in

Molecular data suggest multiple origins and diversification times of freshwater gammarids on the Aegean archipelago

  • 1.

    Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853 (2000).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 2.

    Whittaker, R. J. & Fernández-Palacios, J. M. Island Biogeography: Ecology, Evolution, and Conservation (Oxford University Press, Oxford, 2007).

    Google Scholar 

  • 3.

    Poulakakis, N. et al. A review of phylogeographic analyses of animal taxa from the Aegean and surrounding regions. J. Zool. Syst. Evol. Res. 53, 18–32 (2015).

    Article  Google Scholar 

  • 4.

    4Woodward, J. The Physical Geography of the Mediterranean. Vol. 8 (Oxford University Press on Demand, 2009).

  • 5.

    De Figueroa, J. M. T., López-Rodríguez, M. J., Fenoglio, S., Sánchez-Castillo, P. & Fochetti, R. Freshwater biodiversity in the rivers of the Mediterranean Basin. Hydrobiologia 719, 137–186 (2013).

    Article  Google Scholar 

  • 6.

    Triantis, K. A. & Mylonas, M. Greek islands biology. In Encyclopedia of Islands (eds Gillespie, R. & Glague, D. A.) 388–392 (University of California Press, Berkeley, CA, 2009).

    Google Scholar 

  • 7.

    Meulenkamp, J. The Neogene in the southern Aegean area. Opera Bot. 30, 5–12 (1971).

    Google Scholar 

  • 8.

    van der Geer, A., Dermitzakis, M. & de Vos, J. Crete before the Cretans: The reign of dwarfs. Pharos 13, 121–132 (2006).

    Google Scholar 

  • 9.

    9Dermitzakis, M. & Papanikolaou, D. In Annales geologiques des pays helleniques. 245–289.

  • 10.

    Perissoratis, C. & Conispoliatis, N. The impacts of sea-level changes during latest Pleistocene and Holocene times on the morphology of the Ionian and Aegean seas (SE Alpine Europe). Mar. Geol. 196, 145–156 (2003).

    ADS  Article  Google Scholar 

  • 11.

    MacNeil, C., Dick, J. T. & Elwood, R. W. The trophic ecology of freshwater Gammarus spp. (Crustacea: Amphipoda): Problems and perspectives concerning the functional feeding group concept. Biol. Rev. 72, 349–364 (1997).

    Article  Google Scholar 

  • 12.

    Kelly, D. W., Dick, J. T. & Montgomery, W. I. The functional role of Gammarus (Crustacea, Amphipoda): Shredders, predators, or both?. Hydrobiologia 485, 199–203 (2002).

    Article  Google Scholar 

  • 13.

    Bilton, D. T., Freeland, J. R. & Okamura, B. Dispersal in freshwater invertebrates. Annu. Rev. Ecol. Syst. 32, 159–181 (2001).

    Article  Google Scholar 

  • 14.

    Hupało, K., Mamos, T., Wrzesińska, W. & Grabowski, M. First endemic freshwater Gammarus from Crete and its evolutionary history—An integrative taxonomy approach. PeerJ 6, e4457 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  • 15.

    Karaman, G. S. & Pinkster, S. Freshwater Gammarus species from Europe, North Africa and Adjacent Regions of Asia (Crustacea-Amphipoda).: Part I. Gammarus pulex-Group and Related Species. Bijdragen tot de Dierkunde 47, 1–97 (1977).

    Article  Google Scholar 

  • 16.

    Karaman, G. S. & Pinkster, S. Freshwater Gammarus species from Europe, North Africa and adjacent regions of Asia (Crustacea-Amphipoda): Part II. Gammarus roeseli-group and related species. Bijdragen tot de Dierkunde 47, 165–196 (1977).

    Article  Google Scholar 

  • 17.

    Karaman, G. S. & Pinkster, S. Freshwater Gammarus Species from Europe, North Africa and Adjacent Regions of Asia (Crustacea-Amphipoda).: Part III. Gammarus balcanicus-Group and Related Species. Bijdragen tot de Dierkunde 57, 207–260 (1987).

