in magpies suggests recent history is not responsible for the morphological variation. Mitochondrial cytochrome oxidase I sequence variation was analysed for two species of feather lice associated with G. tibicen. Philopterus sp. has greater habitat specificity than Brueelia semiannulata and as predicted showed deeper divergences among populations than B. semiannulata. There was concordance between the distribution of mitochondrial clades for Philopterus sp. and magpies. The overlap of eastern magpie haplotypes and western Philopterus sp. haplotypes at one site suggested secondary contact among eastern and western clades in northern Australia. Two clades were also evident for B. semiannulata. However they were not congruent with geographic structure of the host or Philopterus sp. Rather, the two non-overlapping B. semiannulata clades were distributed in northern and southern Australia. The divergent clades of B. semiannulata may represent populations that diverged on magpies that were isolated prior to the last period of aridity. It was evident that gene flow occurs among populations of northern and southern B. semiannulata; therefore the contemporary maintenance of divergent clades may be due to selection. One possibility is that selection for thermal tolerance is maintaining current distributions of B. semiannulata.Overall microsatellite variation and mtDNA variation in host and lice suggest that increasing aridity and Pleistocene refugia played a role in structuring populations of the Australian magpie. Since the Pleistocene, the dispersal ability and generalist habitat requirements may have facilitated the movement of magpies into an almost contiguous modern distribution across the continent. This study supports the idea that Pleistocene aridification played an important role in structuring intraspecific variation in low latitudinal southern hemisphere avian species.