Genome-wide SNP data reveal improved evidence for Antarctic glacial refugia and dispersal of terrestrial invertebrates.
Antarctic Peninsula
dispersal
mitochondrial
refugia
single-nucleotide polymorphism
springtails
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
11 2019
11 2019
Historique:
received:
15
04
2019
revised:
19
09
2019
accepted:
25
09
2019
pubmed:
10
10
2019
medline:
19
6
2020
entrez:
10
10
2019
Statut:
ppublish
Résumé
Antarctica is isolated, surrounded by the Southern Ocean and has experienced extreme environmental conditions for millions of years, including during recent Pleistocene glacial maxima. How Antarctic terrestrial species might have survived these glaciations has been a topic of intense interest, yet many questions remain unanswered, particularly for Antarctica's invertebrate fauna. We examine whether genetic data from a widespread group of terrestrial invertebrates, springtails (Collembola, Isotomidae) of the genus Cryptopygus, show evidence for long-term survival in glacial refugia along the Antarctic Peninsula. We use genome-wide SNP analyses (via genotyping-by-sequencing, GBS) and mitochondrial data to examine population diversity and differentiation across more than 20 sites spanning >950 km on the Peninsula, and from islands both close to the Peninsula and up to ~1,900 km away. Population structure analysis indicates the presence of strong local clusters of diversity, and we infer that patterns represent a complex interplay of isolation in local refugia coupled with occasional successful long-distance dispersal events. We identified wind and degree days as significant environmental drivers of genetic diversity, with windier and warmer sites hosting higher diversity. Thus, we infer that refugial areas along the Antarctic Peninsula have allowed populations of indigenous springtails to survive in situ throughout glacial periods. Despite the difficulties of dispersal in cold, desiccating conditions, Cryptopygus springtails on the Peninsula appear to have achieved multiple long-distance colonization events, most likely through wind-related dispersal events.
Banques de données
GENBANK
['GQ215400', 'GQ215488', 'MN473376', 'MN473393']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4941-4957Informations de copyright
© 2019 John Wiley & Sons Ltd.
Références
Adams, B. J., Bardgett, R. D., Ayres, E., Wall, D. H., Aislabie, J., Bamforth, S., … Stevens, M. I. (2006). Diversity and distribution of Victoria Land biota. Soil Biology & Biochemistry, 38(10), 3003-3018. https://doi.org/10.1016/j.soilbio.2006.04.030
Arnold, B., Corbett-Detig, R. B., Hartl, D., & Bomblies, K. (2013). RADseq underestimates diversity and introduces genealogical biases due to nonrandom haplotype sampling. Molecular Ecology, 22(11), 3179-3190. https://doi.org/10.1111/mec.12276
Baird, H. P., Janion-Scheepers, C., Stevens, M. I., Leihy, R. I., & Chown, S. L. (2019). The ecological biogeography of indigenous and introduced Antarctic springtails. Journal of Biogeography, 46(9), 1959-1973. https://doi.org/10.1111/jbi.13639
Barker, P. F., & Camerlenghi, A. (2001). Glacial history of the Antarctic Peninsula from Pacific margin sediments. In P. F. Barker, A. Camerlenghi, G. D. Acton, & A. T. S. Ramsay (Eds.), Antarctic glacial history and sea-level change. 178, 1-40.College Station, TX: Ocean Drilling Program.
