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High levels of genetic structuring in the Antarctic springtail Cryptopygus terranovus

Published online by Cambridge University Press:  08 February 2017

Antonio Carapelli ,
Chiara Leo  and
Francesco Frati
Antonio Carapelli*
Affiliation:
Department of Life Sciences, University of Siena, Via Aldo Moro 2, 53100, Siena, Italy
Chiara Leo
Affiliation:
Department of Life Sciences, University of Siena, Via Aldo Moro 2, 53100, Siena, Italy
Francesco Frati
Affiliation:
Department of Life Sciences, University of Siena, Via Aldo Moro 2, 53100, Siena, Italy
*
[email protected]
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Abstract

Previous work focused on allozymes and mitochondrial haplotypes has detected high levels of genetic variability between Cryptopygus terranovus populations, a springtail species endemic to Antarctica, until recently named Gressittacantha terranova. This study expands these biogeographical surveys using additional analytical techniques, providing a denser haplotype dataset and a wider sampling of localities. Specimens were collected from 11 sites across Victoria Land and sequenced for the cytochrome c oxidase subunit I mitochondrial gene (cox1). Haplotypes were used for population genetics, demographic, molecular clock and Bayesian phylogenetic analyses. Landscape distribution and clustering of haplotypes were also examined for the first time in this species. Only three (out of 67) haplotypes are shared among populations, suggesting high genetic structure and limited gene flow between sites. As in previous studies, the population of Apostrophe Island has a closer genetic similarity with those of the central sites, rather than with its neighbours. Molecular clock estimates point to early differentiation of haplotypes in the late/mid-Miocene, also supporting the view that C. terranovus is a relict species that survived on the Antarctic continent during the Last Glacial Maximum. The present genetic composition of populations represents a mixture of ancient and more recent haplotypes, sometimes occurring in the same localities.

Keywords

AntarcticabiogeographyCollembolacox1 haplotypesVictoria Land
Type
Biological Sciences
Information
Antarctic Science , Volume 29 , Issue 4 , August 2017 , pp. 311 - 323
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Copyright
© Antarctic Science Ltd 2017 

