Species, ESUs or populations? Delimiting and describing morphologically cryptic diversity in Australian desert spring amphipods
Nicholas P. Murphy A E , Rachael A. King B C and Steven Delean DA Department of Ecology, Environment and Evolution, La Trobe University, Bundoora, Victoria 3086, Australia.
B Australian Centre for Evolutionary Biology and Biodiversity, and School of Earth and Environmental Sciences, The University of Adelaide, SA 5005, Australia.
C South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.
D The Environment Institute and School of Earth and Environmental Sciences, The University of Adelaide, North Terrace, Adelaide, SA 5005, Australia.
E Corresponding author. Email n.murphy@latrobe.edu.au
Invertebrate Systematics 29(5) 457-467 https://doi.org/10.1071/IS14036
Submitted: 16 July 2014 Accepted: 28 July 2015 Published: 30 October 2015
Abstract
Cryptic species are frequently being discovered in refugial habitats, such as desert springs and groundwater systems. Unfortunately, many of these taxa remain as unnamed entities years after their initial discovery. Recent advances in the use of molecular data and coalescent analyses allow DNA-based delimitation of species to move from single locus, tree-based methods to multilocus coalescent analyses. This study compares two DNA-based approaches to delimit species of putatively cryptic freshwater amphipods (Chiltoniidae) from desert springs in central Australia. In addition, a morphometric analysis of 11 characters was undertaken to determine whether the DNA-delimited species were morphologically distinguishable. The single locus method results in identification of lineages that are not supported as species under the multilocus coalescent analyses. We conclude that Wangiannachiltonia guzikae King, 2009, as currently circumscribed, represents six genetically distinct amphipod species, and we describe and name these species despite no clear diagnosable morphological differences. Critically, all of these newly recognised species have extremely limited distributions, which increases the biodiversity significance of their desert spring habitat.
References
Abrams, K. M., King, R. A., Guzik, M. T., Cooper, S. J., and Austin, A. D. (2013). Molecular phylogenetic, morphological and biogeographic evidence for a new genus of parabathynellid crustaceans (Syncarida: Bathynellacea) from groundwater in an ancient southern Australian landscape. Invertebrate Systematics 27, 146–172.| Molecular phylogenetic, morphological and biogeographic evidence for a new genus of parabathynellid crustaceans (Syncarida: Bathynellacea) from groundwater in an ancient southern Australian landscape.Crossref | GoogleScholarGoogle Scholar |
Baur, H., and Leuenberger, C. (2011). Analysis of ratios in multivariate morphometry. Systematic Biology 60, 813–825.
| Analysis of ratios in multivariate morphometry.Crossref | GoogleScholarGoogle Scholar | 21828084PubMed |
Brower, A. V. Z. (2010). Alleviating the taxonomic impediment of DNA barcoding and setting a bad precedent: names for ten species of Astraptes fulgerator (Lepidoptera: Hesperiidae: Eudaminae) with DNA-based diagnoses. Systematics and Biodiversity 8, 485–491.
| Alleviating the taxonomic impediment of DNA barcoding and setting a bad precedent: names for ten species of Astraptes fulgerator (Lepidoptera: Hesperiidae: Eudaminae) with DNA-based diagnoses.Crossref | GoogleScholarGoogle Scholar |
Carstens, B. C., Pelletier, T. A., Reid, N. M., and Satler, J. D. (2013). How to fail at species delimitation. Molecular Ecology 22, 4369–4383.
| How to fail at species delimitation.Crossref | GoogleScholarGoogle Scholar | 23855767PubMed |
Cook, L. G., Edwards, R. D., Crisp, M. D., and Hardy, N. B. (2010). Need morphology always be required for new species descriptions? Invertebrate Systematics 24, 322–326.
| Need morphology always be required for new species descriptions?Crossref | GoogleScholarGoogle Scholar |
Cooper, S. J. B., Bradbury, J. H., Saint, K. M., Leys, R., Austin, A. D., and Humphreys, W. F. (2007). Subterranean archipelago in the Australian arid zone: mitochondrial DNA phylogeography of amphipods from central Western Australia. Molecular Ecology 16, 1533–1544.
| Subterranean archipelago in the Australian arid zone: mitochondrial DNA phylogeography of amphipods from central Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1Gmu7w%3D&md5=c6621aaa61c0722738cf3835b1f0f52dCAS |
Dayrat, B. (2005). Towards integrative taxonomy. Biological Journal of the Linnean Society. Linnean Society of London 85, 407–415.
| Towards integrative taxonomy.Crossref | GoogleScholarGoogle Scholar |
Ebach, M. C. (2011). Taxonomy and the DNA barcoding enterprise. Zootaxa 2742, 67–68.
