Phylogenetics of the freshwater crab (Potamonautes MacLeay, 1838) fauna from ‘sky islands’ in Mozambique with the description of a new species (Brachyura: Potamoidea: Potamonautidae)

  • Savel R. Daniels Department of Botany and Zoology, Private Bag X1, University of Stellenbosch, Matieland, 7602 http://orcid.org/0000-0003-2956-3256
  • Gabriela B. Bittencourt-Silva Department of Life Sciences, Natural History Museum, London
  • Vanessa Muianga Museu de Historia Natural, Travessia de Zambeze, Maputo
  • Julian Bayliss Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, OX3 0BP
DOI: https://doi.org/10.5852/ejt.2020.716
Keywords: alpha taxonomy, species diversity, novel lineages, sky island, conservation

Abstract

Patterns and processes of cladogenesis among taxa living on the Mozambique ‘sky islands’ remain poorly studied. During the present study, we report on a new freshwater crab species from Mount Lico, an inselberg and ‘sky island’ in the Zambezia Province of Mozambique. Phylogenetic analyses using three mitochondrial DNA sequence loci (12S rRNA, 16S rRNA and COI) were used to determine the evolutionary placement of the freshwater crab specimens from Mount Lico. The freshwater crab specimens from Mount Lico were retrieved sister to Potamonautes choloensis. The new species, Potamonautes licoensis sp. nov., is described and compared with other southern African freshwater crab species. Divergence time estimations for the Mozambican freshwater crab species suggest a Miocene / Plio–Pleistocene diversification. Some endemic ‘sky island’ species form an early branching and are sister to other predominantly East African species, while other ‘sky island’ species are more recently derived and nested within a predominantly southern African clade. The present study presents the description of the fourth endemic freshwater crab species from Mozambique and suggests that the species diversity in the country is likely highly underrepresented, reiterating the call for renewed systematic surveys. An argument for the conservation of these mountainous ‘sky islands’ is presented.

References

Akaike H. 1973. Information theory as an extension of maximum likelihood principle. In: Petrov, B.N., Csake, F (eds) Second International Symposium on Information Theory: 267–281. Akademiai Kaido, Budapest.

Assefa A., Ehrich D., Taberlet P., Nemomissa S. & Brochmann C. 2007. Pleistocene colonization of afro-alpine ‘sky islands’ by the arctic-alpine Arabis alpina. Heredity 99: 133–142. https://doi.org/10.1038/sj.hdy.6800974

Barnes A., Reiss T. & Daniel S.R. 2020. Systematics of the Peripatopsis clavigera species complex (Onycophora: Peripatopsidae) reveals cryptic cladogenic patterning: with the description of five new species. Invertebrate Systematics 34 (6): 569–590. https://doi.org/10.1071/IS19071

Bayliss J., Timberlake J., Branch W., Bruessow C., Collins S., Congdon C., Da Sousa C., Herrmann E., Dowsett R.J., Dowsett-Lemaire F., Fishpool L.D.C., Harris T., Georgiadis S., Liggitt B., Monadjem A., Patel I.H., Ribeiro D., Spottiswoode C.N., Taylor P., Willcock S. & Smith P. 2014. The discovery, biodiversity, and conservation of Mabu forest – the largest mid-altitude rainforest in southern Africa. Oryx 48: 177–185. https://doi.org/10.1017/S0030605313000720

Bayliss J.L., Collins S.C. & Congdon T.C.E. 2016. A new species of Iolaus Hübner, [1819] subgenus Epamera Druce, 1891 (Lepidoptera: Lycaenidae: Theclinae) from Mts Namuli and Mabu, Northern Mozambique. Metamorphosis 27: 23–30.

Bayliss J., Congdon T.C.E. & Collins S.C. 2018. A new subspecies of Papilio (Princeps) pelodurus Butler, 1896 (Lepidoptera: Papilionidae: Papilioninae) from several mountains in northern Mozambique. Metamorphosis 29: 132–136.

Bayliss J., Brattström O., Bampton I. & Collins S.C. 2019. A new species of Leptomyrina Butler, 1898 (Lepidoptera: Lycaenidae) from Mts Mecula, Namuli, Inago, Nallume and Mabu in Northern Mozambique. Metamorphosis 30: 19–24.