Barnes, D. K. A., Hodgson, D. A., Convey, P., Allen, C. S., & Clarke, A. (2006). Incursion and excursion of Antarctic biota: Past, present and future. Global Ecology and Biogeography: A Journal of Macroecology, 15(2), 121-142. https://doi.org/10.1111/j.1466-822X.2006.00216.x
Bennett, K. R., Hogg, I. D., Adams, B. J., & Hebert, P. D. N. (2016). High levels of intraspecific genetic divergences revealed for Antarctic springtails: Evidence for small-scale isolation during Pleistocene glaciation. Biological Journal of the Linnean Society, 119(1), 166-178. https://doi.org/10.1111/bij.12796
Biersma, E. M., Jackson, J. A., Bracegirdle, T. J., Griffiths, H., Linse, K., & Convey, P. (2018). Low genetic variation between South American and Antarctic populations of the bank-forming moss Chorisodontium aciphyllum (Dicranaceae). Polar Biology, 41(4), 599-610. https://doi.org/10.1007/s00300-017-2221-1
Biersma, E. M., Jackson, J. A., Stech, M., Griffiths, H., Linse, K., & Convey, P. (2018). Molecular data suggest long-term in situ Antarctic persistence within Antarctica's most speciose plant genus, Schistidium. Frontiers in Ecology and Evolution, 6, 77. https://doi.org/10.3389/fevo.2018.00077
Block, W., Smith, R. I. L., & Kennedy, A. D. (2009). Strategies of survival and resource exploitation in the Antarctic fellfield ecosystem. Biological Reviews of the Cambridge Philosophical Society, 84(3), 449-484. https://doi.org/10.1111/j.1469-185X.2009.00084.x
Bradburd, G. S., Ralph, P. L., & Coop, G. M. (2016). A spatial framework for understanding population structure and admixture. PLoS Genetics, 12(1), e1005703.
Brooks, S. T., Jabour, J., van den Hoff, J., & Bergstrom, D. M. (2019). Our footprint on Antarctica competes with nature for rare ice-free land. Nature Sustainability, 2, 185-190. https://doi.org/10.1038/s41893-019-0237-y
Burton-Johnson, A., Black, M., Fretwell, P. T., & Kaluza-Gilbert, J. (2016). An automated methodology for differentiating rock from snow, clouds and sea in Antarctica from Landsat 8 imagery: A new rock outcrop map and area estimation for the entire Antarctic continent. The Cryosphere, 10(4), 1665-1677.
Carapelli, A., Convey, P., Frati, F., Spinsanti, G., & Fanciulli, P. P. (2017). Population genetics of three sympatric springtail species (Hexapoda: Collembola) from the South Shetland Islands: Evidence for a common biogeographic pattern. Biological Journal of the Linnean Society, 120(4), 788-803. https://doi.org/10.1093/biolinnean/blw004
Chong, C.-W., Pearce, D. A., & Convey, P. (2015). Emerging spatial patterns in Antarctic prokaryotes. Frontiers in Microbiology, 6, 1058. https://doi.org/10.3389/fmicb.2015.01058
Chown, S. L., Clarke, A., Fraser, C. I., Cary, S. C., Moon, K. L., & McGeoch, M. A. (2015). The changing form of Antarctic biodiversity. Nature, 522(7557), 431. https://doi.org/10.1038/nature14505
Chown, S. L., & Convey, P. (2016). Antarctic entomology. Annual Review of Entomology, 61, 119-137. https://doi.org/10.1146/annurev-ento-010715-023537
Clarke, A., Barnes, D., & Hodgson, D. (2005). How isolated is Antarctica? Trends in Ecology & Evolution, 20(1), 1-3. https://doi.org/10.1016/j.tree.2004.10.004
Collins, G. E., Hogg, I. D., Convey, P., Barnes, A. D., & McDonald, I. R. (2019). Spatial and temporal scales matter when assessing the species and genetic diversity of springtails (Collembola) in Antarctica. Frontiers in Ecology and Evolution, 7, 76. https://doi.org/10.3389/fevo.2019.00076
Convey, P. (1996). The influence of environmental characteristics on life history attributes of Antarctic terrestrial biota. Biological Reviews of the Cambridge Philosophical Society, 71(2), 191-225. https://doi.org/10.1111/j.1469-185X.1996.tb00747.x
Convey, P. (2017). Antarctic ecosystems. In Reference module in life sciences. Amsterdam, The Netherlands: Elsevier. https://doi.org/10.1016/B978-0-12-809633-8.02182-8
Convey, P., Gibson, J. A. E., Hillenbrand, C.-D., Hodgson, D. A., Pugh, P. J. A., Smellie, J. L., & Stevens, M. I. (2008). Antarctic terrestrial life - challenging the history of the frozen continent? Biological Reviews of the Cambridge Philosophical Society, 83(2), 103-117. https://doi.org/10.1111/j.1469-185X.2008.00034.x
Convey, P., & Smith, R. I. L. (1997). The terrestrial arthropod fauna and its habitats in northern Marguerite Bay and Alexander Island, maritime Antarctic. Antarctic Science, 9, 12-26. https://doi.org/10.1017/S0954102097000035
Convey, P., & Smith, R. I. L. (2006). Geothermal bryophyte habitats in the South Sandwich Islands, maritime Antarctic. Journal of Vegetation Science, 17(4), 529-538. https://doi.org/10.1111/j.1654-1103.2006.tb02474.x
Convey, P., & Stevens, M. I. (2007). Ecology. Antarctic biodiversity. Science, 317(5846), 1877-1878.
