Multilocus coalescent species delimitation reveals widespread cryptic differentiation among Drakensberg mountain-living freshwater crabs (Decapoda : Potamonautes)
Ethel Emmarantia Phiri A and Savel Regan Daniels A BA Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa.
B Corresponding author. Email: srd@sun.ac.za
Invertebrate Systematics 30(1) 60-74 https://doi.org/10.1071/IS15035
Submitted: 24 July 2015 Accepted: 2 December 2015 Published: 16 March 2016
Abstract
Cryptic lineages present major challenges for evolutionary and conservation studies, particularly where these lineages remain undiscovered. Freshwater crabs are known to harbour cryptic diversity, in most cases with limited morphological differences. During the present study, we used a multilocus (12S rRNA, 16S rRNA, COI, 28S rRNA, DecapANT and PEPCK) Bayesian species delimitation to examine cryptic diversity within a freshwater crab species complex (Potamonautes clarus/P. depressus). We sampled 25 highland rivers in the Tugela and uMkomazi River drainage systems of the Drakensberg Mountain range, in the KwaZulu–Natal province of South Africa. Our results showed there to be at least eight lineages: six novel potamonautid freshwater crabs, and two described taxa P. clarus and P. depressus. Divergence from the most recent common ancestor occurred between the mid- and late Miocene (12.1 Mya), while divergence within the species complex occurred ~10.3 Mya up until the Holocene (0.11 Mya). The discovery of six novel lineages of freshwater crabs from a seemingly restricted distribution range has conservation implications, but to date most conservation planning strategies have focussed on freshwater vertebrates. By conducting a fine-scale phylogenetic survey using invertebrates, this study provides a platform for the inclusion of freshwater invertebrates in future conservation assessments.
Additional keywords: Bayesian phylogenetics and phylogeography, conservation, cryptic species, divergence time estimation.
References
Agapow, P. M., Bininda-Emonds, O. R., Crandall, K. A., Gittleman, J. L., Mace, G. M., Marshall, J. C., and Purvis, A. (2004). The impact of species concept on biodiversity studies. The Quarterly Review of Biology 79, 161–179.| The impact of species concept on biodiversity studies.Crossref | GoogleScholarGoogle Scholar |
Barber, B. R., Xu, J., Pérez-Losada, M., Jara, C. G., and Crandall, K. A. (2012). Conflicting evolutionary patterns due to mitochondrial introgression and multilocus phylogeography of the patagonian freshwater crab Aegla neuquensis. PLoS One 7, e37105.
| Conflicting evolutionary patterns due to mitochondrial introgression and multilocus phylogeography of the patagonian freshwater crab Aegla neuquensis.Crossref | GoogleScholarGoogle Scholar |
Barnard, K. H. (1950). Descriptive catalogue of South African decapod Crustacea (crabs and shrimps). Annals of the South African Museum 38, 1–837.
Bauer, A. M., Parham, J. F., Brown, R. M., Stuart, B. L., Grismer, L., Papenfuss, T. J., Böhme, W., Savage, J. M., Carranza, S., Grismer, J. L., Wagner, P., Schmitz, A., Ananjeva, N. B., and Inger, F. R. (2011). Availability of new Bayesian-delimited gecko names and the importance of character-based species descriptions. Proceedings. Biological Sciences 278, 490–492.
| Availability of new Bayesian-delimited gecko names and the importance of character-based species descriptions.Crossref | GoogleScholarGoogle Scholar |
Belliard, J., Böet, P., and Tales, E. (1997). Regional and longitudinal patterns of fish community structure in the Seine River basin, France. Environmental Biology of Fishes 50, 133–147.
| Regional and longitudinal patterns of fish community structure in the Seine River basin, France.Crossref | GoogleScholarGoogle Scholar |
Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K. K., and Das, I. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22, 148–155.
| Cryptic species as a window on diversity and conservation.Crossref | GoogleScholarGoogle Scholar |
Brito, P. H., and Edwards, S. V. (2009). Multilocus phylogeography and phylogenetics using sequence-based markers. Genetica 135, 439–455.
| Multilocus phylogeography and phylogenetics using sequence-based markers.Crossref | GoogleScholarGoogle Scholar |
Brown, R. P., and Yang, Z. (2010). Bayesian dating of shallow phylogenies with a relaxed clock. Systematic Biology 59, 119–131.
| Bayesian dating of shallow phylogenies with a relaxed clock.Crossref | GoogleScholarGoogle Scholar |
Camargo, A., and Sites, J. W., Jr (2013). Species delimitation: a decade after the renaissance. In ‘The Species Problem – Ongoing Issues’. (Ed. I. Y. Pavlinov.)
