Cryptic diversity and speciation in endemic Cytherissa (Ostracoda, Crustacea) from Lake Baikal

Abstract

Lake Baikal (Siberia) is the most ancient and deepest of all ancient lakes on Earth. It holds a (mostly endemic) diversity of thousands of animal species, including a speciose radiation of ostracods of the genus Cytherissa. Applying molecular tools to this crustacean group reveals that several morphological species are actually species clusters. Based on combined 16S and 28S DNA sequence data from thirteen classic Cytherissa species and one subspecies sensu Mazepova (1990), we recognize 26 different genetic Cytherissa species, 18 with morphological variation and eight truly cryptic species. These results suggest that the actual specific diversity of Cytherissa in Lake Baikal might easily be double of what is presently known. Baikalian endemic species most likely live in the cradle in which they originated and this opens perspectives to infer modes of speciation. Our current distribution data of Cytherissa species provide first indications for both geographic (lakes basins and shores) and ecological (sediment type, water depth) separation. Our present data thus provide the first steps towards future, rigorous testing of focussed hypotheses on the causality of speciation through either allopatric isolation or parapatric ecological clines.

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References

  1. Altschul, S. F., T. L. Madden, A. A. Schäffer, J. Zhang, Z. Zhang, W. Miller & D. J. Lipman, 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389–3402.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Anseeuw, D., B. Nevado, P. Busselen, J. Snoeks & E. Verheyen, 2012. Extensive introgression among ancestral mtDNA lineages: phylogenetic relationships of the Utaka within the Lake Malawi Cichlid Flock. International Journal of Evolutionary Biology 2012: 865603.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bandelt, H., P. Forster & A. Röhl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.

    CAS  Article  PubMed  Google Scholar 

  4. Bedulina, D. S., V. V. Takhteev, S. G. Pogrebnyak, E. B. Govorukhina, E. V. Madyarova, Y. A. Lubyaga, K. P. Vereshchagina, M. A. Timofeyev & T. Luckenbach, 2014. On Eulimnogammarus messerschmidtii, sp. n. (Amphipoda: Gammaridea) from Lake Baikal, Siberia, with redescription of E. cyanoides (Sowinsky) and remarks on taxonomy of the genus Eulimnogammarus. Zootaxa 3838: 518–544.

    Article  PubMed  Google Scholar 

  5. Beheregaray, L. B. & A. Caccone, 2007. Cryptic biodiversity in a changing world. Journal of Biology 6: 9. doi:10.1186/jbiol60.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Bickford, D., D. J. Lohman, N. S. Sodhi, P. K. L. Ng, R. Meier, K. Winker, K. K. Ingram & A. Das, 2007. Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22: 148–155.

    Article  PubMed  Google Scholar 

  7. Birky, C. W. J. R., 2013. Species detection and identification in sexual organisms using population genetic theory and DNA sequences. PLoS ONE 8: e52544.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Birky, C. W., J. Adams, M. Gemmel & J. Perry, 2010. Using population genetic theory and DNA sequences for species identification in asexual organisms. PLoS ONE 5: e10609.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Birky Jr., C. W. & T. G. Barraclough, 2009. Asexual speciation. In Schön, I., K. Martens & P. van Dijk (eds), Lost sex, the evolutionary biology of parthenogenesis. Springer, Dordrecht: 201–216.

    Google Scholar 

  10. Bode, S. N. S., D. K. Lamatsch, M. J. F. Martins, O. Schmit, J. Vandekerkhove, F. Mezquita, T. Namiotko, G. Rossetti, I. Schön, R. K. Butlin & K. Martens, 2010. Exceptional cryptic diversity and multiple origins of parthenogenesis in a freshwater ostracod. Molecular Phylogenetics and Evolution 5: 542–552.

    Article  Google Scholar 

  11. Brandao Nunes, S., J. Sauer & I. Schön, 2010. Circumantarctic and eurybathid distribution in Southern Ocean benthos? A genetic test using Macrocyprididae (Crustacea, Ostracoda) as model organism. Molecular Phylogeny and Evolution 159: 219–243.

