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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amemiya CT, Alfoldi J, Lee AP, Fan SH, Philippe H, MacCallum I, et al (2013) The African coelacanth genome provides insights into tetrapod evolution. Nature 496:311–316. https://doi.org/10.1038/nature12027
Arthington AH (2009) Australian lungfish, Neoceratodus forsteri, threatened by a new dam. Environ Biol Fishes 84:211–221. https://doi.org/10.1007/s10641-008-9414-y
Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744. https://doi.org/10.1046/j.1365-294X.2003.02063.x
Bancroft TL (1911) On a weak point in the life history of Neoceratodus forsteri (Krefft). Proc R Soc Queensland 23:251–256
Bentley AI, Schmidt DJ, Hughes JM (2010) Extensive intraspecific genetic diversity of a freshwater crayfish in a biodiversity hotspot. Freshw Biol 55:1861–1873. https://doi.org/10.1111/j.1365-2427.2010.02420.x
Bouckaert R, Heled J, Kuhnert D, Vaughan T, Wu CH, Xie D, et al (2014) BEAST 2: a software platform for bayesian evolutionary analysis. Plos Comput Biol 10. https://doi.org/10.1371/journal.pcbi.1003537
Brinkmann H, Denk A, Zitzler J, Joss JJ, Meyer A (2004) Complete mitochondrial genome sequences of the South American and the Australian lungfish: testing of the phylogenetic performance of mitochondrial data sets for phylogenetic problems in tetrapod relationships. J Mol Evol 59:834–848. https://doi.org/10.1007/s00239-004-0122-8
Brizga SO, Arthington AH, Choy S, Poplawski W (2000) Burnett basin WAMP: current environmental conditions and impacts of existing water resource development. Queensland Government, Australia
Brooks SG, Kind PK (2002) Ecology and demography of the Queensland lungfish (Neoceratodus forsteri) in the Burnett River, Queensland with reference to the impacts of Walla Weir and future water infrastructure development. Queensland Agency for Food and Fibre Services, Queensland Department of Primary Industries
Burridge CP, Craw D, Fletcher D, Waters JM (2008) Geological dates and molecular rates: fish DNA sheds light on time dependency. Mol Biol Evol 25:624–633. https://doi.org/10.1093/molbev/msm271
Delport W, Poon AFY, Frost SDW, Pond SLK (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455–2457. https://doi.org/10.1093/bioinformatics/btq429
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. Bmc Evol Biol 7. https://doi.org/10.1186/1471-2148-7-214
Excoffier L, Lischer H (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Feutry P, Kyne PM, Pillans RD, Chen X, Naylor GJP, Grewe PM (2014) Mitogenomics of the Speartooth Shark challenges ten years of control region sequencing. BMC Evol Biol 14. https://doi.org/10.1186/s12862-014-0232-x
Frentiu FD, Ovenden JR, Street R (2001) Australian lungfish (Neoceratodus forsteri: Dipnoi) have low genetic variation at allozyme and mitochondrial DNA loci: a conservation alert? Conserv Genet 2:63–67. https://doi.org/10.1023/a:1011576116472
Glenn TC, Nilsen R, Kieran TJ, Finger JW, Pierson TW, Bentley KE, et al (2016) Adapterama I: universal stubs and primers for thousands of dual-indexed Illumina libraries (iTru & iNext). https://doi.org/10.1101/049114
Harris PT, Heap A, Passlow V, Hughes M, Daniell J, Hemer M, Anderson O (2005) Tidally incised valleys on tropical carbonate shelves: an example from the northern Great Barrier Reef, Australia. Mar Geol 220:181–204. https://doi.org/10.1016/j.margeo.2005.06.019
Harrisson K, Pavlova A, Gan HM, Lee YP, Austin CM, Sunnucks P (2016) Pleistocene divergence across a mountain range and the influence of selection on mitogenome evolution in threatened Australian freshwater cod species. Heredity 116:506–515. https://doi.org/10.1038/hdy.2016.8
Heinicke MP, Sander JM, Hedges SB (2009) Lungfishes (Dipnoi). In: Hedges SB, Kumar S (eds) The Timetree of Life. Oxford University Press, New York, pp 348–350
Heled J, Drummond AJ (2008) Bayesian inference of population size history from multiple loci. BMC Evol Biol. https://doi.org/10.1186/1471-2148-8-289
Heller R, Bruniche-Olsen A, Siegismund HR (2012) Cape buffalo mitogenomics reveals a Holocene shift in the African human-megafauna dynamics. Mol Ecol 21:3947–3959. https://doi.org/10.1111/j.1365-294X.2012.05671.x
Huey JA, Espinoza T, Hughes JM (2013) Natural and anthropogenic drivers of genetic structure and low genetic variation in the endangered freshwater cod, Maccullochella mariensis. Conserv Genet 14:997–1008. https://doi.org/10.1007/s10592-013-0490-y
Hughes JM, Schmidt DJ, Huey JA, Real KM, Espinoza T, McDougall A, et al (2015) Extremely low microsatellite diversity but distinct population structure in a long-lived threatened species, the Australian lungfish Neoceratodus forsteri (Dipnoi). Plos One. https://doi.org/10.1371/journal.pone.0121858