Camargo, A., Morando, M., Avila, L. J., and Sites, J. W. (2012). Species delimitation with abc and other coalescent‐based methods: a test of accuracy with simulations and an empirical example with lizards of the Liolaemus darwinii complex (Squamata: Liolaemidae). Evolution 66, 2834–2849.
| Species delimitation with abc and other coalescent‐based methods: a test of accuracy with simulations and an empirical example with lizards of the Liolaemus darwinii complex (Squamata: Liolaemidae).Crossref | GoogleScholarGoogle Scholar |
Carstens, B. C., and Dewey, T. A. (2010). Species delimitation using combined coalescent and information-theoretic approach: an example from North American Myotis bats. Systematic Biology 59, 400–414.
| Species delimitation using combined coalescent and information-theoretic approach: an example from North American Myotis bats.Crossref | GoogleScholarGoogle Scholar |
Cavers, S., Telford, A., Arenal Cruz, F., Pérez Castañeda, A. J., Valencia, R., Navarro, C., Buonamici, A., Lowe, A. J., and Vendramin, G. G. (2013). Cryptic species and phylogeographical structure in the tree Cedrela odorata L. throughout the Neotropics. Journal of Biogeography 40, 732–746.
| Cryptic species and phylogeographical structure in the tree Cedrela odorata L. throughout the Neotropics.Crossref | GoogleScholarGoogle Scholar |
Colborn, J., Crabtree, R. E., Shaklee, J. B., Pfeiler, E., and Bowen, B. W. (2001). The evolutionary enigma of bonefishes (Albula spp.): cryptic species and ancient separations in a globally distributed shore fish. Evolution 55, 807–820.
| The evolutionary enigma of bonefishes (Albula spp.): cryptic species and ancient separations in a globally distributed shore fish.Crossref | GoogleScholarGoogle Scholar |
Cook, B. D., Bunn, S. E., and Hughes, J. M. (2002). Genetic structure and dispersal of Macrobrachium australiense (Decapoda: Palaemonidae) in western Queensland, Australia. Freshwater Biology 47, 2098–2112.
| Genetic structure and dispersal of Macrobrachium australiense (Decapoda: Palaemonidae) in western Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |
Cowling, S. A., Cox, P. M., Jones, C. D., Maslin, M. A., Peros, M., and Spall, S. A. (2008). Simulated glacial and interglacial vegetation across Africa: implications for species phylogenies and trans-African migration of plants and animals. Global Change Biology 14, 827–840.
| Simulated glacial and interglacial vegetation across Africa: implications for species phylogenies and trans-African migration of plants and animals.Crossref | GoogleScholarGoogle Scholar |
Cumberlidge, N., and Daniels, S. R. (2014). Recognition of two new species of freshwater crabs fromthe Seychelles based on molecular evidence (Potamoidea: Potamonautidae). Invertebrate Systematics 28, 17–31.
| Recognition of two new species of freshwater crabs fromthe Seychelles based on molecular evidence (Potamoidea: Potamonautidae).Crossref | GoogleScholarGoogle Scholar |
Daniels, S. R. (2011). Reconstructing the colonisation and diversification history of the endemic freshwater crab (Seychellum alluaudi) in the granitic and volcanic Seychelles Archipelago. Molecular Phylogenetics and Evolution 61, 534–542.
| Reconstructing the colonisation and diversification history of the endemic freshwater crab (Seychellum alluaudi) in the granitic and volcanic Seychelles Archipelago.Crossref | GoogleScholarGoogle Scholar |
Daniels, S. R., Stewart, B. A., and Gibbons, M. J. (1998). Potamonautes granularis sp. nov. (Brachyura, Potamonautidae), a new cryptic species of river crab from the Olifants River system, South Africa. Crustaceana 71, 885–903.
| Potamonautes granularis sp. nov. (Brachyura, Potamonautidae), a new cryptic species of river crab from the Olifants River system, South Africa.Crossref | GoogleScholarGoogle Scholar |
Daniels, S. R., Stewart, B. A., and Gibbons, M. J. (1999). Genetic structure among populations of Potamonautes perlatus (Decapoda: Potamonautidae) from the Olifants River system in the Western Cape, South Africa. Journal of Zoology 249, 137–142.
| Genetic structure among populations of Potamonautes perlatus (Decapoda: Potamonautidae) from the Olifants River system in the Western Cape, South Africa.Crossref | GoogleScholarGoogle Scholar |
Daniels, S. R., Stewart, B. A., and Burmeister, L. (2001). Geographic patterns of genetic and morphological divergence amongst populations of a freshwater crab with the description of a species from mountain streams in the Western Cape. Zoologica Scripta 30, 181–197.