    Google Scholar 

  12. Brown, D. M., R. A. Brenneman, N. J. Georgiadis, K. Koepfli, J. P. Pollinger, B. Mila, E. L. Louis Jr., G. F. Grether, D. K. Jacobs & R. K. Wayne, 2007. Extensive population genetic structure in the giraffe. BMC Biology 5: 57.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Cristescu, M. E., S. J. Adamowicz, J. J. Vaillant & D. G. Haffner, 2010. Ancient lakes revisited: from the ecology to the genetics of speciation. Molecular Ecology 19: 4837–4851.

    Article  PubMed  Google Scholar 

  14. Danielopol, D. L. & J. Tétart, 1990. Morphology of Cytherissa and Cyprideis: supplementary data on the appendages and the karyotype. In Danielopol, D. L., P. Carbonel & J. P. Colin (eds), Cytherissa (Ostracoda)—the Drosophila of palaeolimnology, Vol. 47–48, 55–67. Bulletin de l’Institut de Géologie du Bassin d’Acquitaine, Université Bordeaux, Bordeaux.

    Google Scholar 

  15. Darriba, D., G. L. Taboada, R. Doallo & D. Posada, 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Eldredge, N. & J. Cracraft, 1980. Phylogenetic patterns and the evolutionary process. Columbia University Press, New York.

    Google Scholar 

  17. Elmer, K. R., J. A. Davila & S. C. Lougheed, 2007. Cryptic diversity and deep divergence in an upper Amazonian frog, Eleutherodactylus ockendeni. BMC Evolutionary Biology 7: 247.

    Article  PubMed  Google Scholar 

  18. Fontaneto, D., T. G. Barraclough, K. Chen, C. Ricci & E. A. Herniou, 2008. Molecular evidence for broad-scale distributions in bdelloid rotifers: everything is not everywhere but most things are very widespread. Molecular Ecology 17: 3136–3146.

    CAS  Article  PubMed  Google Scholar 

  19. Genner, M. J. & G. F. Turner, 2011. Ancient hybridization and phenotypic novelty within Lake Malawi’s cichlid fish radiation. Molecular Biology and Evolution 29: 195–206.

    Article  PubMed  Google Scholar 

  20. Guindon, S. & O. Gascuel, 2003. PhyML—a simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696–704.

    Article  PubMed  Google Scholar 

  21. Gustafsson, D. R., D. A. Price & C. Erséus, 2009. Genetic variation in the popular lab worm Lumbriculus variegatus (Annelida: Clitellata: Lumbriculidae) reveals cryptic speciation. Molecular Phylogenetics and Evolution 51: 182–189.

    CAS  Article  PubMed  Google Scholar 

  22. Hall, T. A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symposium Series 41: 95–98.

    CAS  Google Scholar 

  23. Hammer, Ø., D. A. T. Harper & P. D. Ryan, 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1): 9.

    Google Scholar 

  24. Itskovich, V. B., O. V. Kaluzhnaya, E. Veynberg & D. Erpenbeck, 2015. Endemic Lake Baikal sponges from deep water. 1: potential cryptic speciation and discovery of living species known only from fossils. Zootaxa 3990: 123–137.

    Article  PubMed  Google Scholar 

  25. Karanovic, I., 2015. Barcoding of ancient lake ostracods (Crustacea) reveals speciation with extremely low distances. PLoS ONE 10: e0121133.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Katoh, K. & D. M. Standley, 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Koblmüller, S., N. Duftner, K. M. Sefc, M. Aibara, M. Stipacek, M. Blanc, B. Egger & C. Sturmbauer, 2007. Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika—the result of repeated introgressive hybridization. BMC Evolutionary Biology 7: 7.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Koenders, A., K. Martens, S. Halse & I. Schön, 2012. Cryptic species of the Eucypris virens species complex (Ostracoda, Crustacea) have invaded Western Australia. Biological Invasions 14: 2187–2201.

    Article  Google Scholar 

  29. Marrone, F., S. Lo Brutto & M. Arculeo, 2010. Molecular evidence for the presence of cryptic evolutionary lineages in the freshwater copepod genus Hemidiaptomus G.O. Sars, 1903 (Calanoida, Diaptomidae). Hydrobiologia 644: 115–125.

