Skip to main content

Advertisement

Log in

Temperature-related activity of Gomphiocephalus hodgsoni (Collembola) mitochondrial DNA (COI) haplotypes in Taylor Valley, Antarctica

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Gomphiocephalus hodgsoni (Collembola) is the most common and widely distributed arthropod in the Dry Valleys of southern Victoria Land, and is genetically diverse with over 70 mitochondrial cytochrome c oxidase subunit I (COI) haplotypes. There is also considerable physiological variation among G. hodgsoni individuals in their cold tolerance and metabolic activity. Here, we assessed genetic haplotypes of G. hodgsoni relative to the environmental conditions during which individuals were active. We sequenced the COI region of 151 individuals collected in pitfall traps from three sites within Taylor Valley and found 19 unique haplotypes that separated into two distinct lineages (1.6 % divergence), with one lineage comprising 80 % of the sequenced population. During two-hourly sampling, air temperature was the strongest predictor of activity between the two lineages (R 2 = 0.56), and when combined with subsurface soil temperature, relative humidity and photosynthetically active radiation, explanatory power increased to R 2 = 0.71. With steadily increasing air temperatures predicted for much of Antarctica, it is likely that some haplotypes will have a selective advantage and potentially result in decreased genetic variability within populations. We suggest that temporal monitoring of the relative proportions of COI haplotypes or other appropriate genetic markers may provide a subtle measure of biological responses to environmental changes within Antarctic terrestrial ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ballard JWO, Pichaud N (2013) Mitochondrial DNA: more than an evolutionary bystander. Funct Ecol 28:218–231

    Article  Google Scholar 

  • Bender EA, Case TJ, Gilpin ME (1984) Perturbation experiments in community ecology: theory and practice. Ecology 65:1–13

    Article  Google Scholar 

  • Blier PU, Lemieux H, Pichaud N (2013) Holding our breath in our modern world: will mitochondria keep the pace with climate changes? Can J Zool 92:591–601

    Article  Google Scholar 

  • Block W (1985) Ecological and physiological studies of terrestrial arthropods in the Ross Dependency 1984–85. Br Antarct Surv Bull 68:115–122

    Google Scholar 

  • Cannon RJC, Block W (1988) Cold tolerance of microarthropods. Biol Rev 63:23–77

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Convey P (2011) Antarctic terrestrial biodiversity in a changing world. Polar Biol 34:1629–1641

    Article  Google Scholar 

  • Convey P, Chown SL, Clarke A, Barnes DKA, Bokhorst S, Cummings V, Ducklow HW, Frati F, Green TGA, Gordon S, Griffiths HJ, Howard-Williams C, Huiskes AHL, Laybourn-Parry J, Lyons WB, McMinn A, Morley SA, Peck LS, Quesada A, Robinson SA, Schiaparelli S, Wall DH (2014) The spatial structure of Antarctic biodiversity. Ecol Monogr 84:203–244

    Article  Google Scholar 

  • Correa CC, Aw WC, Melvin RG, Pichaud N, Ballard JWO (2012) Mitochondrial DNA variants influence mitochondrial bioenergetics in Drosophila melanogaster. Mitochondrion 12:459–464

    Article  CAS  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Denton GH, Hughes TJ (2000) Reconstruction of the Ross ice drainage system, Antarctica, at the last glacial maximum. Geogr Ann Ser A Phys Geogr 82:143–166

    Article  Google Scholar 

  • Denton GH, Marchant DR (2000) The geological basis for a reconstruction of a grounded ice sheet in McMurdo Sound, Antarctica, at the last glacial maximum. Geogr Ann Ser A Phys Geogr 82:167–211

    Article  Google Scholar 

  • Doran PT, McKay CP, Clow GD, Dana GL, Fountain AG, Nylen T, Lyons WB (2002) Valley floor climate observations from the McMurdo dry valleys, Antarctica, 1986–2000. J Geophys Res 107:4772

    Article  Google Scholar 

  • Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2010) Geneious v5.1. Biomatters Ltd, Auckland. http://www.geneious.com

  • Fitzsimons JM (1971) Temperature and three species of Antarctic arthropods. Pacif Insects Monogr 25:127–135

    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. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Fraser CI, Terauds A, Smellie J, Convey P, Chown SL (2014) Geothermal activity helps life survive glacial cycles. Proc Natl Acad Sci USA 111:5634–5639

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Green TGA, Sancho LG, Türk R, Seppelt RD, Hogg ID (2011) High diversity of lichens at 84°S, Queen Maud Mountains, suggests preglacial survival of species in the Ross Sea region, Antarctica. Polar Biol 34:1211–1220

