Hostname: page-component-7c8c6479df-ph5wq Total loading time: 0 Render date: 2024-03-28T12:04:19.528Z Has data issue: false hasContentIssue false

Conservation implications of spatial genetic structure in two species of oribatid mites from the Antarctic Peninsula and the Scotia Arc

Published online by Cambridge University Press:  01 February 2018

Bettine Jansen van Vuuren*
Affiliation:
Centre for Ecological Genomics and Wildlife Conservation, Department of Zoology, University of Johannesburg, Auckland Park 2006, South Africa
Jennifer E. Lee
Affiliation:
British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge CB3 0ET, UK Centre for Invasion Biology, Stellenbosch University, Stellenbosch 7602, South Africa Current address: Government of South Georgia and the South Sandwich Islands, Government House, Stanley, Falkland Islands
Peter Convey
Affiliation:
British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge CB3 0ET, UK
Steven L. Chown
Affiliation:
School of Biological Sciences, Monash University, VIC 3800, Australia

Abstract

Mitochondrial and nuclear sequence data from two Antarctic ameronothroid mites, Halozetes belgicae and Alaskozetes antarcticus, were used to address three key questions important for understanding both the evolution of biodiversity and its future conservation in the Antarctic Peninsula Region: i) Do populations of mites across the Antarctic Peninsula and Scotia Arc constitute distinct genetic lineages? ii) What implications does the spatial genetic structure in these species have for current understanding of the region’s glacial history? iii) What are the conservation implications of these findings? Our results indicate that both mite species have been present in the Antarctic since at least the Pliocene. At the regional scale, both species are comprised of a number of divergent, but sympatric, lineages that are genetically as distinct as some species within the genera Halozetes and Alaskozetes. At the local scale, complex structure suggests limited and stochastic post-Holocene dispersal. For both species, considerable spatial genetic structure exists across the region, similar to that found in other terrestrial invertebrates. These results support the implementation of stringent biosecurity measures for moving between the Scotia Arc islands and the Antarctic Peninsula, and throughout the latter, to conserve both evolutionary history and future evolutionary trajectories.