    CAS  Article  Google Scholar 

  30. Martens, K., 1994. Ostracod speciation in ancient lakes: a review. In Martens, K., B. Goddeeris & G. Coulter (eds), Speciation in Ancient Lakes, Advances in Limnology, Vol. 44. Sinauer Associates, Sunderland: 203–222.

    Google Scholar 

  31. Martens, K., 1997. Speciation in ancient lakes. Trends in Ecology and Evolution 12: 177–182.

    CAS  Article  PubMed  Google Scholar 

  32. Martens, K., 2000. Factors affecting the divergence of mate recognition systems in the Limnocytherinae (Crustacea, Ostracoda). Hydrobiologia 419: 83–101.

    Article  Google Scholar 

  33. Martens, K., I. Schön, C. Meisch & D. J. Horne, 2008. Global diversity of ostracods (Ostracoda, Crustacea) in freshwater. Hydrobiologia 595: 185–193.

    Article  Google Scholar 

  34. Martin, P., 1994. Lake Baikal. In Martens, K., B. Goddeeris & G. Coulter (eds), Speciation in Ancient Lakes. Advances in Limnology. Sinauer Associates, Sunderland.

    Google Scholar 

  35. Mayr, E., 1942. Systematics and the Origin of Species. Columbia University Press, New York.

    Google Scholar 

  36. Mayr, E., 1963. Animal Species and Evolution. The Belknap press, Cambridge.

    Google Scholar 

  37. Mazepova, G., 1990. Rakushokovye ratchki (Ostracoda) Baikala Nauk. Sib. Otdel. Akad. Nauk SSR, Novosibirsk: 1–470.

    Google Scholar 

  38. Mazepova, G. F., 1998. List of Ostracoda species. In Kozhova, O. M. & L. R. Izmest’eva (eds), Lake Baikal Evolution and Biodiversity. Backhuys Publishers, Leiden: 371–377.

    Google Scholar 

  39. Mazepova, G. F., 2006. Ostracoda of Lake Hövsgöl, Mongolia. In Goulden, C. E., T. Sitnikova, J. Gelhaus & B. Boldgiv (eds), The Geology. Biodiversity and Ecology of Lake Hövsgöl (Mongolia). Backhys Publisher, Leiden: 217–232.

    Google Scholar 

  40. Meier, J. I., D. A. Marques, S. Mwaiko, C. E. Wagner, L. Excoffier & O. Seehausen, 2017. Ancient hybridization fuels cichlid fish adaptive radiations. Nature Communications 8: 14363.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Meyer, B. S., M. Matschiner & W. Salzburger, 2015. A tribal level phylogeny of Lake Tanganyika cichlid fishes based on a genomic multi-marker approach. Molecular Phylogenetics and Evolution 83: 56–71.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Michel, E., A. S. Cohen, K. West, M. R. Johnston & P. W. Kat, 1992. Large African lakes as natural laboratories for evolution: examples from the endemic gastropod fauna of Lake Tanganyika. Mitteilungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 23: 85–99.

    Google Scholar 

  43. Müller, J., H. Oberhänsli, M. Melles, M. Schwab, V. Rachold & H.-W. Hubberten, 2001. Late Pliocene sedimentation in Lake Baikal: implications for climatic and tectonic change in SE Siberia. Palaeogeography, Palaeoclimatololgy and Palaeoecology 174: 305–326.

    Article  Google Scholar 

  44. Muschick, M., A. Indermaur & W. Salzburger, 2012. Convergent evolution within an adaptive radiation of cichlid fishes. Current Biology 22: 2362–2368.

    CAS  Article  PubMed  Google Scholar 

  45. Nevado, B., S. Koblmüller, C. Sturmbauer, J. Snoeks, J. Usano-Alemany & E. Verheyen, 2009. Complete mitochondrial DNA replacement in a Lake Tanganyika cichlid fish. Molecular Ecology 18: 4240–4255.

    CAS  Article  PubMed  Google Scholar 

  46. Nevado, B., T. Backeljau, M. Hanssens & E. Verheyen, 2011. Repeated unidirectional introgression of nuclear and mitochondrial DNA between four congeneric Tanganyikan cichlids. Molecular Biology and Evolution 28: 2253–2267.