| Geographic patterns of genetic and morphological divergence amongst populations of a freshwater crab with the description of a species from mountain streams in the Western Cape.Crossref | GoogleScholarGoogle Scholar |
Daniels, S. R., Stewart, B. A., Gouws, G., Cunningham, M., and Matthee, C. A. (2002). Phylogenetic relationships of the southern African freshwater crab fauna derived from multiple data sets reveal biogeographic patterning. Molecular Phylogenetics and Evolution 25, 511–523.
| Phylogenetic relationships of the southern African freshwater crab fauna derived from multiple data sets reveal biogeographic patterning.Crossref | GoogleScholarGoogle Scholar |
Daniels, S. R., Gouws, G., Stewart, B. A., and Coke, M. (2003). Molecular and morphometric data demonstrate the presence of cryptic lineages among freshwater crabs (Decapoda: Potamonautidae: Potamonautes) from the Drakensberg Mountains, South Africa. Biological Journal of the Linnean Society. Linnean Society of London 78, 129–147.
| Molecular and morphometric data demonstrate the presence of cryptic lineages among freshwater crabs (Decapoda: Potamonautidae: Potamonautes) from the Drakensberg Mountains, South Africa.Crossref | GoogleScholarGoogle Scholar |
Daniels, S. R., Mouton, P. le F. N., and du Toit, D. A. (2004). Molecular data suggest that melanistic ectotherms at the south‐western tip of Africa are the products of Miocene climatic events: evidence from cordylid lizards. Journal of Zoology 263, 373–383.
| Molecular data suggest that melanistic ectotherms at the south‐western tip of Africa are the products of Miocene climatic events: evidence from cordylid lizards.Crossref | GoogleScholarGoogle Scholar |
Daniels, S. R., Gouws, G., and Crandall, K. A. (2006a). Phylogeographic patterning in a freshwater crab species (Decapoda: Potamonautidae: Potamonautes) reveals the signature of historical climatic oscillations. Journal of Biogeography 33, 1538–1549.
| Phylogeographic patterning in a freshwater crab species (Decapoda: Potamonautidae: Potamonautes) reveals the signature of historical climatic oscillations.Crossref | GoogleScholarGoogle Scholar |
Daniels, S. R., Cumberlidge, N., Pérez-Losada, M., Marijnissen, S. A. E., and Crandall, K. A. (2006b). Evolution of Afrotropical freshwater crab lineages obscured by morphological convergence. Molecular Phylogenetics and Evolution 40, 227–235.
| Evolution of Afrotropical freshwater crab lineages obscured by morphological convergence.Crossref | GoogleScholarGoogle Scholar |
Daniels, S. R., Hofmeyr, M. D., Henen, B., and Crandall, K. A. (2007). Living with the genetic signature of Miocene induced change: evidence from the phylogeographic structure of the endemic angulate tortoise Chersina angulata. Molecular Phylogenetics and Evolution 45, 915–926.
| Living with the genetic signature of Miocene induced change: evidence from the phylogeographic structure of the endemic angulate tortoise Chersina angulata.Crossref | GoogleScholarGoogle Scholar |
Daniels, S. R., Phiri, E. E., Klaus, S., Albrecht, C., and Cumberlidge, N. (2015). Multilocus phylogeny of the Afrotropical freshwater crab fauna reveals historical drainage connectivity and transoceanic dispersal since the Eocene. Systematic Biology 64, 549–567.
| Multilocus phylogeny of the Afrotropical freshwater crab fauna reveals historical drainage connectivity and transoceanic dispersal since the Eocene.Crossref | GoogleScholarGoogle Scholar |
De Queiroz, K. (1998). The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In ‘Endless Farms: Species and Speciation’. (Eds D. J. Howard and S. H. Berlocher.) pp. 57–75. (Oxford University Press: Oxford.)
De Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology 56, 879–886.
| Species concepts and species delimitation.Crossref | GoogleScholarGoogle Scholar |
Degnan, J. H., and Rosenberg, N. A. (2009). Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends in Ecology & Evolution 24, 332–340.
| Gene tree discordance, phylogenetic inference and the multispecies coalescent.Crossref | GoogleScholarGoogle Scholar |
Diedericks, G., and Daniels, S. R. (2014). Ain’t no mountain high enough, ain’t no valley low enough? Phylogeography of the rupicolous Cape girdled lizard (Cordylus cordylus) reveals a generalist pattern. Molecular Phylogenetics and Evolution 71, 234–248.
| Ain’t no mountain high enough, ain’t no valley low enough? Phylogeography of the rupicolous Cape girdled lizard (Cordylus cordylus) reveals a generalist pattern.Crossref | GoogleScholarGoogle Scholar |
Dingle, R. V., Giesser, W. G., and Newton, A. R. (1983). ‘Mesozoic and Tertiary Geology of Southern Africa.’ (AA Balkema: Rotterdam.)