Branch W.R. & Bayliss J. 2009. A new species of Atheris (Serpentes: Viperidae) from northern Mozambique. Zootaxa 2113: 41–54. https://doi.org/10.11646/zootaxa.2113.1.2

Branch W.R. & Tolley K.A. 2010. A new species of chameleon (Sauria: Chamaeleonidae: Nadzikambia) from Mount Mabu, central Mozambique. African Journal of Herpetology 59: 157–172. https://doi.org/10.1080/21564574.2010.516275

Branch W.R., Bayliss J. & Tolley K.A. 2014. Pygmy chameleons of the Rhampholeon platyceps complex (Squamata: Chamaeleonidae): description of four new species from isolated ‘sky islands’ of northern Mozambique. Zootaxa 3814: 1–36. https://doi.org/10.11646/zootaxa.3814.1.1

Branch W.R., Bayliss J., Bittencourt-Silva G.B., Conradie W., Engelbrecht H., Loader S.O., Menegon M., Nanvonomaquitxo C. & Tolley K.A. 2019. A new species of tree snake (Dipsadoboa, Serpentes: Colubridae) from ‘sky island’ forest in northern Mozambique, with notes on other members of the Dipsadoboa werneri group. Zootaxa 4646: 541–563. https://doi.org/10.11646/zootaxa.4646.3.6

Bonnefille R. 2010. Cenozoic vegetation, climate changes and hominid evolution in tropical Africa. Global and Planetary Change 72: 390–411. https://doi.org/10.1016/j.gloplacha.2010.01.015

Busschau T., Conradie W. & Daniels S.R. 2019. Evidence for cryptic diversification in a rupicolous forest-dwelling gecko (Gekkonidae: Afroedura pondolia) from a biodiversity hotspot. Molecular Phylogenetics and Evolution 139: 106549. https://doi.org/10.1016/j.ympev.2019.106549

Chace F.A. 1953. Zoological results of a fifth expedition to East Africa. VI. Decapod Crustacea. Bulletin of the Museum of Comparative Zoology 110: 427–443. Available from https://www.biodiversitylibrary.org/page/2817476 [accessed 27 Aug. 2020].

Congdon T.C.E. & Bayliss J. 2012. Butterflies of Mt Mecula and Mt Yao, Niassa Province, Northern Mozambique. Metamorphosis 23: 26–34.

Congdon C., Collins S. & Bayliss J. 2010. Butterflies of south east Africa’s mountains (Mozambique and Malawi). Metamorphosis 21: 45–107.

Conradie W., Bittencourt-Silva G.B., Farooq H.M., Loader S.P., Menegon M. & Tolley K.A. 2018. New species of mongrel frogs (Pyxicephalidae: Nothophryne) for northern Mozambique inselbergs. African Journal of Herpetology 67: 61–85. https://doi.org/10.1080/21564574.2017.1376714

Cumberlidge N., Naskrecki P. & Daniels S.R. 2016. Potamonautes gorongosa, a new species of potamonautid freshwater crab from Mozambique, southern Africa. Nauplius 24: e2016029. https://doi.org/10.1590/2358-2936e2016029

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. https://doi.org/10.1016/j.ympev.2011.07.015

Daniels S.R. 2017. Sympatric colour morphs or distinct species? Examining species boundaries amongst two South African freshwater crabs (Decapoda: Potamonautidae: Potamonautes MacLeay, 1838) with the description of a new species. Journal of Crustacean Biology 37: 723–731. https://doi.org/10.1093/jcbiol/rux087

Daniels S.R. & Bayliss J. 2012. Neglected refugia of biodiversity: mountainous regions in Mozambique and Malawi yield two novel freshwater crab species (Potamonautidae: Potamonautes). Zoological Journal of the Linnean Society 164: 498–509. https://doi.org/10.1111/j.1096-3642.2011.00773.x

Daniels S.R. & Klaus S. 2018. Divergent evolutionary origins and biogeographic histories of two freshwater crabs (Brachyura: Potamonautes) on the West African conveyer belt islands of São Tomé and Príncipe. Molecular Phylogenetics and Evolution 127: 119–128. https://doi.org/10.1016/j.ympev.2018.05.016

Daniels S.R., Stewart B.A. & Cook P.A. 2002a. Congruent patterns of genetic variation in a burrowing freshwater crab revealed by allozyme and mtDNA sequence analysis. Hydrobiologia 468: 171–179. https://doi.org/10.1023/A:1015203909091

Daniels S.R., Stewart B.A., Gouws G., Cunningham M. & Matthee C.A. 2002b. Phylogenetic relationships of the southern African freshwater crab fauna (Decapoda: Potamonautidae: Potamonautes) derived from multiple data sets reveal biogeographic patterning. Molecular Phylogenetics and Evolution 25: 511–523. https://doi.org/10.1016/S1055-7903(02)00281-6

Daniels S.R., Cumberlidge N., Pérez-Losada M., Marijnissen S.A.E. & Crandall K.A. 2006. Evolution of Afrotropical freshwater crab lineages obscured by morphological convergence. Molecular Phylogenetics and Evolution 40: 227–235. https://doi.org/10.1016/j.ympev.2006.02.022