Convey, P., Stevens, M. I., Hodgson, D. A., Smellie, J. L., Hillenbrand, C.-D., Barnes, D. K. A., … Cary, S. C. (2009). Exploring biological constraints on the glacial history of Antarctica. Quaternary Science Reviews, 28(27-28), 3035-3048. https://doi.org/10.1016/j.quascirev.2009.08.015
Coulson, S. J., Hodkinson, I. D., Webb, N. R., & Harrison, J. A. (2002). Survival of terrestrial soil-dwelling arthropods on and in seawater: Implications for trans-oceanic dispersal. Functional Ecology, 16(3), 353-356. https://doi.org/10.1046/j.1365-2435.2002.00636.x
Courtright, E. M., Wall, D. H., Virginia, R. A., Frisse, L. M., Vida, J. T., & Thomas, W. K. (2000). Nuclear and mitochondrial DNA sequence diversity in the Antarctic nematode Scottnema lindsayae. Journal of Nematology, 32(2), 143-153.
Curtis, A., & Kyle, P. (2011). Geothermal point sources identified in a fumarolic ice cave on Erebus volcano, Antarctica using fiber optic distributed temperature sensing. Geophysical Research Letters, 38(16), L16802. https://doi.org/10.1029/2011gl048272
Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., … 1000 Genomes Project Analysis Group (2011). The variant call format and VCFtools. Bioinformatics, 27(15), 2156-2158. https://doi.org/10.1093/bioinformatics/btr330
Dornelas, M., Magurran, A. E., Buckland, S. T., Chao, A., Chazdon, R. L., Colwell, R. K., … Vellend, M. (2013). Quantifying temporal change in biodiversity: Challenges and opportunities. Proceedings of the Royal Society B: Biological Sciences, 280(1750), 20121931.
Elshire, R. J., Glaubitz, J. C., Sun, Q., Poland, J. A., Kawamoto, K., Buckler, E. S., & Mitchell, S. E. (2011). A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE, 6(5), e19379. https://doi.org/10.1371/journal.pone.0019379
Ersts, P. J. (n.d.). Geographic Distance Matrix Generator (version 1.2.3). Retrieved from http://biodiversityinformatics.amnh.org/open_source/gdmg/
Everatt, M. J., Convey, P., Bale, J. S., Roger Worland, M., & Hayward, S. A. L. (2015). Responses of invertebrates to temperature and water stress: A polar perspective. Journal of Thermal Biology, 54, 118-132. https://doi.org/10.1016/j.jtherbio.2014.05.004
Excoffier, L., Dupanloup, I., Huerta-Sánchez, E., Sousa, V. C., & Foll, M. (2013). Robust demographic inference from genomic and SNP data. PLoS Genetics, 9(10), e1003905. https://doi.org/10.1371/journal.pgen.1003905
Excoffier, L., & Lischer, H. E. L. (2010). arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10(3), 564-567.
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(2), 479-491.
Fanciulli, P. P., Summa, D., Dallai, R., & Frati, R. (2001). High levels of genetic variability and population differentiation in Gressittacantha terranova (Collembola, Hexapoda) from Victoria Land, Antarctic. Antarctic Science, 13, 246-254.
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(5), 294-299.