Drummond, A. J., and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
| BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar |
Drummond, A. J., Nicholls, G. K., Rodrigo, A. G., and Solomon, W. (2002). Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161, 1307–1320.
Drummond, A. J., Rambaut, A., and Suchard, M. (2009). BEAST, Version 1.5.2. Available at http://code.google.com/p/beast-mcmc/ [Verified February 2016]
Drummond, A. J., Rambaut, A., and Bouckaert, R. (2012a). Divergence Dating Tutorial with BEAST 2.0. Available at https://beast2.googlecode.com/files/DivergenceDatingTutorial.v2.0.e.pdf [Verified February 2016]
Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012b). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
| Bayesian phylogenetics with BEAUti and the BEAST 1.7.Crossref | GoogleScholarGoogle Scholar |
Edwards, S. V. (2009). Is a new and general theory of molecular systematics emerging? Evolution 63, 1–19.
| Is a new and general theory of molecular systematics emerging?Crossref | GoogleScholarGoogle Scholar |
Ence, D. D., and Carstens, B. C. (2011). SpedeSTEM: a rapid and accurate method for species delimitation. Molecular Ecology Resources 11, 473–480.
| SpedeSTEM: a rapid and accurate method for species delimitation.Crossref | GoogleScholarGoogle Scholar |
Fitch, F. L., and Millar, J. A. (1971). Potassium-Argon radio ages of Karoo volcanic rocks from Lesotho. Bulletin Volcanologique 35, 64–84.
| Potassium-Argon radio ages of Karoo volcanic rocks from Lesotho.Crossref | GoogleScholarGoogle Scholar |
Fouquet, A., Vences, M., Salducci, M.-D., Meyer, A., Marty, C., Blanc, M., and Gilles, A. (2007). Revealing cryptic diversity using molecular phylogenetics and phylogeography in frogs of the Scinax ruber and Rhinella margaritifera species groups. Molecular Phylogenetics and Evolution 43, 567–582.
| Revealing cryptic diversity using molecular phylogenetics and phylogeography in frogs of the Scinax ruber and Rhinella margaritifera species groups.Crossref | GoogleScholarGoogle Scholar |
Fraser, L. H., and Keddy, P. A. (eds.) (2005). ‘The World’s Largest Wetlands: Ecology and Conservation.’ (Cambridge University Press: Cambridge, UK.)
Fujita, M. K., and Leaché, A. D. (2011). A coalescent perspective on delimiting and naming species: a reply to Bauer et al. Proceedings of the Royal Society B 278, 493–495.
| A coalescent perspective on delimiting and naming species: a reply to Bauer et al.Crossref | GoogleScholarGoogle Scholar |
Funk, W. C., Caminer, M., and Ron, S. R. (2012). High levels of cryptic species diversity uncovered in Amazonian frogs. Proceedings of the Royal Society B, Biological Series 279, 1806–1814.
Gascon, C., Malcolm, J. R., Patton, J. L., da Silva, M. N. F., Bogart, J. P., Lougheed, S. C., Peres, C. A., Neckel, S., and Boag, P. T. (2000). Riverine barriers and the geographic distribution of Amazonian species. Proceedings of the National Academy of Sciences of the United States of America 97, 13672–13677.
| Riverine barriers and the geographic distribution of Amazonian species.Crossref | GoogleScholarGoogle Scholar |
Gouws, G., Stewart, B. A., and Coke, M. (2000). Evidence for a new species of river crab (Decapoda, Brachyura, Potamonautidae) from the Drakensberg, South Africa. Journal of Crustacean Biology 20, 743–758.
| Evidence for a new species of river crab (Decapoda, Brachyura, Potamonautidae) from the Drakensberg, South Africa.Crossref | GoogleScholarGoogle Scholar |
Gouws, G., Stewart, B. A., and Daniels, S. R. (2004). Cryptic species within the freshwater isopod Mesamphisopus capensis (Phreatoicidea: Amphisopodidae) in the Western Cape, South Africa: allozyme and 12S rRNA sequence data and morphometric evidence. Biological Journal of the Linnean Society. Linnean Society of London 81, 235–253.
| Cryptic species within the freshwater isopod Mesamphisopus capensis (Phreatoicidea: Amphisopodidae) in the Western Cape, South Africa: allozyme and 12S rRNA sequence data and morphometric evidence.Crossref | GoogleScholarGoogle Scholar |
Hebert, P., Penton, E. H., Burns, J. M., Janzen, D., and Hallwachs, W. (2004). Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101, 14812–14817.
| Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator.Crossref | GoogleScholarGoogle Scholar |
Heled, J., and Drummond, A. (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 |
Hey, J. (2001). ‘Genes, Categories, and Species: the Evolutionary and Cognitive Causes of the Species Problem.’ (Oxford University Press: New York.)