Daniels S.R., Phiri E.E. & Bayliss J. 2014. Renewed sampling of inland aquatic habitats in southern Africa yields two novel freshwater crab species (Decapoda: Potamonautidae: Potamonautes). Zoological Journal of the Linnean Society 171: 356–369. https://doi.org/10.1111/zoj.12139

Daniels S.R., Phiri E.E., Klaus S., Albrecht C. & 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. https://doi.org/10.1093/sysbio/syv011

Daniels S.R., Busschau T. & Cumberlidge N. 2019. Two new species of freshwater crabs of the genus Potamonautes MacLeay, 1838 (Decapoda: Brachyura: Potamonautidae) from the forests of KwaZulu-Natal, South Africa. Journal of Crustacean Biology 39: 426–435. https://doi.org/10.1093/jcbiol/ruz024

Davidson A. & Rex D. 1980. Age of volcanism and rifting in southwestern Ethiopia. Nature 283: 657–658. https://doi.org/10.1038/283657a0

deMenocal P.B. 2004. African climate change and faunal evolution during the Pliocene-Pleistocene. Earth and Planetary Science Letters 220: 3–24. https://doi.org/10.1016/S0012-821X(04)00003-2

Demos T.C., Peterhans J.C.K., Agwanda B. & Hickerson M.J. 2014. Uncovering cryptic diversity and refugial persistence among small mammal lineages across the Eastern Afromontane biodiversity hotspot. Molecular Phylogenetics and Evolution 71: 41–54. https://doi.org/10.1016/j.ympev.2013.10.014

Gouws G., Peer N. & Perissinatto R. 2015. mtDNA lineage diversity of a potamonautid freshwater crab in KwaZulu-Natal, South Africa. Koedoe 57: 1–12. https://doi.org/10.4102/koedoe.v57i1.1324

Hofmeyr M.D., Vamberger M., Branch W., Schleicher A. & Daniels S.R. 2017. Tortoise (Reptilia, Testudinidae) radiations in Southern Africa from the Eocene to the present. Zoologica Scripta 46: 380–400. https://doi.org/10.1111/zsc.12223

Kissling W.D., Eiserhardt W.L., Baker W.J., Borchsenius F., Couvreur T.L.P., Baslev H. & Svenning J-C. 2012. Cenozoic imprints on the phylogenetic structure of palm species assemblages worldwide. Proceedings of the National Academy of Sciences of the United States of America 109: 7379–7384. https://doi.org/10.1073/pnas.1120467109

Mittermeier R.A., Robles P., Hoffman M., Pilgrim J., Brooks T., Mittermeier C.G., Lamoreux J. & da Fonseca G.A.B. 2004. Hotspots Revisited. Earth’s Biologically Richest and Most Endangered Terrestrial Ecoregions. CEMEX, Agrupación Sierra Madre, S.C., Mexico City.

Nielsen S.V., Daniel S.R., Conradie W., Heinicke M.P. & Noonan B.P. 2018. Multilocus phylogenetics in a widespread African anuran lineage (Brevicipitidae: Breviceps) reveals patterns of diversity reflecting geoclimatic change. Journal of Biogeography 45: 2067–2079. https://doi.org/10.1111/jbi.13394

Nylander J.A.A.A., Ronquist F., Huelsenbeck J.P. & Nieves-Aldrey J.L. 2004. Bayesian phylogenetic analysis of combined data. Systematic Biology 53: 47–67. https://doi.org/10.1080/10635150490264699

Peer N., Perissinotto R., Gouws G. & Miranda N.A.F. 2015. Description of a new species of Potamonautes MacLeay, 1838, from the iSimangaliso Wetland Park, South Africa. ZooKeys 503: 23–43. https://doi.org/10.3897/zookeys.503.9532

Peer N., Gouws G., Lazo-Wasem E., Perissinotto R. & Miranda N.A.F. 2017. Redescription of Potamonautes sidneyi (Rathbun, 1904) (Decapoda, Potamonautidae) and description of a new congeneric species from KwaZulu-Natal, South Africa. ZooKeys 657: 1–28. https://doi.org/10.3897/zookeys.657.11623

Phiri E.E. & Daniels S.R. 2013. Hidden in the highlands: the description and phylogenetic positioning of a novel endemic freshwater crab species (Potamonautidae: Potamonautes) from Zimbabwe. Invertebrate Systematics 27: 530–539. https://doi.org/10.1071/IS13012

Phiri E.E. & 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 Linnaean Society 170: 310–332. https://doi.org/10.1111/zoj.12103

Phiri E.E. & Daniels S.R. 2016. Multilocus coalescent species delimitation reveals widespread cryptic differentiation among Drakensberg mountain-living freshwater crabs (Decapoda: Potamonautes). Invertebrate Systematics 30: 60–74. https://doi.org/10.1071/IS15035