Fraser, C. I., McGaughran, A., Chuah, A., & Waters, J. M. (2016). The importance of replicating genomic analyses to verify phylogenetic signal for recently evolved lineages. Molecular Ecology, 25(15), 3683-3695. https://doi.org/10.1111/mec.13708
Fraser, C. I., Morrison, A. K., Hogg, A. M. C., Macaya, E. C., van Sebille, E., Ryan, P. G., … Waters, J. M. (2018). Antarctica's ecological isolation will be broken by storm-driven dispersal and warming. Nature Climate Change, 8(8), 704-708. https://doi.org/10.1038/s41558-018-0209-7
Fraser, C. I., Nikula, R., Ruzzante, D. E., & Waters, J. M. (2012). Poleward bound: Biological impacts of Southern Hemisphere glaciation. Trends in Ecology & Evolution, 27(8), 462-471. https://doi.org/10.1016/j.tree.2012.04.011
Fraser, C. I., Nikula, R., Spencer, H. G., & Waters, J. M. (2009). Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum. Proceedings of the National Academy of Sciences of the United States of America, 106(9), 3249-3253. https://doi.org/10.1073/pnas.0810635106
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(15), 5634-5639. https://doi.org/10.1073/pnas.1321437111
Fu, Y. X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147(2), 915-925.
Gautier, M., Gharbi, K., Cezard, T., Foucaud, J., Kerdelhué, C., Pudlo, P., … Estoup, A. (2013). The effect of RAD allele dropout on the estimation of genetic variation within and between populations. Molecular Ecology, 22(11), 3165-3178. https://doi.org/10.1111/mec.12089
Gillespie, R. G., Baldwin, B. G., Waters, J. M., Fraser, C. I., Nikula, R., & Roderick, G. K. (2012). Long-distance dispersal: A framework for hypothesis testing. Trends in Ecology & Evolution, 27(1), 47-56. https://doi.org/10.1016/j.tree.2011.08.009
Greenslade, P., Farrow, R. A., & Smith, J. M. B. (1999). Long distance migration of insects to a subantarctic island. Journal of Biogeography, 26(6), 1161-1167. https://doi.org/10.1046/j.1365-2699.1999.00356.x
Hawes, T. C., Worland, M. R., Bale, J. S., & Convey, P. (2008). Rafting in Antarctic Collembola. Journal of Zoology, 274(1), 44-50.
Hayward, S. A. L., Roger Worland, M., Convey, P., & Bale, J. S. (2004). Habitat moisture availability and the local distribution of the Antarctic Collembola Cryptopygus antarcticus and Friesea grisea. Soil Biology & Biochemistry, 36(6), 927-934. https://doi.org/10.1016/j.soilbio.2004.02.007
Hijmans, R. J., & van Etten, J. (2012). raster: Geographic analysis and modelling with raster data. R package version 2.0-12. Retrieved from http://CRAN.R-project.org/package=raster
Hills, S. F. K., Stevens, M. I., & Gemmill, C. E. C. (2010). Molecular support for Pleistocene persistence of the continental Antarctic moss Bryum argenteum. Antarctic Science, 22(6), 721-726.
Iakovenko, N. S., Smykla, J., Convey, P., Kašparová, E., Kozeretska, I. A., Trokhymets, V., … Janko, K. (2015). Antarctic bdelloid rotifers: Diversity, endemism and evolution. Hydrobiologia, 761(1), 5-43. https://doi.org/10.1007/s10750-015-2463-2
Jombart, T. (2008). adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24(11), 1403-1405. https://doi.org/10.1093/bioinformatics/btn129
Kamvar, Z. N., Tabima, J. F., & Grünwald, N. J. (2014). poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ, 2, e281.
Kennedy, A. D. (1993). Water as a limiting factor in the Antarctic terrestrial environment: A biogeographical synthesis. Arctic and Alpine Research, 25(4), 308. https://doi.org/10.2307/1551914
Knaus, B. J., & Grunwald, N. J. (2016). vcfr: An R package to manipulate and visualize VCF format data. Molecular Ecology Resources, 17(1), 44-53.
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). mega 10.0.5: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35, 1547-1549.