    Article  Google Scholar 

  • 18.

    Pinkster, S. A revision of the genus Echinogammarus Stebbing, 1899 with some notes on related genera (Crustacea, Amphipoda). Memorie del Museo Civico di Storia Naturale (IIa serie) Sezione Scienze della Vita (A. Biologia) 10, 1–183 (1993).

    Google Scholar 

  • 19.

    Copilaş-Ciocianu, D. & Petrusek, A. The southwestern Carpathians as an ancient centre of diversity of freshwater gammarid amphipods: Insights from the Gammarus fossarum species complex. Mol. Ecol. 24, 3980–3992 (2015).

    Article  PubMed  Google Scholar 

  • 20.

    Copilaş-Ciocianu, D. & Petrusek, A. Phylogeography of a freshwater crustacean species complex reflects a long-gone archipelago. J. Biogeogr. 44, 421–432 (2017).

    Article  Google Scholar 

  • 21.

    Grabowski, M., Mamos, T., Bącela-Spychalska, K., Rewicz, T. & Wattier, R. A. Neogene paleogeography provides context for understanding the origin and spatial distribution of cryptic diversity in a widespread Balkan freshwater amphipod. PeerJ 5, e3016 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • 22.

    Grabowski, M., Wysocka, A. & Mamos, T. Molecular species delimitation methods provide new insight into taxonomy of the endemic gammarid species flock from the ancient Lake Ohrid. Zool. J. Linn. Soc. 181, 272–285 (2017).

    Google Scholar 

  • 23.

    Hou, Z., Sket, B. & Li, S. Phylogenetic analyses of Gammaridae crustacean reveal different diversification patterns among sister lineages in the Tethyan region. Cladistics 30, 352–365 (2014).

    Article  Google Scholar 

  • 24.

    Katouzian, A.-R. et al. Drastic underestimation of amphipod biodiversity in the endangered Irano-Anatolian and Caucasus biodiversity hotspots. Sci. Rep. 6, 22507 (2016).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 25.

    Mamos, T., Wattier, R., Burzyński, A. & Grabowski, M. The legacy of a vanished sea: A high level of diversification within a European freshwater amphipod species complex driven by 15 My of Paratethys regression. Mol. Ecol. 25, 795–810 (2016).

    Article  PubMed  Google Scholar 

  • 26.

    Mamos, T., Wattier, R., Majda, A., Sket, B. & Grabowski, M. Morphological vs molecular delineation of taxa across montane regions in Europe: The case study of Gammarus balcanicus Schäferna, (Crustacea: Amphipoda). J. Zool. Syst. Evol. Res. 52, 237–248 (2014).

    Article  Google Scholar 

  • 27.

    Hou, Z., Sket, B., Fišer, C. & Li, S. Eocene habitat shift from saline to freshwater promoted Tethyan amphipod diversification. Proc. Natl. Acad. Sci. 108, 14533–14538 (2011).

    ADS  CAS  Article  PubMed  Google Scholar 

  • 28.

    Özbek, M. & Özkan, N. Gökçeada içsularının Amphipoda (Crustacea: Malacostraca) faunası Amphipoda (Crustacea: Malacostraca) fauna of the inland-waters of Gökçeada Island. Ege J. Fish. Aquat. Sci. 34, 63–67 (2017).

    Google Scholar 

  • 29.

    Hillis, D. M., Moritz, C., Mable, B. K. & Olmstead, R. G. Molecular systematics Vol. 23 (Sinauer Associates, Sunderland, 1996).

    Google Scholar 

  • 30.

    Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    CAS  Article  PubMed  Google Scholar 

  • 31.

    Kearse, M. et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  • 32.

    Ratnasingham, S. & Hebert, P. D. BOLD: The Barcode of Life Data System (https://www.barcodinglife.org). Molecular ecology notes 7, 355–364 (2007).

  • 33.

    Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. ABGD, automatic barcode gap discovery for primary species delimitation. Mol. Ecol. 21, 1864–1877 (2012).

    CAS  Article  PubMed  Google Scholar 

  • 34.