Portik D.M., Travers D., Bauer A.M. & Branch W.R. 2013. A new species of Lygodactylus (Squamata: Gekkonidae) endemic to Mount Namuli, an isolated ‘sky island’ of northern Mozambique. Zootaxa 3710: 415–453. https://doi.org/10.11646/zootaxa.3710.5.2

Posada D. 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256. https://doi.org/10.1093/molbev/msn083

Posada D. & Buckley T.R. 2004. Model selection and model averaging in phylogenetics: advantages of the Akaike Information Criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53: 793–808. https://doi.org/10.1080/10635150490522304

Reed S.K. & Cumberlidge N. 2004. Notes on the taxonomy of Potamonautes obesus (A Milne-Edwards, 1868) and Potamonautes calcaratus (Gordon, 1929) (Brachyura: Potamoidea: Potamonautidae) from eastern and southern Africa. Zootaxa 418: 1–20. https://doi.org/10.11646/zootaxa.418.1.1

Ronquist F., Teslenko M., Van Der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029

Rose C., Polissar P.J., Tierney J.E., Filley T. & deMenocal P.B. 2016. Changes in northeast African hydrology and vegetation associated with Pliocene–Pleistocene sapropel cycles. Philosophical Transactions of the Royal Society B 371: 20150243. https://doi.org/10.1098/rstb.2015.0243

Sepulchre P., Ramstein G., Fluteau F., Schuster M., Tiercelin, J-J. & Brunet M. 2006. Tectonic uplift and eastern Africa aridification. Science 313: 1419–1423. https://doi.org/10.1126/science.1129158

Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood based phylogenetic analysis with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690. https://doi.org/10.1093/bioinformatics/btl446

Stewart B.A. 1997. Biochemical and morphological evidence for a new species of river crab Potamonautes parvispina sp. nov. (Brachyura, Potamonautidae). Crustaceana 70: 737–753. https://doi.org/10.1163/156854097X00168

Swofford D.L. 2002. PAUP* Phylogenetic Analysis Using Parsimony (and other methods), Version 4.10. Illinois Natural History Survey, Champaign, Illinois.

Taylor P., Stoffberg S., Monadjem A., Schoema M.C., Bayliss J. & Cotterill F.P.D. 2012. Four new bat species (Rhinolophus hildebrandtii complex) reflect Plio-Pleistocene divergence of dwarfs and giants across an Afromontane archipelago. PLoS ONE, 7: e41744. https://doi.org/10.1371/journal.pone.0041744

Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F. & Higgins D.G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876–4882. https://doi.org/10.1093/nar/25.24.4876

Tolley K.A., Chase B.M. & Forest F. 2008. Speciation and radiations track climate transitions since the Miocene climatic optimum: a case study of southern African chameleons. Journal of Biogeography 35: 1402–1414. https://doi.org/10.1111/j.1365-2699.2008.01889.x

Uno K.T., Polissar P.J., Jackson K.E. & deMenocal P.B. 2016. Neogene biomarker record of vegetation change in eastern Africa. Proceedings of the National Academy of Sciences of the United States of America 113: 6355–6363. https://doi.org/10.1073/pnas.1521267113

Van Velzen R., Collins S.C., Brattström O. & Congdon T.C.E. 2016. Description of a new species of Cymothoe Hübner, 1819 from northern Mozambique (Lepidoptera: Nymphalidae: Limenitidinae). Metamorphosis 27: 34–41.

Wood L.E. & Daniels S.R. 2016. Genetic and morphological evidence for a new mountain-living freshwater crab species (Decapoda: Potamonautidae: Potamonautes) from the Western Cape province of South Africa. Invertebrate Systematics 30: 219–230. https://doi.org/10.1071/IS15051

Published
2020-09-11
How to Cite
Daniels, S. R., Bittencourt-Silva, G. B., Muianga, V., & Bayliss, J. (2020). Phylogenetics of the freshwater crab (Potamonautes MacLeay, 1838) fauna from ‘sky islands’ in Mozambique with the description of a new species (Brachyura: Potamoidea: Potamonautidae). European Journal of Taxonomy, (716). https://doi.org/10.5852/ejt.2020.716
Issue
No. 716 (2020)
Section
Zoology

Copyright (c) 2020 Savel R. Daniels, Gabriela B. Bittencourt-Silva, Vanessa Muianga, Julian Bayliss

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Creative Commons Copyright Notices

Authors who publish with this journal agree to the following terms:

  1. Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY 4.0) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
  2. Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
  3. Authors are NOT PERMITTED to post their submitted work online (e.g., in institutional repositories or on personal websites) prior to publication, as it may lead to nomenclatural issues.