    CAS  Article  PubMed  Google Scholar 

  47. Pfenninger, M. & K. Schwenk, 2007. Cryptic animal species are homogeneously distributed along taxa and biogeographic regions. BMC Evolutionary Biology 7: 121.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Poulin, R. & G. Pérez-Ponce de León, 2017. Global analysis reveals that cryptic diversity is linked with habitat but not mode of life. Journal of Evolutionary Biology 30: 641–649. doi:10.1111/jeb.13034.

  49. Puillandre, N., A. Lambert, S. Brouillet & G. Achaz, 2012. ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology 21: 1864–1877.

    CAS  Article  PubMed  Google Scholar 

  50. Rambaut, A., 2017. Figtree, a graphical viewer of phylogenetic trees. http://tree.bio.ed.ac.uk/software/figtree.

  51. Ronquist, F., M. Teslenko, P. van der Mark, D. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M. A. Suchard & J. P. Huelsenbeck, 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Rüber, L., E. Verheyen & A. Meyer, 1999. Replicated evolution of trophic specializations in an endemic cichlid fish lineage from Lake Tanganyika. Proceedings of the National Academy of Sciences USA 96: 10230–10235.

    Article  Google Scholar 

  53. Rüber, L., A. Meyer, C. Sturmbauer & E. Verheyen, 2001. Population structure in two sympatric species of the Lake Tanganyika cichlid tribe Eretmodini: evidence for introgression. Molecular Ecology 10: 1207–1225.

    Article  PubMed  Google Scholar 

  54. Schön, I. & K. Martens, 2004. Adaptive, preadaptive and non-adaptive components of radiations in ancient lakes: a review. Organisms, Diversity and Evolution 4: 137–156.

    Article  Google Scholar 

  55. Schön, I. & K. Martens, 2012. Molecular analyses of ostracod flocks from Lake Baikal and Lake Tanganyika. Hydrobiologia 682: 91–110.

    Article  Google Scholar 

  56. Schön, I. & K. Martens, 2016. Ostracod (Ostracoda, Crustacea) genomics – promises and challenges. Marine Genomics 29: 19–25.

    Article  PubMed  Google Scholar 

  57. Schön, I., R. K. Butlin, H. I. Griffiths & K. Martens, 1998. Slow molecular evolution in an ancient asexual ostracod. Proceedings of the Royal Society of London Series B 265: 235–242.

    Article  Google Scholar 

  58. Schön, I., E. Verheyen & K. Martens, 2000. Speciation in ancient lake ostracods: comparative analysis of Baikalian Cytherissa and Tanganyikan Cyprideis. Mitteilungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 27: 2674–2681.

    Google Scholar 

  59. Schön, I., K. Martens, K. Van Doninck & R. K. Butlin, 2003. Evolution in the slow lane: molecular rates of evolution in sexual and asexual ostracods (Crustacea: Ostracoda). Biological Journal of the Linnean Society 79: 93–100.

    Article  Google Scholar 

  60. Schön, I., K. Martens & S. Halse, 2010. Genetic diversity in Australian ancient asexual Vestalenula (Ostracoda, Darwinulidae)—little variability down-under. Hydrobiologia 641: 59–70.

    Article  Google Scholar 

  61. Schön, I., R. Pinto, S. Halse, A. Smith, K. Martens & C. W. Birky, 2012. Cryptic diversity in putative ancient asexual darwinulids (Crustacea: Ostracoda). PLoS ONE 7: e39844.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Schön, I., C. Poux, E. Verheyen & K. Martens, 2014. High cryptic diversity and persistent lineage segregation in endemic Romecytheridea (Crustacea, Ostracoda) from the ancient Lake Tanganyika. Hydrobiologia 739: 119–131.

    Article  Google Scholar 

  63. Sherbakov, D. Y., 1999. Molecular phylogenetic studies on the origin of biodiversity in Lake Baikal. Trends in Ecology and Evolution 14: 92–95.

    Article  Google Scholar 

  64. Sherstyankin, P. P. & L. N. Kuimova, 2006. Hydrophysical processes in Lake Baikal in its transition from subtropical to modern climates. Hydrobiologia 568(S): 253–257.