Type
Biological Sciences
Copyright
© Antarctic Science Ltd 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allegrucci, G., Carchini, G., Convey, P. & Sbordoni, V. 2012. Evolutionary geographic relationships among orthocladine chironmid midges from Maritime Antarctic and sub-Antarctic islands. Biological Journal of the Linnean Society, 106, 258274.Google Scholar
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, 166178.Google Scholar
Bertler, N.A.N. & Barrett, P.J. 2010. Vanishing polar ice sheets. In Dodson, J., ed. Changing climates, earth systems and society. Dordrecht: Springer, 4983.Google Scholar
Block, W. 1984. Terrestrial microbiology, invertebrates and ecosystems. In Laws, R.M., ed. Antarctic ecology. London: Academic Press, 163236.Google Scholar
Carapelli, A., Leo, C. & Frati, F. 2017. High levels of genetic structuring in the Antarctic springtail Cryptopygus terranovus . Antarctic Science, 29, 311323.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 Science, B362, 23072331.Google Scholar
Chown, S.L. & Convey, P. 2016. Antarctic entomology. Annual Review of Entomology, 61, 119137.Google Scholar
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, 431438.Google Scholar
Chown, S.L., Huskies, A.H.L., Gremmen, N.J.M., Lee, J.E., Terauds, A., Crosbie, K., Frenot, Y., Hughes, K.A., Imura, S., Kiefer, K., Lebouvier, M., Raymond, B., Tsujimoto, M., Ware, C., van de Vijver, B. & Bergstrom, D.M. 2012. Continent-wide risk assessment for the establishment of nonindigenous species in Antarctica. Proceedings of the National Academy of Sciences of the United States of America, 109, 49384943.Google Scholar
Chown, S.L., Brooks, C.M., Terauds, A., Le Bohec, C., van Klaveren-Impagliazzo, C., Whittington, J.D., Butchart, S.H.M., Coetzee, B.W.T., Collen, B., Convey, P., Gaston, K.J., Gilbert, N., Gill, M., Hoft, R., Johnston, S., Kennicutt, M.C., Kriesell, H.J., Le Maho, Y., Lynch, H.J., Palomares, M., Puig-Marco, R., Stoett, P. & McGeoch, M.A. 2017. Antarctica and the strategic plan for biodiversity. PLoS Biology, 10.1371/journal.pbio.2001656.Google Scholar
Cicconardi, F., Nardi, F., Emerson, B.C., Frati, F. & Fanciulli, P.P. 2010. Deep phylogeographic divisions and long-term persistence of forest invertebrates (Hexapoda: Collembola) in the north-western Mediterranean basin. Molecular Ecology, 19, 386400.Google Scholar
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, 83, 103117.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, 203244.Google Scholar
Danforth, B.N. & Ji, S.Q. 1998. Elongation factor-1 alpha occurs as two copies in bees: implications for phylogenetic analysis of EF-1 alpha sequences in insects. Molecular Biology and Evolution, 15, 225235.Google Scholar
Drummond, A.J. & Rambaut, A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 10.1186/1471-2148-7-214.Google Scholar
Edgar, R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 17921797.Google Scholar
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, 564567.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, 246254.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, 294299.Google Scholar
Fraser, C.I., Connell, L., Lee, C.K. & Cary, S.C. 2017. Evidence of plant and animal communities at exposed and subglacial (cave) geothermal sites in Antarctica. Polar Biology, 10.1007/s00300-017-2198-9.Google Scholar
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, 56345639.CrossRefGoogle ScholarPubMed
Frati, F., Spinsanti, G. & Dallai, R. 2001. Genetic variation of mtCOII gene sequences in the collembolan Isotoma klovstadi from Victoria Land, Antarctica: evidence for population differentiation. Polar Biology, 24, 934940.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, 766773.Google Scholar
Hughes, K.A. & Convey, P. 2010. The protection of Antarctic terrestrial ecosystems from inter- and intra-continental transfer of non-indigenous species by human activities: a review of current systems and practices. Global Environmental Change - Human and Policy Dimensions, 20, 96112.Google Scholar
Laumann, M., Norton, R.A., Weigmann, G., Scheu, S., Maraun, M. & Heethoff, M. 2007. Speciation in the parthenogenetic oribatid mite genus Tectocepheus (Acari, Oribatida) as indicated by molecular phylogeny. Pedobiologia, 51, 111122.Google Scholar
Lee, J.E. & Chown, S.L. 2011. Quantification of intra-regional propagule movements in the Antarctic. Antarctic Science, 23, 337342.Google Scholar
Lee, J.R., Raymond, B., Bracegirdle, T.J., Chadès, I., Fuller, R.A., Shaw, J.D. & Terauds, A. 2017. Climate change drives expansion of Antarctic ice-free habitat. Nature, 10.1038/nature22996.Google Scholar
Librado, P. & Rozas, J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 14511452.Google Scholar
Mantel, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Research, 27, 209220.Google Scholar
Marshall, D.J. & Convey, P. 2004. Latitudinal variation in habitat specificity of ameronothrid mites (Oribatida). Experimental and Applied Acarology, 34, 2135.Google Scholar
Maslen, N.R. & Convey, P. 2006. Nematode diversity and distribution in the southern Maritime Antarctic: clues to history? Soil Biology & Biochemistry, 38, 31413151.Google Scholar
McGaughran, A., Stevens, M.I., Hogg, I.D. & Carapelli, A. 2011. Extreme glacial legacies: a synthesis of the Antarctic springtail phylogeographic record. Insects, 2, 6282.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, 103119.Google Scholar
McGeoch, M.A., Shaw, J.D., Terauds, A., Lee, J.E. & Chown, S.L. 2015. Monitoring biological invasion across the broader Antarctic: a baseline and indicator framework. Global Environmental Change - Human and Policy Dimensions, 32, 108125.Google Scholar
Morgan, F., Barker, G., Briggs, C., Price, R. & Keys, H. 2007. Environmental domains of Antarctica version 2.0 final report. Landcare Research Contract Report: LCO708/055. Available at: https://www.landcareresearch.co.nz/publications/researchpubs/eda_v2_final_report.pdf.Google Scholar
Mortimer, E., van Vuuren, B.J., 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 - Biological Sciences, B278, 12471255.Google Scholar
Nolan, L., Hogg, I.D., Stevens, M.I. & Haase, M. 2006. Fine scale distribution of mtDNA haplotypes for the springtail Gomphiocephalus hodgsoni (Collembola) corresponds to an ancient shoreline in Taylor Valley, Continental Antarctica. Polar Biology, 29, 813819.Google Scholar
Posada, D. 2009. Selection of models of DNA evolution with jModelTest. Methods in Molecular Biology, 537, 93112.Google Scholar
Rambaut, A. & Drummond, A.J. 2007. Tracer v1.4. Available at: http://beast.bio.ed.ac.uk/Tracer.Google Scholar
Rogers, A.D. 2007. Evolution and biodiversity of Antarctic organisms: a molecular perspective. Philosophical Transactions of the Royal Society - Biological Sciences, B362, 21912214.Google Scholar
Salomone, N., Emerson, B.C., Hewitt, G.M. & Bernini, F. 2002. Phylogenetic relationships among the Canary Island Steganacaridae (Acari, Oribatida) inferred from mitochondrial DNA sequence data. Molecular Ecology, 11, 7989.Google Scholar
Smellie, J.L., Haywood, A.M., Hillenbrand, C.-D., Lunt, D.J. & Valdes, P.J. 2009. Nature of the Antarctic Peninsula ice sheet during the Pliocene: geological evidence and modelling results compared. Earth-Science Reviews, 94, 7994.Google Scholar
Spence, P., Holmes, R.M., Hogg, A.M., Griffies, S.M., Stewart, K.D. & England, M.H. 2017. Localized rapid warming of West Antarctic subsurface waters by remote winds. Nature Climate Change, 7, 595603.Google Scholar
Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 10.1093/bioinformatics/btu033.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, 23572369.Google Scholar
Student, J., Amelung, B. & Lamers, M. 2016. Towards a tipping point? Exploring the capacity to self-regulate Antarctic tourism using agent-based modelling. Journal of Sustainable Tourism, 24, 412429.CrossRefGoogle Scholar
Terauds, A., Chown, S.L., Morgan, F., Peat, H.J., Watts, D.J., Keys, H., Convey, P. & Bergstrom, D.M. 2012. Conservation biogeography of the Antarctic. Diversity and Distributions, 18, 726741.Google Scholar
Tin, T., Fleming, Z.L., Hughes, K.A., Ainley, D.G., Convey, P., Moreno, C.A., Pfeiffer, S., Scott, J. & Snape, I. 2009. Impacts of local human activities on the Antarctic environment. Antarctic Science, 21, 333.Google Scholar
Trusel, L.D., Frey, K.E., Das, S.B., Karnauskas, K.B., Munneke, P.K., van Meijgaard, E. & van den Broeke, M.R. 2015. Divergent trajectories of Antarctic surface melt under two twenty-first-century climate scenarios. Nature Geoscience, 10.1038/NGEO2563.Google Scholar
Whinam, J., Chilcott, N. & Bergstrom, D.M. 2005. Sub-Antarctic hitchhikers: expeditioners as vectors for the introduction of alien organisms. Biological Conservation, 121, 207219.Google Scholar