Hey, J. (2009). On the arbitrary identification of real species. In ‘Speciation and Patterns of Diversity’. (Eds R. K. Butlin, J. R. Bridle and D. Schluter.) pp. 15–28. (Cambridge University Press: Cambridge.)
Hogg, I. D., Eadie, J. M., and de Lafontaine, Y. (1998). Atmospheric change and the diversity of aquatic invertebrates: are we missing the boat? Environmental Monitoring and Assessment 49, 291–301.
| Atmospheric change and the diversity of aquatic invertebrates: are we missing the boat?Crossref | GoogleScholarGoogle Scholar |
Huelsenbeck, J. P., and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
| MrBayes: Bayesian inference of phylogenetic trees.Crossref | GoogleScholarGoogle Scholar |
Hughes, R. H., and Hughes, J. S. (1992). A directory of African Wetlands. IUCN. Available at https://portals.iucn.org/library/sites/library/files/documents/1992-007.pdf [Verified February 2016]
Jara, C. G., Pérez-Losada, M., and Crandal, K. A. (2003). Aegla occidentalis (Crustacea: Decapoda: Aeglidae), a new species of freshwater crab from ther Nehuelbuta Coastal Range, Chile. Proceedings of the Biological Society of Washington 116, 933–942.
Jesse, R., Schubart, C. D., and Klaus, S. (2010). Identification of a cryptic lineage within Potamon fluviatile (Herbst) (Crustacea: Brachyura: Potamidae). Invertebrate Systematics 24, 348–356.
| Identification of a cryptic lineage within Potamon fluviatile (Herbst) (Crustacea: Brachyura: Potamidae).Crossref | GoogleScholarGoogle Scholar |
Klaus, S., Mendoza, J. C., Liew, J. H., Plath, M., Meier, R., and Yeo, D. C. (2013). Rapid evolution of troglomorphic characters suggests selection rather than neutral mutation as a driver of eye reduction in cave crabs. Biology Letters 9, 2012.1098.
Knee, W., Beaulieu, F., Skevington, J. H., Kelso, S., Cognato, A. I., and Forbes, M. R. (2012). Species boundaries and host range of tortoise mites (Uropodoidea) phoretic on bark beetles (Scolytinae), using morphometric and molecular markers. PLoS One 7, e47243.
| Species boundaries and host range of tortoise mites (Uropodoidea) phoretic on bark beetles (Scolytinae), using morphometric and molecular markers.Crossref | GoogleScholarGoogle Scholar |
Knowles, L. L. (2009). Estimating species trees: methods of phylogenetic analysis when there is incongruence across genes. Systematic Biology 58, 463–467.
| Estimating species trees: methods of phylogenetic analysis when there is incongruence across genes.Crossref | GoogleScholarGoogle Scholar |
Knowles, L. L., and Kubatko, L. S. (Eds) (2010). Estimating species trees: an introduction to concepts and models. In ‘Estimating Species Trees: Practical and Theoretical Aspects’. pp. 1–14. (Wiley-Blackwell: Hoboken, NJ.)
Knowlton, N. (1986). Cryptic and sibling species among the decapod Crustacea. Journal of Crustacean Biology 6, 356–363.
| Cryptic and sibling species among the decapod Crustacea.Crossref | GoogleScholarGoogle Scholar |
Knowlton, N. (1993). Sibling species in the sea. Annual Review of Ecology Evolution and Systematics 24, 189–216.
| Sibling species in the sea.Crossref | GoogleScholarGoogle Scholar |
Kubatko, L. S., and Degnan, J. H. (2008). Inconsistency of phylogenetic estimates from concatenated data under coalescence. Systematic Biology 56, 17–24.
| Inconsistency of phylogenetic estimates from concatenated data under coalescence.Crossref | GoogleScholarGoogle Scholar |
Kubatko, L. S., Carstens, B. C., and Knowles, L. L. (2009). STEM: species tree estimation using maximum likelihood for gene trees under coalescence. Bioinformatics 25, 971–973.
| STEM: species tree estimation using maximum likelihood for gene trees under coalescence.Crossref | GoogleScholarGoogle Scholar |
Leaché, A. D., and Fujita, M. K. (2010). Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proceedings of the Royal Society B, Biological Series 277, 3071–3077.