    Article  Google Scholar 

  • Greenslade P, Stevens MI, Torricelli G, D’Haese CA (2011) An ancient Antarctic endemic genus restored: morphological and molecular support for Gomphiocephalus hodgsoni (Collembola: Hypogastruridae). Syst Entomol 36:223–240

    Article  Google Scholar 

  • Hawes TC (2011) Rafting in the Antarctic springtail, Gomphiocephalus hodgsoni. Antarct Sci 23:456–460

    Article  Google Scholar 

  • Hawes TC, Torricelli G, Stevens MI (2010) Haplotype diversity in the Antarctic springtail Gressittacantha terranova at fine spatial scales—a Holocene twist to a Pliocene tale. Antarct Sci 22:766–773

    Article  Google Scholar 

  • Hebert PD, Cywinska A, Ball SL (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B Biol Sci 270:313–321

    Article  CAS  Google Scholar 

  • Hogg ID, Wall DH (2011) Global change and Antarctic terrestrial biodiversity. Polar Biol 34:1625–1627

    Article  Google Scholar 

  • Hogg ID, Cary SC, Convey P, Newsham KK, O’Donnell AG, Adams BJ, Aislabie J, Frati F, Stevens MI, Wall DH (2006) Biotic interactions in Antarctic terrestrial ecosystems: are they a factor? Soil Biol Biochem 38:3035–3040

    Article  CAS  Google Scholar 

  • Hopkin SP (1997) Biology of the springtails (Insecta: Collembola). Oxford University Press, New York

    Google Scholar 

  • Hopkins DW, Sparrow AD, Novis PM, Gregorich EG, Elberling B, Greenfield LG (2006) Controls on the distribution of productivity and organic resources in Antarctic Dry Valley soils. Proc R Soc Lond B Biol Sci 273:2687–2695

    Article  CAS  Google Scholar 

  • Ivanova NV, Dewaard JR, Hebert PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol Ecol Notes 6:998–1002

    Article  CAS  Google Scholar 

  • Janetschek H (1963) On the terrestrial fauna of the Ross-Sea area, Antarctica (preliminary report). Pac Insects 5:305–311

    Google Scholar 

  • Janetschek H (1970) Environments and ecology of terrestrial arthropods in the high Antarctic. In: Holdgate MW (ed) Antarctic ecology, vol 2. Academic Press, London, pp 871–885

    Google Scholar 

  • Kennedy AD (1993) Water as a limiting factor in the antarctic terrestrial environment: a biogeographical synthesis. Arct Alp Res 25:308–315

    Article  Google Scholar 

  • Köhler H-R, Eckwert H, Triebskorn R, Bengtsson G (1999) Interaction between tolerance and 70 kDa stress protein (hsp70) induction in collembolan populations exposed to long-term metal pollution. Appl Soil Ecol 11:43–52

    Article  Google Scholar 

  • Levy J, Lyons WB, Adams B (2013) Understanding terrestrial ecosystem response to Antarctic climate change. Eos Trans Am Geophys Union 94:33

    Article  Google Scholar 

  • Marchant DR, Head JW (2007) Antarctic dry valleys: microclimate zonation, variable geomorphic processes, and implications for assessing climate change on Mars. Icarus 192:187–222

    Article  Google Scholar 

  • McGaughran A, Convey P, Stevens MI, Chown SL (2010) Metabolic rate, genetic and microclimate variation among springtail populations from sub-Antarctic Marion Island. Polar Biol 33:909–918

    Article  Google Scholar 

  • McGaughran A, Hogg ID, Convey P (2011) Extended ecophysiological analysis of Gomphiocephalus hodgsoni (Collembola): flexibility in life history strategy and population response. Polar Biol 34:1713–1725

    Article  Google Scholar 

  • Nielsen UN, Wall DH (2013) The future of soil invertebrate communities in polar regions: different climate change responses in the Arctic and Antarctic? Ecol Lett 16:409–419

    Article  PubMed  Google Scholar 

  • Nolan L, Hogg ID, Stevens MI, Haase M (2006) Fine scale distribution of mtDNA haplotypes for the springtail Gomphiocephalus hodgsoni (Collembola) corresponds to an ancient shoreline in Taylor Valley, Antarctica. Polar Biol 29:813–819

    Article  Google Scholar 

  • Peterson D, Howard-Williams C (2001) The latitudinal gradient project. Antarct NZ Spec Publ 6:1–46