Fensham, R. J., Silcock, J. L., Kerezsy, A., and Ponder, W. (2011). Four desert waters: setting arid zone wetland conservation priorities through understanding patterns of endemism. Biological Conservation 144, 2459–2467.
| Four desert waters: setting arid zone wetland conservation priorities through understanding patterns of endemism.Crossref | GoogleScholarGoogle Scholar |
Frankham, R., Ballou, J. D., Dudash, M. R., Eldridge, M. D., Fenster, C. B., Lacy, R. C., and Ryder, O. A. (2012). Implications of different species concepts for conserving biodiversity. Biological Conservation 153, 25–31.
| Implications of different species concepts for conserving biodiversity.Crossref | GoogleScholarGoogle Scholar |
Fujita, M. K., Leaché, A. D., Burbrink, F. T., McGuire, J. A., and Moritz, C. (2012). Coalescent-based species delimitation in an integrative taxonomy. Trends in Ecology & Evolution 27, 480–488.
Goldstein, P. Z., and DeSalle, R. (2011). Integrating DNA barcode data and taxonomic practice: determination, discovery, and description. BioEssays 33, 135–147.
| Integrating DNA barcode data and taxonomic practice: determination, discovery, and description.Crossref | GoogleScholarGoogle Scholar | 21184470PubMed |
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
| New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXks1Kms7s%3D&md5=0d70faea5aa5d3d3efa85872d470cc93CAS | 20525638PubMed |
Guzik, M. T., Adams, M. A., Murphy, N. P., Cooper, S. J. B., and Austin, A. D. (2012). Desert springs: deep phylogeographic structure in an ancient endemic crustacean (Phreatomerus latipes). PLoS One 7, e37642.
| Desert springs: deep phylogeographic structure in an ancient endemic crustacean (Phreatomerus latipes).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVyrs7%2FF&md5=79380ba34b6c18c90a4177ae548c04a4CAS | 22815684PubMed |
Harvey, M. S., Rix, M. G., Framenau, V. W., Hamilton, Z. R., Johnson, M. S., Teale, R. J., Humphreys, G., and Humphreys, W. F. (2011). Protecting the innocent: studying short-range endemic taxa enhances conservation outcomes. Invertebrate Systematics 25, 1–10.
| Protecting the innocent: studying short-range endemic taxa enhances conservation outcomes.Crossref | GoogleScholarGoogle Scholar |
Heled, J., and Drummond, A. J. (2010). Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution 27, 570–580.
| Bayesian inference of species trees from multilocus data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitlart7s%3D&md5=8a8ff90c2b847e8d6e3e402005fdeffbCAS | 19906793PubMed |
Hughes, J. B., Hellmann, J. J., Ricketts, T. H., and Bohannan, B. J. M. (2001). Counting the uncountable: statistical approaches to estimating microbial diversity. Applied and Environmental Microbiology 67, 4399–4406.
| Counting the uncountable: statistical approaches to estimating microbial diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXns1Wisro%3D&md5=80ad6a234225265c46cec79bccb0fc2cCAS | 11571135PubMed |
Jörger, K. M., and Schrödl, M. (2013). How to describe a cryptic species? Practical challenges of molecular taxonomy. Frontiers in Zoology 10, 59.
| How to describe a cryptic species? Practical challenges of molecular taxonomy.Crossref | GoogleScholarGoogle Scholar | 24073641PubMed |
Juan, C., Guzik, M. T., Jaume, D., and Cooper, S. J. B. (2010). Evolution in caves: Darwin’s ‘wrecks of ancient life’ in the molecular era. Molecular Ecology 19, 3865–3880.
| Evolution in caves: Darwin’s ‘wrecks of ancient life’ in the molecular era.Crossref | GoogleScholarGoogle Scholar | 20637049PubMed |
Karl, S., and Avise, J. (1993). PCR-based assays of mendelian polymorphisms from anonymous single-copy nuclear DNA: techniques and applications for population genetics. Molecular Biology and Evolution 10, 342–361.
| 1:CAS:528:DyaK3sXitVKitbc%3D&md5=49059961592ef8d43bcac7ccea96b92cCAS | 8098128PubMed |
King, R. A. (2009). Two new genera and species of chiltoniid amphipods (Crustacea: Amphipoda: Talitroidea) from freshwater mound springs in South Australia. Zootaxa 2293, 35–59.
King, R. A., Bradford, T., Austin, A. D., Humphreys, W. F., and Cooper, S. J. (2012). Divergent molecular lineages and not-so-cryptic species: the first descriptions of stygobitic chiltoniid amphipods (Talitroidea: Chiltoniidae) from Western Australia. Journal of Crustacean Biology 32, 465–488.
| Divergent molecular lineages and not-so-cryptic species: the first descriptions of stygobitic chiltoniid amphipods (Talitroidea: Chiltoniidae) from Western Australia.Crossref | GoogleScholarGoogle Scholar |
Leaché, A. D., and Fujita, M. K. (2010). Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proceedings of the National Academy of Sciences of the United States of America 277, 3071–3077.
