Mitogenomic analysis of the Australian lungfish (Neoceratodus forsteri) reveals structuring of indigenous riverine populations and late Pleistocene movement between drainage basins

Abstract

Neoceratodus forsteri: is a freshwater species of Dipnoan currently listed as ‘vulnerable to extinction’ under Australian legislation. The species is restricted to at least two indigenous riverine populations in southeastern Queensland, and several other putatively translocated populations. Current understanding of genetic relationships among populations is based on studies of allozymes, microsatellites and mitochondrial DNA (mtDNA) fragments. A notable feature of all these datasets was low genetic variability. Here we sequence the complete mitogenome of 71 N. forsteri individuals from five populations to improve resolution of mtDNA diversity, examine relationships among populations, and evaluate recent demographic history. We recorded 137 variable positions forming 41 haplotypes in the 16,573 bp mitogenome alignment. Strong genetic structure was observed among riverine samples (global ΦST = 0.342) in a pattern consistent with translocation history. Tinana Creek was confirmed as an isolated and genetically unique subpopulation that should be recognized as a distinct management unit. Two previously unreported mtDNA clades (0.46% mean divergence) were found and suggest that genetic exchange among coastal catchments may have been facilitated by riverine connections on the exposed continental shelf during the late Pleistocene. Extended Bayesian skyline analysis showed no evidence for recent historical change in female effective population size, and codon-based selection tests found no evidence for positive selection in coding genes. Overall, our results emphasise the utility of the full mtDNA molecule for capturing population structure in taxa with low genetic diversity. In such cases, informative variation may be scattered across disparate parts of the mitogenome. Surveying relatively short fragments of mtDNA may lead to significant underestimates of population structure when applied to threatened species with low genetic diversity.

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Acknowledgements

Funding for this study was provided by an Australian Research Council Linkage Grant LP13010018 with the support of South East Queensland Water, Queensland Department of Natural Resources and Mines, Queensland Department of Agriculture, Fisheries and Forestry. Samples were collected under Fisheries Permit Numbers 140615 (Seqwater) and 174232 (Griffith University). For their help with various aspects of this project, we thank David Roberts, Thomas Espinoza, Andrew McDougall, Peter Kind, Steven Brooks, Nicole Hogg, and Fraxa Caraiani. We thank Brad Pusey for permission to use the lungfish drawing in Fig. 3.

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Correspondence to Daniel J. Schmidt.

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All field and experimental protocols carried out in this study were approved by the Griffith University Animal Ethics Committee. All procedures were carried out according to Australian Ethics Committee protocol numbers CA2011/10/551 (Seqwater) and ENV/17/14/AEC (Griffith University).

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Bishop, C.R., Hughes, J.M. & Schmidt, D.J. Mitogenomic analysis of the Australian lungfish (Neoceratodus forsteri) reveals structuring of indigenous riverine populations and late Pleistocene movement between drainage basins. Conserv Genet 19, 587–597 (2018). https://doi.org/10.1007/s10592-017-1034-7

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Keywords

  • Genetic diversity
  • Population structure
  • Mitogenome
  • Australian lungfish
  • Phylogeography