Abstract
Previous phylogenetic investigations on the mayfly Baetis rhodani Pictet from several European countries, excluding Italy, strongly suggested the presence of cryptic species. Our paper reports a DNA-taxonomy phylogenetic analysis of B. rhodani with additional populations coming from Italian and UK sites, and aims to identify potential cryptic species with a coalescent-based method (GMYC model) and to understand the mechanisms of local coexistence of cryptic species. Twenty-five haplotypes of Italian samples and five haplotypes of UK samples were identified and added to a large European dataset. A total of 11 potential cryptic species have been recognised, and three of them co-occured in one Italian area. Such cryptic species seem to be phylogenetically over-dispersed on the tree and temporally segregated, and the seasonal substitution pattern of cryptic species could explain the apparently widespread distribution of the B. rhodani complex and its ability to adapt to different temperatures and food resources, justifying some of the differences observed in the relationship between water temperature, growth rates and phenology documented from field studies.
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References
Alba-Tercedor, J., 1986. Ecologa Distribucin y Ciclos de Desarrollo de Efemerpteros de Sierra Nevada (Granada, Espaa). II: Baetidae (Insecta: Ephemeroptera). Limnetica 1: 234–246.
Baekken, T., 1981. Growth patterns and food habits of and in a west Norwegian river. Holarctic Ecology 4: 139–144.
Baird, D. J. & B. W. Sweeney, 2011. Applying DNA barcoding in benthology: the state of the science. Journal of the North American Benthological Society 30(1): 122–124.
Ball, S. L. & D. N. Hebert, 2005. Biological identifications of mayflies (Ephemeroptera) using DNA barcodes. Journal of North American Benthological Society 24: 508–524.
Benech, V., 1972. Le polyvoltinisme chez Baetis rhodani Pictet (Insecta, Ephemeroptera) dans un ruisseau a truites des Pyrenees-Atlantiques, le Lissuraga. Annales de Hydrobiologie 3: 141–171.
Brittain, J. E., 1982. Biology of mayflies. Annual Review of Entomology 27: 119–147.
Buckley, T. R., C. Simon & G. K. Chambers, 2001. Phylogeography of the New Zealand Cicada Maoricicada campbelli based on mitochondrial DNA sequences: ancient clades associated with cenozoic environmental change. Evolution 55: 1395–1407.
Buffagni, A. & T. Gomba, 1996. Larval development and ecology of Baeti liebenauae Keffermüller (Ephemeroptera: Baetidae) in a north Italian lowland spring. Annales de Limnologie 32(4): 221–228.
Caterino, M. S. & F. A. H. Sperling, 1999. Papilio phylogeny based on mitochondrial cytochrome oxidase I and II genes. Molecular Phylogenetics and Evolution 11: 122–137.
Cavender-Bares, J., K. H. Kozak, P. V. A. Fine & S. W. Kembel, 2009. The merging of community ecology and phylogenetic biology. Ecology Letters 12: 693–715.
Chippindale, P. T., V. K. Dave, D. H. Whitmore & J. V. Robinson, 1999. Phylogenetic relationships of North American Damselflies of the genus Ischnura (Odonata: Zygoptera: Coenagrionidae) based on sequences of three mitochondrial genes. Molecular Phylogenetics and Evolution 11: 110–121.
Clement, M., D. Posada & K. A. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1660.
DeWalt, R. E., 2011. DNA barcoding: a taxonomic point of view. Journal of the North American Benthological Society 30(1): 174–181.
Eaton, A. E., 1871. A Monograph of the Ephemeridae. Transactions of the Entomological Society of London 1–64.
Elliott, J. M., 1972. Effect of temperature on the time of hatching in Baetis rhodani (Ephemeroptera, Baetidae). Oecologia 9: 47–51.
Elliott, J. M., U. H. Humpesch & T. T. Macan, 1988. Larvae of the British Ephemeroptera: A Key with Ecological Notes. Freshwater Biological Association Scientific Publication No. 49. Cumbria, England.
Erba, S., L. Melissano & A. Buffagni, 2003. Life cycles of Baetidae (Insecta: Ephemeroptera) in a North Italian Prealpine stream. In Gaino, E. (ed.), Research Update on Ephemeroptera and Plecoptera. Università di Perugia, Perugia: 177–186.