    Monaghan, M. T. et al. Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Syst. Biol. 58, 298–311 (2009).

    CAS  Article  PubMed  Google Scholar 

  • 35.

    Pons, J. et al. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst. Biol. 55, 595–609 (2006).

    Article  PubMed  Google Scholar 

  • 36.

    Kapli, P. et al. Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33, 1630–1638 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 37.

    Fourment, M. & Gibbs, M. J. PATRISTIC: A program for calculating patristic distances and graphically comparing the components of genetic change. BMC Evol. Biol. 6, 1 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 38.

    Lefébure, T., Douady, C., Gouy, M. & Gibert, J. Relationship between morphological taxonomy and molecular divergence within Crustacea: Proposal of a molecular threshold to help species delimitation. Mol. Phylogenet. Evol. 40, 435–447 (2006).

    Article  CAS  Google Scholar 

  • 39.

    Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).

    CAS  Article  Google Scholar 

  • 40.

    Bouckaert, R. R. & Drummond, A. J. bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evol. Biol. 17, 42 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • 41.

    Xia, X. DAMBE7: New and improved tools for data analysis in molecular biology and evolution. Mol. Biol. Evol. 35, 1550–1552 (2018).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 42.

    Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. An index of substitution saturation and its application. Mol. Phylogenet. Evol. 26, 1–7 (2003).

    CAS  Article  PubMed  Google Scholar 

  • 43.

    Lanfear, R., Calcott, B., Ho, S. Y. & Guindon, S. PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29, 1695–1701 (2012).

    CAS  Article  PubMed  Google Scholar 

  • 44.

    Bouckaert, R. et al. BEAST 2: A software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, e10003537 (2014).

  • 45.

    Baele, G., Li, W. L. S., Drummond, A. J., Suchard, M. A. & Lemey, P. Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics. Mol. Biol. Evol. 30, 239–243 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 46.

    Drummond, A. J., Ho, S. Y., Phillips, M. J. & Rambaut, A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006).

  • 47.

    Wysocka, A. et al. A tale of time and depth: Intralacustrine radiation in endemic Gammarus species flock from the ancient Lake Ohrid. Zool. J. Linn. Soc. 167, 345–359 (2013).

    Article  Google Scholar 

  • 48.

    Wysocka, A. et al. Origin of the Lake Ohrid gammarid species flock: Ancient local phylogenetic lineage diversification. J. Biogeogr. 41, 1758–1768 (2014).

    Article  Google Scholar 

  • 49.

    Cristescu, M. E., Hebert, P. D. & Onciu, T. M. Phylogeography of Ponto-Caspian crustaceans: A benthic–planktonic comparison. Mol. Ecol. 12, 985–996 (2003).

    CAS  Article  PubMed  Google Scholar 

  • 50.

    Nahavandi, N., Ketmaier, V., Plath, M. & Tiedemann, R. Diversification of Ponto-Caspian aquatic fauna: Morphology and molecules retrieve congruent evolutionary relationships in Pontogammarus maeoticus (Amphipoda: Pontogammaridae). Mol. Phylogenet. Evol. 69, 1063–1076 (2013).

    Article  PubMed  Google Scholar 

  • 51.

    Macdonald Iii, K. S., Yampolsky, L. & Duffy, J. E. Molecular and morphological evolution of the amphipod radiation of Lake Baikal. Mol. Phylogenet. Evol. 35, 323–343 (2005).

    Article  CAS  Google Scholar 

  • 52.

    Mats, V., Shcherbakov, D. Y. & Efimova, I. Late Cretaceous-Cenozoic history of the Lake Baikal depression and formation of its unique biodiversity. Stratigr. Geol. Correl. 19, 404 (2011).

    ADS  Article  Google Scholar 

  • 53.

    Sherbakov, D. Y. On the phylogeny of Lake Baikal amphipods in the light of mitochondrial and nuclear DNA sequence data. Crustaceana 72, 911–919 (1999).

    Article  Google Scholar 

  • 54.

    Copilaş-Ciocianu, D., Sidorov, D. & Gontcharov, A. Adrift across tectonic plates: Molecular phylogenetics supports the ancient Laurasian origin of old limnic crangonyctid amphipods. Organ. Divers. Evol. 19, 191–207 (2019).