Leys, R., Watts, C. H. S., Cooper, S. J. B., and Humphreys, W. F. (2003). Evolution of subterranean diving beetles (Coleoptera: Dytiscidae: Hydroporini, Bidessini) in the arid zone of Australia. Evolution 57, 2819–2834.
| 14761060PubMed |
Librado, P., and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
| DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFeqtr8%3D&md5=cdfb8c35061b6117a309c7e7542f0dc0CAS | 19346325PubMed |
Lohse, K. (2009). Can mtDNA barcodes be used to delimit species? A response to Pons et al. (2006). Systematic Biology 58, 439–442.
| Can mtDNA barcodes be used to delimit species? A response to Pons et al. (2006).Crossref | GoogleScholarGoogle Scholar | 20525596PubMed |
Murphy, N. P., Adams, M., and Austin, A. D. (2009). Independent colonization and extensive cryptic speciation of freshwater amphipods in the isolated groundwater springs of Australia’s Great Artesian Basin. Molecular Ecology 18, 109–122.
| 1:CAS:528:DC%2BD1MXit1Grsr0%3D&md5=edb70ef12a381dfa53ef4b72ed34a311CAS | 19140968PubMed |
Murphy, N. P., Adams, M., Guzik, M. T., and Austin, A. D. (2013). Extraordinary micro-endemism in Australian desert spring amphipods. Molecular Phylogenetics and Evolution 66, 645–653.
| Extraordinary micro-endemism in Australian desert spring amphipods.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s7isVGitw%3D%3D&md5=7855fbd457c63dfe35b3ab5cd6a5cabaCAS | 23142695PubMed |
Nevill, J. C., Hancock, P. J., Murray, B. R., Ponder, W. F., Humphreys, W. F., Phillips, M. L., and Groom, P. K. (2010). Groundwater-dependent ecosystems and the dangers of groundwater overdraft: a review and an Australian perspective. Pacific Conservation Biology 16, 187–208.
Ponder, W. F., Eggler, P., and Coglan, D. J. (1995). Genetic differentiation of aquatic snails (Gastropoda: Hydrobiidae) from artesian springs in arid Australia. Biological Journal of the Linnean Society 56, 553–596.
Pons, J., Barraclough, T. G., Gomez-Zurita, J., Cardoso, A., Duran, D. P., Hazell, S., Kamoun, S., Sumlin, W. D., and Vogler, A. P. (2006). Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595–609.
| Sequence-based species delimitation for the DNA taxonomy of undescribed insects.Crossref | GoogleScholarGoogle Scholar | 16967577PubMed |
Posada, D. (2008). Jmodeltest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
| Jmodeltest: phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlKgsb4%3D&md5=ca0a10d07e6e1e3343dbe4441b3f8a36CAS | 18397919PubMed |
R Development Team (2011). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Robertson, H. L., Guzik, M. T., and Murphy, N. P. (2014). Persistence in the desert: ephemeral waterways and small‐scale gene flow in the desert spring amphipod, Wangiannachiltonia guzikae. Freshwater Biology 59, 653–665.
| Persistence in the desert: ephemeral waterways and small‐scale gene flow in the desert spring amphipod, Wangiannachiltonia guzikae.Crossref | GoogleScholarGoogle Scholar |
Rundell, R. J., and Price, T. D. (2009). Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends in Ecology & Evolution 24, 394–399.
| Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation.Crossref | GoogleScholarGoogle Scholar |
Stephens, M., and Donnelly, P. (2003). A comparison of Bayesian methods for haplotype reconstruction from population genotype data. American Journal of Human Genetics 73, 1162–1169.
| A comparison of Bayesian methods for haplotype reconstruction from population genotype data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptVGnsL4%3D&md5=4efdd60a165c6d87c0c575c74c627b27CAS | 14574645PubMed |
Wakeley, J., Nielsen, R., Liu-Cordero, S. N., and Ardlie, K. (2001). The discovery of single-nucleotide polymorphisms – and inferences about human demographic history. American Journal of Human Genetics 69, 1332–1347.
| The discovery of single-nucleotide polymorphisms – and inferences about human demographic history.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhslSgsw%3D%3D&md5=3ba0715bb9314d3cc77ef14eb246cadbCAS | 11704929PubMed |
Yang, Z., and Rannala, B. (2010). Bayesian species delimitation using multilocus sequence data. Proceedings of the National Academy of Sciences of the United States of America 107, 9264–9269.
| Bayesian species delimitation using multilocus sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmslGrtLs%3D&md5=39d806c8a645a74200d7281fdfce13deCAS | 20439743PubMed |