Excoffier, L., G. Laval & S. Schneider, 2005. Arlequin ver. 3.1: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50.
Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology Biotechnology 3(5): 294–299.
Fontaneto, D., E. A. Herniou, C. Boschetti, M. Caprioli, G. Melone, C. Ricci & T. G. Barraclough, 2007. Evidence for independently evolving species in bdelloid rotifers. PLoS Biology 5: 914–921.
Gaino, E., 1987. Aquatic stages in the development of Habrophlebia eldae Jacob & Sartori, 1984. Genova 119(2): 81–90.
Gattolliat, J. & M. Sartori, 2008. What is Baetis rhodani (Pictet, 1843) (Insecta, Ephemeroptera, Baetidae)? Designation of a neotype and redescription of the species from its original area. Zootaxa 1957: 69–80.
Guindon, S. & O. Gascuel, 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematics Biology 52: 696–704.
Hewitt, G. M., 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society. Linnean Society of London 58: 247–276.
Humpesch, U. H., 1979. Life cycles and growth rates of Baetis spp. (Ephemeroptera: Baetidae) in the laboratory and in two stony streams in Austria. Freshwater Biology 9: 467–479.
Keane, T. M., C. J. Creevey, M. M. Pentony, T. J. Naughton & J. O. McInerney, 2006. Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evolutionary Biology 6: 29.
Kembel S.W., 2010. An introduction to the picante package. [available on internet at http://picante.r-forge.r-project.org/picante-intro.pdf].
Kembel, S. W., P. D. Cowan, M. R. Helmus, W. K. Cornwell, H. Morlon, D. D. Ackerly, S. P. Blomberg & C. O. Webb, 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26: 1463–1464.
Landry, B., J. A. Powell & F. A. H. Sperling, 1999. Systematics of the Argyrotaenia franciscana (Lepidoptera: Tortricidae) species group: evidence from mitochondrial DNA. Annals of the Entomological Society of America 92: 40–46.
Logan, J. A., 1999. Extraction, polymerase chain reaction, and sequencing of a 440 base pair region of the mitochondrial cytochrome oxidase I gene from two species of acetone-preserved Damselflies (Odonata: Coenagrionidae, Agrionidae). Environmental Entomology 28: 143–147.
Lohse, K., 2009. Can mtDNA Barcodes Be Used to Delimit Species? A Response to Pons et al. (2006). Systematic Biology 58(4): 439–442.
Lucentini, L., S. Caporali, A. Palomba, H. Lancioni & F. Panara, 2006. A comparison of conservative DNA extraction methods from fins and scales of freshwater fish: a useful tool for conservation genetics. Conservation genetics 7: 1009–1012.
Lugo-Ortiz, C. R. & W. P. McCafferty, 1998. A new Baetis-complex genus (Ephemeroptera: Baetidae) from the Afrotropical region. African Entomology : Journal of the Entomological Society of Southern Africa 6: 297–301.
Martins, J. Jr., S. E. Solomon, A. S. Mikheyev, U. G. Mueller, A. Ortiz & M. Bacci Jr, 2007. Nuclear mitochondrial-like sequences in ants: evidence from Atta cephalotes (Formicidae: Attini). Insect Molecular Biology 6: 777–784.
Moulton, M. J., H. Song & M. F. Whiting, 2010. Assessing the effects of primer specificity on eliminating numt co-amplification in DNA barcoding: a case study from Orthoptera (Arthropoda: Insecta). Molecular Ecology Resources 10: 615–627.
Müller-Liebenau, I., 1969. Revision der Europäischen Arten der Gattung Baetis Leach, 1815 (Insecta: Ephemeroptera). Gewässer und Abwässer 48(49): 1–214.
Nixon, K. C. & Q. D. Wheeler, 1990. An amplification of the phylogenetic species concept. Cladistics 6(3): 211–223.
Pictet, F. J., 1843–1845. Histoire Naturelle des Insectes Nevropteres. Famille des Ephemerines, Geneve.
Plague, G. R., M. Mulvey, T. C. Glenn & J. V. McArthur, 2001. Molecular genetic markers provide no evidence for reproductive isolation among retreat building phenotypes of the net-spinning caddisfly Macrostemum carolina. Molecular Ecology 10: 243–248.
