Evolutionary biogeography of Australian riverine turtles: Elseya spp. and Emydura macquarii krefftii

Todd, Erica V. (2013) Evolutionary biogeography of Australian riverine turtles: Elseya spp. and Emydura macquarii krefftii. PhD thesis, James Cook University.

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Abstract

Australia supports a highly endemic freshwater fauna. The continent's long isolation, Gondwanan heritage, and present aridity make it of particular interest to freshwater biogeographers. Recent molecular genetic studies of freshwater fishes and macroinvertebrates implicate diverse processes of landform evolution, climatic change and sea level fluctuation in shaping current patterns of biodiversity. These studies indicate a biogeographic complexity for Australian freshwaters that is not yet well understood, especially throughout the geographically complex eastern coastal margin. Australian freshwater turtles are one of the continent's few vertebrate freshwater Gondwanan relics that are still taxonomically and ecologically diverse, and geographically widespread. However, in context of their biogeography they remain poorly studied, despite studies on other continents showing turtles to be particularly suited to illuminating complex evolutionary processes. In this thesis is explored the sensitivity of freshwater turtles as models for biogeographic inference in an Australian context, to seek new insights that may clarify and extend our knowledge of Australian freshwater biogeography. Molecular genetic tools are developed and applied to investigate phylogeographies of turtle species from two Australian genera. The evolutionary history of riverine specialist Australian snapping turtles (genus Elseya) is compared to that of the more ecologically generalist and widespread subspecies of Emydura macquarii, and in particular that of Krefft's river turtle, E. m. krefftii. These taxa were chosen as models because both are primarily riverine and broadly sympatric throughout eastern Australia, but differ significantly in niche breadth, range size, and expected dispersal ability.

To address the lack of suitable genetic resources available for Australian short-necked turtles, Next-Generation shotgun genome sequencing was evaluated as a cost-effective means of developing novel genetic resources in two species of freshwater turtle. Low-coverage Roche 454-sequencing was used to randomly sample genomic sequence data for microsatellite repeats in the study species Elseya albagula and Emydura macquarii krefftii. Thousands of microsatellite loci suitable for amplification by PCR were found. Of these, 29 loci were developed for high-resolution population genetic analyses in the study species, which also cross-amplified successfully in a range of other Australian short-necked turtle taxa. Further bioinformatic exploration of the genomic sequence datasets enabled reconstruction of nearcomplete mitochondrial genomes, and characterisation of gene content and repetitive elements. A molecular toolkit of nuclear and mitochondrial markers is presented that provides the foundation for research presented in this thesis, and which will also facilitate future genetic research on Australian freshwater turtles generally.

Drainages within Australia's mid-eastern coastal region (Fitzroy, Burnett and Mary catchments) face considerable urban pressure and contain high freshwater biodiversity and endemism. Mitochondrial (~1.3 kb control region and ND4) and nuclear microsatellite datasets (12 polymorphic loci) were used to investigate genetic structure in the locally endemic whitethroated snapping turtle, Elseya albagula, to clarify historical biogeography and address pressing conservation issues for this species and this region. Individual drainage basins contained discrete genetic units (average pairwise FST = 0.15 and ФST = 0.75 among drainages), though the degree of divergence among drainages varied. The Fitzroy drainage contained a distinct evolutionary lineage, divergent from a second lineage occurring in both the Burnett and Mary drainages. Genetic data were used to make recommendations regarding recognition of evolutionarily significant units and management units for E. albagula. Geological evidence and genetic data for co-distributed freshwater species were consolidated to propose a shared biogeographic history for a diverse regional biota, reflecting historical isolation of the Fitzroy and recent coalescence of the Burnett-Mary drainages during lowered Pleistocene sea levels.

To examine broader-scale evolutionary hypotheses associated with changes to regional riverine connectivity through eustatic sea level change, landform evolution and aridity, a multi-locus molecular approach incorporating mitochondrial (control region, ND4 and 16S) and nuclear (R35 intron) sequences was used to reconstruct phylogenetic relationships and estimate divergence times for all extant Elseya species (including undescribed forms) across Australia and New Guinea. The genus Elseya was shown to contain four divergent, geographically correlated clades, corresponding to all of New Guinea, southern New Guinea plus northern Australia, north-eastern Australia, and south-eastern Australia. These are estimated to have arisen in the Late-Miocene (between ~5.82-9.7 Ma), and diversified further in the early Pleistocene (between ~2.2-2.43 Ma and 1.36-1.66 Ma), coincident with major phases of aridity and climatic upheaval. Overall, snapping turtles were found to have a long vicariant history in Australia and New Guinea, tied to the disconnection of fluvial habitat through landform evolution, sea level change and ongoing aridification. Major implications of these genetic results for understanding freshwater biodiversity evolution in Australia are discussed, including evidence for periodic connectivity with New Guinea, important regional biogeographic barriers (Lake Carpentaria and the Burdekin-Fitzroy drainage divide), and the location of potential freshwater refugia.

Krefft's river turtle, Emydura macquarii krefftii, are common throughout eastern coastal Australia and their extensive longitudinal distribution spans landscape and climatic barriers recently proposed as important in structuring regional freshwater biodiversity. Their evolutionary history in response to climatic oscillations and putative biogeographic barriers was examined using range-wide sampling (649 individuals representing 18 locations across 11 drainages) and analysis of mitochondrial sequences (~1.3 kb control region and ND4) and nuclear microsatellite (12 polymorphic loci) data. Competing demographic (local persistence versus range expansion) and biogeographic (arid corridor versus drainage divide) hypotheses were considered. Krefft's turtles exhibit significant genetic structure across their range at mitochondrial and microsatellite markers, consistent with isolation across drainage divides. Deep north-south regional divergence (2.2%, ND4 p-distance) was consistent with long-term isolation across the Burdekin-Fitzroy drainage divide, not the adjacent Burdekin Gap dry corridor. There was also evidence for rare contemporary overland dispersal across the Burdekin- Fitzroy watershed and for hybridisation with Emydura tanybaraga at the northern range limit. Data suggest Krefft's turtles persisted within the arid Burdekin region throughout multiple episodes of Plio-Pleistocene aridity, though very low contemporary genetic diversity indicates this may have been despite potential population bottlenecks.

Overall, riverine turtle species examined in this thesis exhibited strong, geographically correlated, phylogeographic structure. A remarkable degree of genealogical concordance was observed in phylogeographical patterns between turtle taxa, and turtles and other freshwater groups. Though differences in range size and niche breadth were expected to produce disparities in dispersal ability and phylogeographic structure between the two turtle taxa, both exhibited a primary pattern of genetic structure reflecting isolation across drainage divides. Riverine turtles are indeed sensitive models for inferring historical processes influencing freshwater biodiversity in an Australian context. Molecular data presented in this thesis collectively demonstrate the importance of comparing phylogeographic patterns among co-distributed taxa with variable ecological tolerances and dispersal abilities. Furthermore, the current work not only highlights the potential value of further phylogeographic research into ecologically diverse freshwater turtles in Australia, but provides a comprehensive molecular toolkit for doing so.

Item ID: 39211
Item Type: Thesis (PhD)
Keywords: Australia; biodiversity; biogeography; ecology; Emydura macquarii krefftii; evolution; genetics; Krefft's river turtle; riverine turtles; turtle populations
Date Deposited: 16 Jun 2015 23:38
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060204 Freshwater Ecology @ 33%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060302 Biogeography and Phylogeography @ 33%
06 BIOLOGICAL SCIENCES > 0604 Genetics > 060411 Population, Ecological and Evolutionary Genetics @ 34%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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