    Article  Google Scholar 

  • 55.

    Sigovini, M., Keppel, E. & Tagliapietra, D. Open Nomenclature in the biodiversity era. Methods Ecol. Evol. 7(10), 1217–1225 (2016).

    Article  Google Scholar 

  • 56.

    Ketmaier, V., Argano, R. & Caccone, A. Phylogeography and molecular rates of subterranean aquatic stenasellid isopods with a peri-Tyrrhenian distribution. Mol. Ecol. 12, 547–555 (2003).

    CAS  Article  PubMed  Google Scholar 

  • 57.

    Knowlton, N. & Weigt, L. A. New dates and new rates for divergence across the Isthmus of Panama. Proc. R. Soc. Lond. Ser. B Biol. Sci. 265, 2257–2263 (1998).

    Article  Google Scholar 

  • 58.

    Papadopoulou, A., Anastasiou, I. & Vogler, A. P. Revisiting the insect mitochondrial molecular clock: The mid-Aegean trench calibration. Mol. Biol. Evol. 27, 1659–1672 (2010).

    CAS  Article  PubMed  Google Scholar 

  • 59.

    Hamilton, C. A., Hendrixson, B. E., Brewer, M. S. & Bond, J. E. An evaluation of sampling effects on multiple DNA barcoding methods leads to an integrative approach for delimiting species: A case study of the North American tarantula genus Aphonopelma (Araneae, Mygalomorphae, Theraphosidae). Mol. Phylogenet. Evol. 71, 79–93 (2014).

    CAS  Article  PubMed  Google Scholar 

  • 60.

    Fontaneto, D., Flot, J.-F. & Tang, C. Q. Guidelines for DNA taxonomy, with a focus on the meiofauna. Mar. Biodivers.s 45, 433–451 (2015).

    Article  Google Scholar 

  • 61.

    Yu, G., Rao, D., Matsui, M. & Yang, J. Coalescent-based delimitation outperforms distance-based methods for delineating less divergent species: The case of Kurixalus odontotarsus species group. Sci. Rep. 7, 1–13 (2017).

    Article  CAS  Google Scholar 

  • 62.

    De Queiroz, K. Species concepts and species delimitation. Syst. Biol. 56, 879–886 (2007).

    Article  PubMed  Google Scholar 

  • 63.

    Lagrue, C. et al. Confrontation of cryptic diversity and mate discrimination within G ammarus pulex and G ammarus fossarum species complexes. Freshw. Biol. 59, 2555–2570 (2014).

    Article  Google Scholar 

  • 64.

    Costa, F., Henzler, C., Lunt, D., Whiteley, N. & Rock, J. Probing marine Gammarus (Amphipoda) taxonomy with DNA barcodes. Syst. Biodivers. 7, 365–379 (2009).

    Article  Google Scholar 

  • 65.

    Karaman, G. New data on some gammaridean amphipods (Amphipoda, Gammaridea) from Palearctic. Glasnik Sect. Natl. Sci. Monten Acad. Sci. Arts 15, 20–37 (2003).

    Google Scholar 

  • 66.

    Steininger, F. F. & Rögl, F. Paleogeography and palinspastic reconstruction of the Neogene of the Mediterranean and Paratethys. Geol. Soc. Lond. Spec. Publ. 17, 659–668 (1984).

    ADS  Article  Google Scholar 

  • 67.

    Lefébure, T. et al. Phylogeography of a subterranean amphipod reveals cryptic diversity and dynamic evolution in extreme environments. Mol. Ecol. 15, 1797–1806 (2006).

    Article  CAS  PubMed  Google Scholar 

  • 68.

    Sworobowicz, L. et al. Revisiting the phylogeography of Asellus aquaticus in Europe: Insights into cryptic diversity and spatiotemporal diversification. Freshw. Biol. 60, 1824–1840 (2015).

    Article  Google Scholar 

  • 69.