Mackintosh, A. N., Verleyen, E., O'Brien, P. E., White, D. A., Jones, R. S., McKay, R., … Masse, G. (2014). Retreat history of the East Antarctic Ice Sheet since the Last Glacial Maximum. Quaternary Science Reviews, 100, 10-30. https://doi.org/10.1016/j.quascirev.2013.07.024
Magurran, A. E., & Dornelas, M. (2010). Biological diversity in a changing world. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 365(1558), 3593-3597. https://doi.org/10.1098/rstb.2010.0296
McGaughran, A., Hogg, I. D., & Convey, P. (2011). Extended ecophysiological analysis of Gomphiocephalus hodgsoni (Collembola): Flexibility in life history strategy and population response. Polar Biology, 34(11), 1713-1725. https://doi.org/10.1007/s00300-011-1001-6
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(2), 606-618. https://doi.org/10.1016/j.ympev.2007.10.003
McGaughran, A., Stevens, M. I., Hogg, I. D., & Carapelli, A. (2011). Extreme glacial legacies: A synthesis of the Antarctic springtail phylogeographic record. Insects, 2(2), 62-82. https://doi.org/10.3390/insects2020062
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(1), 103-119. https://doi.org/10.1111/j.1365-2699.2009.02178.x
Morris, G. P., Grabowski, P. P., & Borevitz, J. O. (2011). Genomic diversity in switchgrass (Panicum virgatum): From the continental scale to a dune landscape. Molecular Ecology, 20(23), 4938-4952. https://doi.org/10.1111/j.1365-294X.2011.05335.x
Mortimer, E., Jansen van Vuuren, B., Lee, J. E., Marshall, D. J., Convey, P., & Chown, S. L. (2011). Mite dispersal among the Southern Ocean Islands and Antarctica before the Last Glacial Maximum. Proceedings of the Royal Society B: Biological Sciences, 278(1709), 1247-1255.
Nei, M. (1987). Molecular evolutionary genetics. New York, NY: Columbia University Press.
Nikula, R., Fraser, C. I., Spencer, H. G., & Waters, J. M. (2010). Circumpolar dispersal by rafting in two subantarctic kelp-dwelling crustaceans. Marine Ecology Progress Series, 405, 221-230. https://doi.org/10.3354/meps08523
Nkem, J. N., Wall, D. H., Virginia, R. A., Barrett, J. E., Broos, E. J., Porazinska, D. L., & Adams, B. J. (2005). Wind dispersal of soil invertebrates in the McMurdo Dry Valleys, Antarctica. Polar Biology, 29(4), 346-352. https://doi.org/10.1007/s00300-005-0061-x
Paradis, E. (2010). pegas: An R package for population genetics with an integrated-modular approach. Bioinformatics, 26(3), 419-420. https://doi.org/10.1093/bioinformatics/btp696
Peck, L. S., Convey, P., & Barnes, D. K. A. (2006). Environmental constraints on life histories in Antarctic ecosystems: Tempos, timings and predictability. Biological Reviews of the Cambridge Philosophical Society, 81(1), 75-109. https://doi.org/10.1017/S1464793105006871
Perrings, C., Duraiappah, A., Larigauderie, A., & Mooney, H. (2011). Ecology. The biodiversity and ecosystem services science-policy interface. Science, 331(6021), 1139-1140.