    Article  Google Scholar 

  65. Snoeks, J., L. Rüber & E. Verheyen, 1994. The Tanganyika problem: comments on the taxonomy and distribution patterns of its cichlid fauna. Archiv für Hydrobiologie, Beihefte Ergebnisse der Limnologie 44: 355–372.

    Google Scholar 

  66. Sonnenberg, R., A. W. Nolte & D. Tautz, 2007. An evaluation of LSU rDNA D1-D2 sequences for their use in species identification. Frontiers in Zoology 4: 6.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Sturmbauer, C., S. Baric, W. Salzburger, L. Rüber & E. Verheyen, 2001. Lake level fluctuations synchronize genetic divergences of cichlid fishes in African lakes. Molecular Biology and Evolution 18: 144–154.

    CAS  Article  PubMed  Google Scholar 

  68. Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. Tang, C. Q., F. Leasi, U. Obertegger, A. Kieneke, T. G. Barraclough & D. Fontaneto, 2012. The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proceedings of the National Academy of Sciences of the United States of America 109: 16208–16212.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  70. Timoshkin, O. A., 2001. Lake Baikal: diversity of fauna, problems of its immiscibility and origin, ecology and ‘exotic’ communities. In Timoshkin, O. A. (ed.), Index of animal species inhabiting Lake Baikal and its catchment area. Nauka, Novosibirsk: 74–113.

    Google Scholar 

  71. Tsukagoshi, A., 1988. Reproductive character displacement in the ostracod genus Cythere. Journal of Crustacean Biology 8: 563–575.

    Article  Google Scholar 

  72. Vaidya, G., D. J. Lohman & R. Meier, 2011. SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27: 171–180.

    Article  Google Scholar 

  73. Vainola, R. & R. M. Kamaltynov, 1999. Species diversity and speciation in the endemic amphipods of Lake Baikal: molecular evidence. Crustaceana 72: 945–956.

    Article  Google Scholar 

  74. Vogler, A. P. & M. T. Monaghan, 2007. Recent advances in DNA taxonomy. Journal for Zoological Systematics and Evolutionary Research 45: 1–10.

    Article  Google Scholar 

  75. Wagner, C. E., L. J. Harmon & O. Seehausen, 2012. Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487: 366–369.

    CAS  Article  PubMed  Google Scholar 

  76. Zhang, J., P. Kapli, P. Pavlidis & A. Stamatakis, 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was funded by the Intra European Marie Curie Fellowship CRYSTAL (Cryptic ostracod species in an Ancient Lake: the Cytherissa flock from Baikal, contract: PIEF-GA-2009-253767) and a SYNTHESYS grant to VP. DS acknowledges the RBFBR grant 15-04-03848 for funding. We also acknowledge the ESF EUROCHORES programme Eurodiversity for funding the MOLARCH project (05_EDIV_FP237-MOLARCH), of which Erik Verheyen (Brussels, Belgium) was the coordinator. We thank Julian Cillis (Brussels, Belgium) for technical assistance with SEM images and Janet Higuchi (Maringa, Brazil) for assembling the figure with the SEM pictures. Zohra Elouaazizi is gratefully acknowledged for assistance with DNA sequencing. We also acknowledge our Russian colleagues, foremost M. Grachev and O. Timoshkin, for their support during sampling and the visits of KM and VP to Irkutsk. We also wish to thank the members of the molecular lab and of the Freshwater Biology team in Brussels for their help and assistance, especially Tasnim Patel and Marie Cours. We also thank two referees for their useful comments.

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Correspondence to Isa Schön.

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Isa Schön and Valentina Pieri share the position as first authors.

Guest editors: Koen Martens, Sidinei M. Thomaz, Diego Fontaneto & Luigi Naselli-Flores / Emerging Trends in Aquatic Ecology II.

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Schön, I., Pieri, V., Sherbakov, D.Y. et al. Cryptic diversity and speciation in endemic Cytherissa (Ostracoda, Crustacea) from Lake Baikal. Hydrobiologia 800, 61–79 (2017). https://doi.org/10.1007/s10750-017-3259-3

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Keywords

  • Allopatric speciation
  • Parapatric speciation
  • Depth distribution
  • Sediment types
  • Lake basins
  • East–west shores
  • Sexual reproduction