    Shih, H. T., Yeo, D. C. & Ng, P. K. The collision of the Indian plate with Asia: Molecular evidence for its impact on the phylogeny of freshwater crabs (Brachyura: Potamidae). J. Biogeogr. 36, 703–719 (2009).

    Article  Google Scholar 

  • 70.

    Jesse, R., Grudinski, M., Klaus, S., Streit, B. & Pfenninger, M. Evolution of freshwater crab diversity in the Aegean region (Crustacea: Brachyura: Potamidae). Mol. Phylogenet. Evol. 59, 23–33 (2011).

    Article  PubMed  Google Scholar 

  • 71.

    Szarowska, M., Osikowski, A., Hofman, S. & Falniowski, A. Do diversity patterns of the spring-inhabiting snail Bythinella (Gastropoda, Bythinellidae) on the Aegean Islands reflect geological history?. Hydrobiologia 765, 225–243 (2016).

    Article  Google Scholar 

  • 72.

    Trontelj, P., Machino, Y. & Sket, B. Phylogenetic and phylogeographic relationships in the crayfish genus Austropotamobius inferred from mitochondrial COI gene sequences. Mol. Phylogenet. Evol. 34, 212–226 (2005).

    CAS  Article  PubMed  Google Scholar 

  • 73.

    Szarowska, M., Hofman, S., Osikowski, A. & Falniowski, A. Divergence preceding island formation among Aegean insular populations of the freshwater snail genus Pseudorientalia (Caenogastropoda: Truncatelloidea). Zoolog. Sci. 31, 680–686 (2014).

    Article  PubMed  Google Scholar 

  • 74.

    Previšić, A., Walton, C., Kučinić, M., Mitrikeski, P. T. & Kerovec, M. Pleistocene divergence of Dinaric Drusus endemics (Trichoptera, Limnephilidae) in multiple microrefugia within the Balkan Peninsula. Mol. Ecol. 18, 634–647 (2009).

    Article  CAS  PubMed  Google Scholar 

  • 75.

    Gonçalves, H. et al. Multilocus phylogeography of the common midwife toad, Alytes obstetricans (Anura, Alytidae): Contrasting patterns of lineage diversification and genetic structure in the Iberian refugium. Mol. Phylogenet. Evol. 93, 363–379 (2015).

    Article  PubMed  Google Scholar 

  • 76.

    Rachalewski, M., Banha, F., Grabowski, M. & Anastácio, P. M. Ectozoochory as a possible vector enhancing the spread of an alien amphipod Crangonyx pseudogracilis. Hydrobiologia 717, 109–117 (2013).

    Article  Google Scholar 

  • 77.

    Szarowska, M., Hofman, S., Osikowski, A. & Falniowski, A. Daphniola Radoman, 1973 (Caenogastropoda: Truncatelloidea) at east Aegean islands. Folia Malacologica 22 (2014).

  • 78.

    Hupało, K. et al. Persistence of phylogeographic footprints helps to understand cryptic diversity detected in two marine amphipods widespread in the Mediterranean basin. Mol. Phylogenet. Evol. 132, 53–66 (2019).

    Article  CAS  PubMed  Google Scholar 

  • 79.

    Weiss, M., Macher, J. N., Seefeldt, M. A. & Leese, F. Molecular evidence for further overlooked species within the Gammarus fossarum complex (Crustacea: Amphipoda). Hydrobiologia 721, 165–184 (2014).

    CAS  Article  Google Scholar 

  • 80.

    Hopkins, L. IUCN and the Mediterranean Islands: Opportunities for biodiversity conservation and sustainable use (Gland, Switzerland, International Union for Conservation of Nature, 2002).

    Google Scholar 

  • 81.

    QGIS Development Team. QGIS Geographic Information System. Open source geospatial foundation project. (2016).

  • 82.

    Popov, S. V. et al. Lithological-paleogeographic maps of paratethys: 10 maps late eocene to pliocene. Cour. Forsch Senckenberg 250, 1–46 (2004).

    Google Scholar 


  • Source: Ecology - nature.com

    Researchers using environmental DNA must engage ethically with Indigenous communities

    Commercializing next-generation nuclear energy technology