Pisa, S., Biersma, E. M., Convey, P., Patiño, J., Vanderpoorten, A., Werner, O., & Ros, R. M. (2014). The cosmopolitan moss Bryum argenteum in Antarctica: Recent colonisation or in situ survival? Polar Biology, 37(10), 1469-1477. https://doi.org/10.1007/s00300-014-1537-3
Pugh, P. J. A., & Convey, P. (2008). Surviving out in the cold: Antarctic endemic invertebrates and their refugia. Journal of Biogeography, 35(12), 2176-2186. https://doi.org/10.1111/j.1365-2699.2008.01953.x
Puillandre, N., Lambert, A., Brouillet, S., & Achaz, G. (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21(8), 1864-1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x
R Core Team (2019). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/
Raj, A., Stephens, M., & Pritchard, J. K. (2014). faststructure: Variational inference of population structure in large SNP data sets. Genetics, 197(2), 573-589. https://doi.org/10.1534/genetics.114.164350
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(10), 3158-3170. https://doi.org/10.1016/j.soilbio.2005.11.035
Skotte, L., Korneliussen, T. S., & Albrechtsen, A. (2013). Estimating individual admixture proportions from next generation sequencing data. Genetics, 195(3), 693-702. https://doi.org/10.1534/genetics.113.154138
Smellie, J. L., McIntosh, W. C., & Esser, R. (2006). Eruptive environment of volcanism on Brabant Island: Evidence for thin wet-based ice in northern Antarctic Peninsula during the Late Quaternary. Palaeogeography, Palaeoclimatology, Palaeoecology, 231(1-2), 233-252. https://doi.org/10.1016/j.palaeo.2005.07.035
Soo, R. M., Wood, S. A., Grzymski, J. J., McDonald, I. R., & Cary, S. C. (2009). Microbial biodiversity of thermophilic communities in hot mineral soils of Tramway Ridge, Mount Erebus. Antarctica. Environmental Microbiology, 11(3), 715-728. https://doi.org/10.1111/j.1462-2920.2009.01859.x
Stevens, M. I., Greenslade, P., Hogg, I. D., & Sunnucks, P. (2005). Southern Hemisphere springtails: Could any have survived glaciation of Antarctica? Molecular Biology and Evolution, 23(5), 874-882. https://doi.org/10.1093/molbev/msj073
Stevens, M. I., & Hogg, I. D. (2002). Expanded distributional records of Collembola and Acari in southern Victoria Land, Antarctica. Pedobiologia, 46(5), 485-495. https://doi.org/10.1078/0031-4056-00154
Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123(3), 585-595.
Templeton, A. R., Crandall, K. A., & Sing, C. F. (1992). A cladistic analysis of phenotypic association with haplotypes inferred from restriction site endonuclease mapping and DNA sequence data. (III) Cladogram estimation. Genetics, 132, 619-633.
Terauds, A., Chown, S. L., Morgan, F., J. Peat, H., Watts, D. J., Keys, H., … Bergstrom, D. M. (2012). Conservation biogeography of the Antarctic. Diversity and Distributions, 18(7), 726-741. https://doi.org/10.1111/j.1472-4642.2012.00925.x
Torricelli, G., Carapelli, A., Convey, P., Nardi, F., Boore, J. L., & Frati, F. (2010). High divergence across the whole mitochondrial genome in the ‘pan-Antarctic’ springtail Friesea grisea: Evidence for cryptic species? Gene, 449, 30-40. https://doi.org/10.1016/j.gene.2009.09.006
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(6), 757-765.
van Vuuren, B. J., Lee, J. E., Convey, P., & Chown, S. L. (2018). Conservation implications of spatial genetic structure in two species of oribatid mites from the Antarctic Peninsula and the Scotia Arc. Antarctic Science, 30(2), 105-114. https://doi.org/10.1017/S0954102017000529
Vega, G. C., Convey, P., Hughes, K. A., & Olalla-Tárraga, M. Á. (2019). Humans and wind, shaping Antarctic soil arthropod biodiversity. Insect Conservation and Diversity. https://doi.org/10.1111/icad.12375
Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S (4th ed.). New York, NY: Springer.
Weir, B. S., & Clark Cockerham, C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38(6), 1358-1370.
Worland, M. R., & Convey, P. (2008). The significance of the moult cycle to cold tolerance in the Antarctic collembolan Cryptopygus antarcticus. Journal of Insect Physiology, 54(8), 1281-1285. https://doi.org/10.1016/j.jinsphys.2008.06.009
Worland, M. R., Leinaas, H. P., & Chown, S. L. (2006). Supercooling point frequency distributions in Collembola are affected by moulting. Functional Ecology, 20(2), 323-329. https://doi.org/10.1111/j.1365-2435.2006.01089.x
Yang, B., Cui, L., Perez-Enciso, M., Traspov, A., Crooijmans, R. P. M. A., Zinovieva, N., … Megens, H.-J. (2017). Genome-wide SNP data unveils the globalization of domesticated pigs. Genetics, Selection, Evolution, 49(1), 71. https://doi.org/10.1186/s12711-017-0345-y