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Genetic structuring among naturally isolated dune lake populations; a microcosm of evolutionary processes on oceanic islands

Genetic structuring among naturally isolated dune lake populations; a microcosm of evolutionary processes on oceanic islands
Angela Duffy

2007

School of Natural Resource Sciences, Queensland University of Technology, Brisbane QLD 4000, AUSTRALIA.

ABSTRACT

Oceanic islands have been used as model systems for studies of evolution and speciation as the range of island sizes coupled with their known geological chronosequence make them ideal systems for the study of spatial and temporal variations in species diversity and distributions. These processes also occur on continental islands and mainland habitats but features of oceanic islands, notably their clearly delimited boundaries, natural isolation and simple geological composition make them more amenable to study.

The perched dune lakes of Fraser Island, Australia share many of the properties of oceanic islands. The naturally isolated formation of the perched lakes, clearly delimited boundaries of the freshwater habitat and phase difference compared to the surrounding, terrestrial environment have significant implications for the biota these lakes support. Inhabitants of the perched dune lakes consist of the aquatic and semi-aquatic descendents of colonisers that were able to traverse a land barrier and survive in the oligotrophic, acidic waters over subsequent generations. Barriers to ongoing gene flow among lake populations, are however likely to be different for species with different life history characteristics. I therefore sought to assess the effects of three different life history characteristics on post-colonisation interpopulation gene flow.

A representative species was selected to represent one of each of the following life history characteristics:

• Aquatic species confined to lake for entire life cycle – freshwater shrimp Caridina indistincta
• Semi-aquatic species capable of terrestrial dispersal – freshwater turtle Emydura krefftii
• Semi-aquatic species capable of aerial dispersal – odonate Orthetrum boumiera

137-250 individuals were sampled per species across six lakes separated by 1-6km. Regions of the mitochondrial genome were targeted and molecular screening methods developed and employed to assess the relative levels of post-colonisation gene flow among lake populations.

Parsimony analysis of the 25 unique haplotypes identified in the species with no apparent inter-lake dispersal mechanism, the freshwater shrimp Caridina indistincta, demonstrated that there was no sharing of derived haplotypes among lake populations. Star shaped genealogies were identified in four lake populations indicative of a population expansion and mismatch distribution analysis confirmed a recent population expansion estimated to have occurred no more than 200,000 years ago. This demonstrates that each of the perched dune lakes was colonised by C. indistincta soon after their inception but that no ongoing gene flow among lake populations has occurred.

The population genetic structure of the species assessed which is capable of terrestrial dispersal suggests that although this species of freshwater turtle, Emydura krefftii, is capable of overland dispersal, gene flow among lake populations is limited. Even at the small spatial scale examined in this study, E. krefftii populations displayed a pattern of isolation by distance (r=0.854, p<0.03). Nested clade analysis also suggested a pattern of restricted gene flow with some long distance dispersal in recent times with long distance dispersal and a possible range expansion occurring historically.

The species examined in this study that displayed the most extensive gene flow among lake populations was the dragonfly Orthetrum boumiera (population pairwise ST all <0.1). No relationship was found between genetic and geographic distance (r= -0.0852, p>0.05) and nested clade analysis could not identify a geographical association among haplotypes, indicative of panmixia. While larval life stages of this species are fully aquatic, the winged adult stages of this species appear to be connecting seemingly isolated lake populations, at least at the spatial scale examined here.

The results of this study have demonstrated that these perched dune lakes provide ‘island like’ models for recent biogeographic processes. The pattern of colonisation and subsequent diversification identified in these populations takes the form of in-situ ‘genetic radiations’ with those populations that are isolated forming monophyletic clades endemic to a single lake. The genetic diversity and endemism identified in this study has occurred over much smaller temporal (<500,000 years) and spatial (<6.5km) scales than in studies of oceanic island fauna. However, the mode of formation of the perched dune lakes and the implications that their natural isolation and abiotic genesis have for the evolution of colonisers of these unique habitats has resulted in them being analogous to true oceanic islands.