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References

Brower, A.V.Z. 1994. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proceedings of the National Academy of Sciences of the United States of America, 91, 6491–6495.Google Scholar
Chown, S.L. & Convey, P. 2007. Spatial and temporal variability across life’s hierarchies in the terrestrial Antarctic. Philosophical Transactions of the Royal Society - Biological Sciences, B362, 2307–2331.Google Scholar
Clement, M., Posada, D. & Crandall, K.A. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.CrossRefGoogle ScholarPubMed
Convey, P., Stevens, M.I., Hodgson, D.A., Smellie, J.L., Hillenbrand, C.D., Barnes, D.K.A., Clarke, A., Pugh, P.J.A., Linse, K. & Cary, S.C. 2009. Exploring biological constraints on the glacial history of Antarctica. Quaternary Science Reviews, 28, 3035–3048.Google Scholar
Convey, P., Chown, S.L., Clarke, A., Barnes, D.K.A., Bokhorst, S., Cummings, V., Ducklow, H.W., Frati, F., Green, T.G.A., Gordon, S., Griffiths, H.J., Howard-Williams, C., Huiskes, A.H.L., Laybourn-Parry, J., Lyons, W.B., McMinn, A., Morley, S.A., Peck, L.S., Quesada, A., Robinson, S.A., Schiaparelli, S. & Wall, D.H. 2014. The spatial structure of Antarctic biodiversity. Ecological Monographs, 84, 203–244.Google Scholar
Corander, J. & Tang, J. 2007. Bayesian analysis of population structure based on linked molecular information. Mathematical Biosciences, 205, 19–31.Google Scholar
Excoffier, L., Laval, G. & Schneider, S. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics, 1, 47–50.Google Scholar
Excoffier, L., Smouse, P.E. & Quattro, J.M. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479–491.Google Scholar
Fanciulli, P.P., Summa, D., Dallai, R. & Frati, F. 2001. High levels of genetic variability and population differentiation in Gressittacantha terranova (Collembola, Hexapoda) from Victoria Land, Antarctica. Antarctic Science, 13, 246–254.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.Google Scholar
Fraser, C.I., Nikula, R., Ruzzante, D.E. & Waters, J.M. 2012. Poleward bound: biological impacts of Southern Hemisphere glaciation. Trends in Ecology and Evolution, 27, 462–471.CrossRefGoogle ScholarPubMed
Fraser, C.I., Terauds, A., Smellie, J., Convey, P. & Chown, S.L. 2014. Geothermal activity helps life survive glacial cycles. Proceedings of the National Academy of Sciences of the United States of America, 111, 5634–5639.Google Scholar
Goodall-Copestake, W.P., Tarling, G.A. & Murphy, E.J. 2012. On the comparison of population-level estimates of haplotype and nucleotide diversity: a case study using the gene cox1 in animals. Heredity, 109, 50–56.Google Scholar
Greenslade, P. 1995. Collembola from the Scotia Arc and Antarctic Peninsula including description of two new species and notes on biogeography. Polskie Pismo Entomologiczne, 64, 305–319.Google Scholar
Greenslade, P. 2010. Collembola fauna of the South Shetland Islands revisited. Antarctic Science, 22, 233–242.CrossRefGoogle Scholar
Greenslade, P. 2015. Synonymy of two monobasic Anurophorinae genera (Collembola: Isotomidae) from the Antarctic continent. New Zealand Entomologist, 38, 134–141.Google Scholar
Guillot, G., Estoup, A., Mortier, F. & Cosson, J.F. 2005. A spatial statistical model for landscape genetics. Genetics, 170, 1261–1280.Google Scholar
Hawes, T.C., Torricelli, G. & Stevens, M.I. 2010. Haplotype diversity in the Antarctic springtail Gressittacantha terranova at fine spatial scales – a Holocene twist to a Pliocene tale. Antarctic Science, 22, 766–773.Google Scholar
Hawes, T.C., Worland, M.R., Bale, J.S. & Convey, P. 2008. Rafting in Antarctic Collembola. Journal of Zoology, 274, 44–50.CrossRefGoogle Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L. & DeWaard, J.R. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society - Biological Sciences, B270, 313–321.CrossRefGoogle Scholar
Lanfear, R., Calcott, B., Ho, S.Y.W. & Guidon, S. 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.Google Scholar
Librado, P. & Rozas, J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.CrossRefGoogle ScholarPubMed
Maddison, D.R. & Maddison, W.P. 2005. MacClade 4: analysis of phylogeny and character evolution, version 4.08a. Sunderland, MA: Sinauer Associates.Google Scholar
Mantel, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Research, 27, 209–220.Google Scholar
McGaughran, A., Hogg, I.D. & Stevens, M.I. 2008. Patterns of population genetic structure for springtails and mites in southern Victoria Land, Antarctica. Molecular Phylogenetics and Evolution, 46, 606–618.Google Scholar
McGaughran, A., Stevens, M.I., Hogg, I.D. & Carapelli, A. 2011. Extreme glacial legacies: a synthesis of the Antarctic springtail phylogenetic record. Insects, 2, 62–82.Google Scholar
McGaughran, A., Torricelli, G., Carapelli, A., Frati, F., Stevens, M.I., Convey, P. & Hogg, I.D. 2010. Contrasting phylogeographical patterns for springtails reflect different evolutionary histories between the Antarctic Peninsula and Continental Antarctica. Journal of Biogeography, 37, 103–119.Google Scholar
Nei, M. 1987. Molecular evolutionary genetics. New York, NY: Columbia University Press, 522 pp.CrossRefGoogle Scholar
Nei, M. & Li, W.H. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences of the United States of America, 76, 5269–5273.Google Scholar
Pugh, P.J.A. & Convey, P. 2008. Surviving out in the cold: Antarctic endemic invertebrates and their refugia. Journal of Biogeography, 35, 2176–2186.Google Scholar
Rogers, A.R. & Harpending, H. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552–569.Google ScholarPubMed
Ronquist, F. & Huelsenbeck, J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.Google Scholar
Schneider, S. & Excoffier, L. 1999. Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics, 152, 1079–1089.Google Scholar
Sinclair, B.J. & Stevens, M.I. 2006. Terrestrial microarthropods of Victoria Land and Queen Maud Mountains, Antarctica: implications of climate change. Soil Biology & Biochemistry, 38, 3158–3170.Google Scholar
Stevens, M.I. & Hogg, I.D. 2003. Long-term isolation and recent range expansion from glacial refugia revealed for the endemic springtail Gomphiocephalus hodgsoni from Victoria Land, Antarctica. Molecular Ecology, 12, 2357–2369.Google Scholar
Stevens, M.I., Greenslade, P., Hogg, I.D. & Sunnucks, P. 2006. Southern Hemisphere springtails: could any have survived glaciation of Antarctica? Molecular Biology and Evolution, 23, 874–882.CrossRefGoogle ScholarPubMed
Stevens, M.I., Frati, F., McGaughran, A., Spinsanti, G. & Hogg, I.D. 2007. Phylogeographic structure suggests multiple glacial refugia in northern Victoria Land for the endemic Antarctic springtail Desoria klovstadi (Collembola, Isotomidae). Zoologica Scripta, 36, 201–212.Google Scholar
Swofford, D.L. 2003. PAUP*: phylogenetic analysis using parsimony (*and other methods, version 4. Sunderland, MA: Sinauer Associates.Google Scholar
Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595.Google Scholar
Torricelli, G., Frati, F., Convey, P., Telford, M. & Carapelli, A. 2010. Population structure of Friesea grisea (Collembola, Neanuridae) in the Antarctic Peninsula and Victoria Land: evidence for local genetic differentiation of pre-Pleistocene origin. Antarctic Science, 22, 757–765.Google Scholar
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