Lemme, I., Erbacher, M., Kaffenberger, N., Vences, M., and Köhler, J. (2013). Molecules and morphology suggest cryptic species diversity and an overall complex taxonomy of fish scale geckos, genus Geckolepis. Organisms, Diversity & Evolution 13, 87–95.
| Molecules and morphology suggest cryptic species diversity and an overall complex taxonomy of fish scale geckos, genus Geckolepis.Crossref | GoogleScholarGoogle Scholar |
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 |
Linder, H. P., Johnson, S. D., Kuhlmann, M., Matthee, C. A., Nyffeler, R., and Swartz, E. R. (2010). Biotic diversity in the Southern African winter-rainfall region. Current Opinion in Environmental Sustainability 2, 109–116.
| Biotic diversity in the Southern African winter-rainfall region.Crossref | GoogleScholarGoogle Scholar |
Liu, L. (2008). BEST: Bayesian estimation of species trees under the coalescent model. Bioinformatics 24, 2542–2543.
| BEST: Bayesian estimation of species trees under the coalescent model.Crossref | GoogleScholarGoogle Scholar |
Liu, L., and Pearl, D. K. (2007). Species trees from gene trees: reconstructing Bayesian posterior distributions of a species phylogeny using estimated gene tree distributions. Systematic Biology 56, 504–514.
| Species trees from gene trees: reconstructing Bayesian posterior distributions of a species phylogeny using estimated gene tree distributions.Crossref | GoogleScholarGoogle Scholar |
Liu, L., Yu, L., Kubatko, L., Pearl, D. K., and Edwards, S. V. (2009). Coalescent methods for estimating phylogenetic trees. Molecular Phylogenetics and Evolution 53, 320–328.
| Coalescent methods for estimating phylogenetic trees.Crossref | GoogleScholarGoogle Scholar |
Lohman, D. J., Ingram, K. K., Prawiradilaga, D. M., Winker, K., Sheldon, F. H., Moyle, R. G., Ng, P. K. L., Ong, P. S., Wang, L. K., Braile, T. M., Astuti, D., and Meier, R. (2010). Cryptic genetic diversity in “widespread” Southeast Asian bird species suggests that Philippine avian endemism is gravely underestimated. Biological Conservation 143, 1885–1890.
| Cryptic genetic diversity in “widespread” Southeast Asian bird species suggests that Philippine avian endemism is gravely underestimated.Crossref | GoogleScholarGoogle Scholar |
McCormack, J. E., Heled, J., Delaney, K. S., Peterson, A. T., and Knowles, L. L. (2011). Calibrating divergence times on species trees versus gene trees: implications for speciation history of Aphelocoma jays. Evolution 65, 184–202.
| Calibrating divergence times on species trees versus gene trees: implications for speciation history of Aphelocoma jays.Crossref | GoogleScholarGoogle Scholar |
McFadden, C. S., and van Ofwegen, L. P. (2013). A second, cryptic species of the soft coral genus Incrustatus (Anthozoa: Octocorallia: Clavulariidae) from Tierra del Fuego, Argentina, revealed by DNA barcoding. Helgoland Marine Research 67, 137–147.
| A second, cryptic species of the soft coral genus Incrustatus (Anthozoa: Octocorallia: Clavulariidae) from Tierra del Fuego, Argentina, revealed by DNA barcoding.Crossref | GoogleScholarGoogle Scholar |
Murray, T. E., Fitzpatrick, U., Brown, M. J. F., and Paxton, R. J. (2008). Cryptic species diversity in a widespread bumble bee complex revealed using mitochondrial DNA RFLPs. Conservation Genetics 9, 653–666.
| Cryptic species diversity in a widespread bumble bee complex revealed using mitochondrial DNA RFLPs.Crossref | GoogleScholarGoogle Scholar |
Nei, M., and Kumar, S. (2000). ‘Molecular Evolution and Phylogenetics.’ (Oxford University Press: Oxford.)
O’Meara, B. C. (2010). New heuristic methods for joint species delimitation and species tree inference. Systematic Biology 59, 59–73.
| New heuristic methods for joint species delimitation and species tree inference.Crossref | GoogleScholarGoogle Scholar |
Padial, J. M., and de la Riva, I. (2009). Integrative taxonomy reveals cryptic Amazonian species of Pristimantis (Anura: Strabomantidae). Zoological Journal of the Linnean Society 155, 97–122.
| Integrative taxonomy reveals cryptic Amazonian species of Pristimantis (Anura: Strabomantidae).Crossref | GoogleScholarGoogle Scholar |
Partridge, T. C. (1998). Of diamonds, dinosaurs and diastrophism: 150 million years of landscape evolution in southern Africa. South African Journal of Geology 101, 167–184.
Partridge, T. C., and Maud, R. R. (1987). Geomorphic evolution of Southern Africa since the Mesozoic. South African Journal of Geology 90, 179–208.