  • Pichaud N, Ballard JWO, Tanguay RM, Blier PU (2012) Naturally occurring mitochondrial DNA haplotypes exhibit metabolic differences: insight into functional properties of mitochondria. Evolution 66:3189–3197

    Article  CAS  PubMed  Google Scholar 

  • Ratnasingham S, Hebert PDN (2007) BOLD: the barcode of life data system (www.barcodinglife.org). Mol Ecol Notes 7:355–364

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Sinclair BJ, Sjursen H (2001) Cold tolerance of the Antarctic springtail Gomphiocephalus hodgsoni (Collembola, Hypogastruridae). Antarct Sci 13:271–279

    Article  Google Scholar 

  • Sinclair BJ, Stevens MI (2006) Terrestrial microarthropods of Victoria Land and Queen Maud Mountains, Antarctica: implications of climate change. Soil Biol Biochem 38:3158–3170

    Article  CAS  Google Scholar 

  • Smith TW, Wall DH, Hogg ID, Adams BJ, Nielsen UN, Virginia RA (2012) Thawing permafrost alters nematode viability and soil habitat characteristics in an Antarctic polar desert ecosystem. Pedobiologia 55:75–81

    Article  Google Scholar 

  • Steig EJ, Schneider DP, Rutherford SD, Mann ME, Comiso JC, Shindell DT (2009) Warming of the Antarctic ice-sheet surface since the 1957 international geophysical year. Nature 457:459–462

    Article  CAS  PubMed  Google Scholar 

  • Stevens MI, Hogg ID (2002) Expanded distributional records of Collembola and Acari in Southern Victoria Land, Antarctica. Pedobiologia 46:485–495

    Article  Google Scholar 

  • Stevens MI, Hogg ID (2003) Long-term isolation and recent range expansion revealed for the endemic springtail Gomphiocephalus hodgsoni from Southern Victoria Land, Antarctica. Mol Ecol 12:2357–2369

    Article  CAS  PubMed  Google Scholar 

  • Stevens MI, Hogg ID (2006) Contrasting levels of mitochondrial DNA variability between mites (Penthalodidae) and springtails (Hypogastruridae) from the Trans-Antarctic Mountains suggest long-term effects of glaciation and life history on substitution rates, and speciation processes. Soil Biol Biochem 38:3171–3180

    Article  CAS  Google Scholar 

  • Swofford D (2002) PAUP*: phylogenetic analysis using parsimony, version 4.0b10 for Macintosh. Sinauer Associates Inc Publishers, Sunderland

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tilbrook PJ (1967) The terrestrial invertebrate fauna of the Maritime Antarctic. Philos Trans R Soc Lond Ser B Biol Sci 252:261–278

    Article  Google Scholar 

  • Turner J, Colwell SR, Marshall GJ, Lachlan-Cope TA, Carleton AM, Jones PD, Lagun V, Reid PA, Iagovkina S (2005) Antarctic climate change during the last 50 years. Int J Climatol 25:279–294

    Article  Google Scholar 

  • Vaughn DG, Marshall GJ, Connolley WM, Parkinson C, Mulvaney R, Hodgson DA, King JC, Pudsey CJ, Turner J (2003) Recent rapid regional climate warming on the Antarctic Peninsula. Clim Chang 60:243–274

    Article  Google Scholar 

  • Wise KAJ (1967) Collembola (springtails). Antarct Res Ser 10:123–148

    Google Scholar 

Download references

Acknowledgments

We are extremely grateful to three anonymous reviewers for their thoughtful and constructive comments which improved the manuscript. Sequencing at the University of Waikato was financed by the International Centre for Terrestrial Antarctic Research (ICTAR) and funding from the Government of Canada through the Ontario Genomics Institute and Genome Canada supporting sequencing at the CCDB at the University of Guelph. We thank Antarctica New Zealand staff at Scott Base and Christchurch for their field and logistic support. Financial support of G.C. was provided by the ICTAR Young Investigator Award and the Environmental Research Institute Masters Research Scholarship. C. Lee, C. Cary, J. Sohm, U. Nielsen, B. Adams and D. Wall provided valuable advice and support in Antarctica.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ian D. Hogg.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Collins, G.E., Hogg, I.D. Temperature-related activity of Gomphiocephalus hodgsoni (Collembola) mitochondrial DNA (COI) haplotypes in Taylor Valley, Antarctica. Polar Biol 39, 379–389 (2016). https://doi.org/10.1007/s00300-015-1788-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-015-1788-7

Keywords

Navigation