Illidge T (1893) On Ceratodus forsteri. Proc R Soc Queensland 10:40–44
Jacobsen MW, Hansen MM, Orlando L, Bekkevold D, Bernatchez L, Willerslev E, Gilbert MTP (2012) Mitogenome sequencing reveals shallow evolutionary histories and recent divergence time between morphologically and ecologically distinct European whitefish (Coregonus spp.). Mol Ecol 21:2727–2742. https://doi.org/10.1111/j.1365-294X.2012.05561.x
Jacobsen MW, da Fonseca RR, Bernatchez L, Hansen MM (2016) Comparative analysis of complete mitochondrial genomes suggests that relaxed purifying selection is driving high nonsynonymous evolutionary rate of the NADH2 gene in whitefish (Coregonus ssp.). Mol Phylogenet Evol 95:161–170. https://doi.org/10.1016/j.ympev.2015.11.008
James JE, Piganeau G, Eyre-Walker A (2016) The rate of adaptive evolution in animal mitochondria. Mol Ecol 25:67–78. https://doi.org/10.1111/mec.13475
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kemp A (1986) The biology of the Australian lungfish, Neoceratodus forsteri (Krefft 1870). J Morphol 181–198
Kemp A (1997) A revision of Australian Mesozoic and Cenozoic lungfish of the family neoceratodontidae (Osteichthyes:Dipnoi), with a description of four new species. J Paleontol 71:713–733
Kemp A (2014) Abnormal development in embryos and hatchlings of the Australian lungfish, Neoceratodus forsteri, from two reservoirs in south-east Queensland. Aust J Zool 62:63–79. https://doi.org/10.1071/zo13038
Kemp A, Huynen L (2014) Occurrence of lungfish in the Brisbane River, Queensland, Australia dates back to 3850 year BP. J Archaeol Sci 52:184–188. https://doi.org/10.1016/j.jas.2014.08.021
Knaus BJ, Cronn R, Liston A, Pilgrim K, Schwartz MK (2011) Mitochondrial genome sequences illuminate maternal lineages of conservation concern in a rare carnivore. BMC Ecol 11:10. https://doi.org/10.1186/1472-6785-11-10
Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701. https://doi.org/10.1093/molbev/mss020
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Pond SLK (2012) Detecting individual sites subject to episodic diversifying selection. Plos Genet. https://doi.org/10.1371/journal.pgen.1002764
Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Pond SLK, Scheffler K (2013) FUBAR: a fast, unconstrained Bayesian approximation for inferring selection. Mol Biol Evol 30:1196–1205. https://doi.org/10.1093/molbev/mst030
O’Connor D (1897) Report on preservation of Ceratodus. Proc R Soc Queensland 10–14:101–102
Palsbøll PJ, Bérubé M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol. https://doi.org/10.1016/j.tree.2006.09.003
Paradis E (2009) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics. https://doi.org/10.1093/bioinformatics/btp696
Pusey BJ, Kennard M, Arthington A (2004) Freshwater fishes of north-eastern Australia. CSIRO Publishing, Collingwood, VIC
Schmidt DJ, Espinoza T, Connell M, Hughes JM (2017) Conservation genetics of the Mary River turtle (Elusor macrurus) in natural and captive populations. Aquat Conserv: Mar Freshw Ecosyst. https://doi.org/10.1002/aqc.2851
Todd EV, Blair D, Farley S, Farrington L, Fitzsimmons NN, Georges A,. .. Jerry DR (2013) Contemporary genetic structure reflects historical drainage isolation in an Australian snapping turtle, Elseya albagula. Zool J Linn Soc 169:200–214. https://doi.org/10.1111/zoj.12049
Unmack PJ, Dowling TE (2010) Biogeography of the genus Craterocephalus (Teleostei: Atherinidae) in Australia. Mol Phylogenet Evol 55:968–984. https://doi.org/10.1016/j.ympev.2010.02.019
Unmack PJ, Hammer MP, Adams M, Johnson JB, Dowling TE (2013) The role of continental shelf width in determining freshwater phylogeographic patterns in south-eastern Australian pygmy perches (Teleostei: Percichthyidae). Mol Ecol 22:1683–1699. https://doi.org/10.1111/mec.12204
Wilson AC, Cann RL, Carr SM, George M, Gyllensten UB, Helmbychowski KM, et al (1985) Mitochondrial-DNA and 2 perspectives on evolutionary genetics. Biol J Lin Soc 26:375–400. https://doi.org/10.1111/j.1095-8312.1985.tb02048.x
Winkelmann I, Campos PF, Strugnell J, Cherel Y, Smith PJ, Kubodera T, et al. (2013) Mitochondrial genome diversity and population structure of the giant squid Architeuthis: genetics sheds new light on one of the most enigmatic marine species. Proc R Soc B. https://doi.org/10.1098/rspb.2013.0273
Yokoyama Y, Purcell A, Marshall JF, Lambeck K (2006) Sea-level during the early deglaciation period in the Great Barrier Reef, Australia. Global Planet Chang 53:147–153. https://doi.org/10.1016/j.gloplacha.2006.01.014
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
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).
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-017-1034-7