Partridge, T. C., and Maud, R. R. (2000). Macro-scale geomorphic evolution of southern Africa. In ‘The Cenozoic of Southern Africa’. (Eds T. C. Partridge and R. R. Maud.) pp. 3–18. (Oxford University Press: New York.)
Paupério, J., Herman, J. S., Melo-Ferreira, J., Jaarola, M., Alves, P. C., and Searle, J. B. (2012). Cryptic speciation in the field vole: a multilocus approach confirms three highly divergent lineages in Eurasia. Molecular Ecology 21, 6015–6032.
| Cryptic speciation in the field vole: a multilocus approach confirms three highly divergent lineages in Eurasia.Crossref | GoogleScholarGoogle Scholar |
Pedraza-Lara, C., Doadrio, I., Breinholt, J. W., and Crandall, K. A. (2012). Phylogeny and evolutionary patterns in the dwarf crayfish subfamily (Decapoda: Cambarellinae). PLoS One 7, e48233.
| Phylogeny and evolutionary patterns in the dwarf crayfish subfamily (Decapoda: Cambarellinae).Crossref | GoogleScholarGoogle Scholar |
Pfenninger, M., Staubach, S., Albrecht, C., Streit, B., and Schwenk, K. (2003). Ecological and morphological differentiation among cryptic evolutionary lineages in freshwater limpets of the nominal form-group Ancylus fluviatilis (O.F. Müller, 1774). Molecular Ecology 12, 2731–2745.
| Ecological and morphological differentiation among cryptic evolutionary lineages in freshwater limpets of the nominal form-group Ancylus fluviatilis (O.F. Müller, 1774).Crossref | GoogleScholarGoogle Scholar |
Phiri, E. E., and Daniels, S. R. (2014). Disentangling the divergence and cladogenesis in the freshwater crab species (Potamonautidae: Potamonautes perlatus sensu lato) in the Cape Fold Mountains, South Africa, with the description of two novel cryptic lineages. Zoological Journal of the Linnean Society 170, 310–332.
| Disentangling the divergence and cladogenesis in the freshwater crab species (Potamonautidae: Potamonautes perlatus sensu lato) in the Cape Fold Mountains, South Africa, with the description of two novel cryptic lineages.Crossref | GoogleScholarGoogle Scholar |
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
| jModelTest: phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar |
Puckridge, M., Andreakis, N., Appleyard, S. A., and Ward, R. D. (2013). Cryptic diversity in flathead fishes (Scorpaeniformes: Platycephalidae) across the Indo-West Pacific uncovered by DNA barcoding. Molecular Ecology Resources 13, 32–42.
| Cryptic diversity in flathead fishes (Scorpaeniformes: Platycephalidae) across the Indo-West Pacific uncovered by DNA barcoding.Crossref | GoogleScholarGoogle Scholar |
Rannala, B., and Yang, Z. (2003). Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics 164, 1645–1656.
Rannala, B., and Yang, Z. (2013). Improved Reversible Jump Algorithms for Bayesian Species Delimitation. Genetics 194, 245–253.
| Improved Reversible Jump Algorithms for Bayesian Species Delimitation.Crossref | GoogleScholarGoogle Scholar |
Rivers-Moore, N. A., Goodman, P. S., and Nkosi, M. R. (2007). An assessment of the freshwater natural capital in KwaZulu–Natal for conservation planning. Water S.A. 33, 665–674.
Rivers-Moore, N. A., Goodman, P. S., and Nel, J. L. (2011). Scale-based freshwater conservation planning: towards protecting freshwater biodiversity in KwaZulu‐Natal, South Africa. Freshwater Biology 56, 125–141.
| Scale-based freshwater conservation planning: towards protecting freshwater biodiversity in KwaZulu‐Natal, South Africa.Crossref | GoogleScholarGoogle Scholar |
Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar |
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2, efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2, efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar |
Samways, M. J., Hamer, M., and Veldtman, R. (2012). Development and future of insect conservation in South Africa. In ‘Insect Conservation: Past, Present and Prospects’. pp. 245–278. (Springer: Netherlands.)
Schmitz, G., and Rooyani, F. (1987). ‘Lesotho: Geology, Geomorphology, Soils.’ (National University of Lesotho: Lesotho.)