Pons, J., T. G. Barraclough, J. Gomez-Zurita, A. Cardoso, D. P. Duran, S. Hazell, S. Kamoun, W. D. Sumlin & M. J. Sanderson, 2002. Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach. Molecular Biology and Evolution 19: 101–109.
Rebora, M., L. Lucentini, A. Palomba, F. Panara & E. Gaino, 2005. Genetic differentiation among populations of Baetis rhodani (Ephemeroptera, Baetidae) in three Italian streams. The Italian Journal of Zoology 72: 121–126.
Ronquist, F. & J. P. Huelsenbeck, 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
Rosillon, D., 1986. Life cycles of four ephemeropteran species in a chalky stream. Polskie Archiwum Hydrobiologii 33: 21–31.
Ross, K. G., M. J. B. Krieger, D. D. Shoemaker, E. L. Vargo & L. Keller, 1997. Hierarchical analysis of genetic structure in native fire ant populations: results from three classes of molecular markers. Genetics 147: 643–655.
Sand, K. & J. E. Brittain, 2009. Life cycle shift in Baetis rhodani (Ephemeroptera) in the Norwegian mountains. Aquatic Insects 31: 283–291.
Schultheis, A., A. C. Hendricks & L. A. Weigt, 2002. Genetic evidence for ‘leaky’ cohorts in the semivoltine stonefly Peltoperla tarteri (Plecoptera: Peltoperlidae). Freshwater Biology 47: 367–376.
Simon, C., F. Frati, A. Beckenbach, B. Crespi, H. Liu & P. Flook, 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87: 651–701.
Smith, M. A., N. E. Woodley, D. H. Janzen, W. Hallwachs & P. D. Hebert, 2006. DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Proceedings of the National Academy of Sciences of the United States of America 103: 3657–3662.
Ståhls, G. & E. Savolainen, 2008. MtDNA COI barcodes reveal cryptic diversity in the Baetis vernus group (Ephemeroptera, Baetidae). Molecular Phylogenetics and Evolution 46: 82–87.
Sweeney, B. W., J. M. Battle, J. K. Jackson & T. Dapkey, 2011. Can DNA barcodes of stream macroinvertebrates improve descriptions of community structure and water quality? Journal of the North American Benthological Society 30: 195–216.
Tajima, F., 1989. Statistical methods to test for nucleotide mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.
Tamura, K., M. Nei & S. Kumar, 2007. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences (USA) 101: 11030–11035.
Trewick, S. A., 2000. Molecular evidence for dispersal rather than vicariance as the origin of flightless insect species on the Chatham Islands, New Zealand. Journal of Biogeography 27: 1189–1200.
Ulfstrand, S., 1968. Life cycles of benthic insects in Lapland streams (Ephemeroptera, Plecoptera, Trichoptera, Diptera Simuliidae). Oikos 19: 167–190.
Vamosi, S. M., S. B. Heard, J. C. Vamosi & C. O. Webb, 2009. Emerging patterns in the comparative analysis of phylogenetic community structure. Molecular Ecology 18: 572–592.
Webb, C., D. Ackerly, M. McPeek & M. Donoghue, 2002. Phylogenies and community ecology. Annual Review of Ecology and Systematics 33: 475–505.
Williams, D. D. & D. W. Feltmate, 1992. Chapter 5: Life history and habitat. In Aquatic Insects. CAB International, Wallingford: 158–174.
Williams, H. C., S. J. Ormerod & M. W. Bruford, 2006. Molecular systematics and phylogeography of the cryptic species complex Baetis rhodani (Ephemeroptera, Baetidae). Molecular Phylogenetics and Evolution 40: 370–382.
Acknowledgments
The authors are grateful to Francesco La Piana for collecting Sicilian specimens. This work was supported by National Project FISR-MICENA 2006-2009.
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Lucentini, L., Rebora, M., Puletti, M.E. et al. Geographical and seasonal evidence of cryptic diversity in the Baetis rhodani complex (Ephemeroptera, Baetidae) revealed by means of DNA taxonomy. Hydrobiologia 673, 215–228 (2011). https://doi.org/10.1007/s10750-011-0778-1
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DOI: https://doi.org/10.1007/s10750-011-0778-1