Schönrogge, K., Barr, B., Wardlaw, J. C., Napper, E., Gardner, M. G., Breen, J., Elmes, G. W., and Thomas, J. A. (2002). When rare species become endangered: cryptic speciation in myrmecophilous hoverflies. Biological Journal of the Linnean Society. Linnean Society of London 75, 291–300.
| When rare species become endangered: cryptic speciation in myrmecophilous hoverflies.Crossref | GoogleScholarGoogle Scholar |
Seidel, R. A., Lang, B. K., and Berg, D. J. (2009). Phylogeographic analysis reveals multiple cryptic species of amphipods (Crustacea: Amphipoda) in Chihuahuan Desert springs. Biological Conservation 142, 2303–2313.
| Phylogeographic analysis reveals multiple cryptic species of amphipods (Crustacea: Amphipoda) in Chihuahuan Desert springs.Crossref | GoogleScholarGoogle Scholar |
Shih, H. T., Yeo, D. C. J., and Ng, P. K. L. (2009). The collision of the Indian plate with Asia: molecular evidence for its impact on the phylogeny of freshwater crabs (Brachyura: Potamidae). Journal of Biogeography 36, 703–719.
Shih, H.-T., Ng, P. K. L., Naruse, T., Shokita, S., and Liu, M.-Y. (2011). Pleistocene speciation of freshwater crabs (Crustacea: Potamidae: Geothelphusa) from northern Taiwan and southern Ryukyus, as revealed by phylogenetic relationships. Zoologischer Anzeiger 250, 457–471.
| Pleistocene speciation of freshwater crabs (Crustacea: Potamidae: Geothelphusa) from northern Taiwan and southern Ryukyus, as revealed by phylogenetic relationships.Crossref | GoogleScholarGoogle Scholar |
Sites, J. W., and Marshall, J. C. (2003). Delimiting species: a Renaissance issue in systematic biology. Trends in Ecology & Evolution 18, 462–470.
| Delimiting species: a Renaissance issue in systematic biology.Crossref | GoogleScholarGoogle Scholar |
Sites, J. W., and Marshall, J. C. (2004). Operational criteria for delimiting species. Annual Review of Ecology Evolution and Systematics 35, 199–227.
| Operational criteria for delimiting species.Crossref | GoogleScholarGoogle Scholar |
Smith, B. T., Ribas, C. C., Whitney, B. M., Hernández-Baños, B. E., and Klicka, J. (2013). Identifying biases at different spatial and temporal scales of diversification: a case study in the Neotropical parrotlet genus Forpus. Molecular Ecology 22, 483–494.
| Identifying biases at different spatial and temporal scales of diversification: a case study in the Neotropical parrotlet genus Forpus.Crossref | GoogleScholarGoogle Scholar |
Swartz, E. R., Skelton, P. H., and Bloomer, P. (2009). Phylogeny and biogeography of the genus Pseudobarbus (Cyprinidae): shedding light on the drainage history of rivers associated with the Cape Floristic Region. Molecular Phylogenetics and Evolution 51, 75–84.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
| MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar |
Teske, P. R., McLay, C. L., Sandoval-Castillo, J., Papadopoulos, I., Newman, B. K., Griffiths, C. L., McQuaid, C. D., Barker, N. P., Borgonie, G., and Beheregaray, L. B. (2009). Tri-locus sequence data reject a “Gondwanan origin hypothesis” for the African/South Pacific crab genus Hymenosoma. Molecular Phylogenetics and Evolution 53, 23–33.
| Tri-locus sequence data reject a “Gondwanan origin hypothesis” for the African/South Pacific crab genus Hymenosoma.Crossref | GoogleScholarGoogle Scholar |
Tsang, L. M., Ma, K. Y., Ahyong, S. T., Chan, T. Y., and Chu, K. H. (2008). Phylogeny of Decapoda using two nuclear protein-coding genes: origin and evolution of the Reptantia. Molecular Phylogenetics and Evolution 48, 359–368.
| Phylogeny of Decapoda using two nuclear protein-coding genes: origin and evolution of the Reptantia.Crossref | GoogleScholarGoogle Scholar |
Wielstra, B., Baird, A. B., and Arntzen, J. W. (2013). A multimarker phylogeography of crested newts (Triturus cristatus superspecies) reveals cryptic species. Molecular Phylogenetics and Evolution 67, 167–175.
| A multimarker phylogeography of crested newts (Triturus cristatus superspecies) reveals cryptic species.Crossref | GoogleScholarGoogle Scholar |
Witt, J. D. S., Threloff, D. L., and Hebert, P. D. N. (2006). DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: implications for desert spring conservation. Molecular Ecology 15, 3073–3082.
| DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: implications for desert spring conservation.Crossref | GoogleScholarGoogle Scholar |
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 |
Zink, R. M., and Barrowclough, G. F. (2008). Mitochondrial DNA under siege in avian phylogeography. Molecular Ecology 17, 2107–2121.
| Mitochondrial DNA under siege in avian phylogeography.Crossref | GoogleScholarGoogle Scholar |