The Ancient Britons: Groundwater fauna survived extreme climate changes over tens of millions of years across NW Europe

Caitriona McInerney, Louise Maurice, Anne L. Robertson, Lee R.F.D. Knight, Joerg Arnscheidt, Chris Venditti, James Dooley, Thomas Mathers, Severine Matthijs, Karin Eriksson, Graham Proudlove, Bernd Haenfling

Research output: Contribution to journalArticle

45 Citations (Scopus)

Abstract

Global climate changes during the Cenozoic (65.5 - 0 Ma) caused major biological range shifts and extinctions. In Northern Europe, for example, a pattern of few endemics and the dominance of wide-ranging species is thought to have been determined by the Pleistocene (2.59 – 0.01 Ma) glaciations. This study, in contrast, reveals an ancient subsurface fauna endemic to Britain and Ireland. Using a Bayesian phylogenetic approach we found that two species of stygobitic invertebrates (genus Niphargus) have not only survived the entire Pleistocene in refugia but have persisted for at least 19.5 million years. Other Niphargus species form distinct cryptic taxa that diverged from their nearest continental relative between 5.6 and 1.0 Ma. The study also reveals an unusual biogeographical pattern in the Niphargus genus. It originated in Northwest Europe ~88 Ma and underwent a gradual range expansion. Phylogenetic diversity and species age are highest in Northwest Europe suggesting resilience to extreme climate change, and strongly contrasting the patterns seen in surface fauna. However, species diversity is highest in Southeast Europe indicating that once the genus spread to these areas (~ 25 Ma), geomorphological and climatic conditions enabled much higher diversification. Our study highlights that groundwater ecosystems provide an important contribution to biodiversity and offer insight into the interactions between biological and climatic processes.
LanguageEnglish
Pages1153-1166
JournalMolecular Ecology
Volume23
Issue number5
DOIs
Publication statusPublished - Mar 2014

Fingerprint

fauna
climate change
groundwater
Pleistocene
phylogenetics
range expansion
refugium
glaciation
global climate
species diversity
invertebrate
extinction
biodiversity
Europe
ecosystem

Keywords

  • groundwater
  • groundwater ecology
  • Niphargus
  • Ireland
  • Britain
  • Europe
  • glaciation
  • ancestral state reconstruction
  • Bayesian dating analysis
  • cave
  • phylogeography
  • glacial
  • survival
  • subterranean
  • crustacean
  • crustacea
  • amphipoda
  • climate change

Cite this

McInerney, C., Maurice, L., Robertson, A. L., Knight, L. R. F. D., Arnscheidt, J., Venditti, C., ... Haenfling, B. (2014). The Ancient Britons: Groundwater fauna survived extreme climate changes over tens of millions of years across NW Europe. 23(5), 1153-1166. https://doi.org/10.1111/mec.12664
McInerney, Caitriona ; Maurice, Louise ; Robertson, Anne L. ; Knight, Lee R.F.D. ; Arnscheidt, Joerg ; Venditti, Chris ; Dooley, James ; Mathers, Thomas ; Matthijs, Severine ; Eriksson, Karin ; Proudlove, Graham ; Haenfling, Bernd. / The Ancient Britons: Groundwater fauna survived extreme climate changes over tens of millions of years across NW Europe. 2014 ; Vol. 23, No. 5. pp. 1153-1166.
@article{cc971e4581bd4a2db0bcddf242f46a8b,
title = "The Ancient Britons: Groundwater fauna survived extreme climate changes over tens of millions of years across NW Europe",
abstract = "Global climate changes during the Cenozoic (65.5 - 0 Ma) caused major biological range shifts and extinctions. In Northern Europe, for example, a pattern of few endemics and the dominance of wide-ranging species is thought to have been determined by the Pleistocene (2.59 – 0.01 Ma) glaciations. This study, in contrast, reveals an ancient subsurface fauna endemic to Britain and Ireland. Using a Bayesian phylogenetic approach we found that two species of stygobitic invertebrates (genus Niphargus) have not only survived the entire Pleistocene in refugia but have persisted for at least 19.5 million years. Other Niphargus species form distinct cryptic taxa that diverged from their nearest continental relative between 5.6 and 1.0 Ma. The study also reveals an unusual biogeographical pattern in the Niphargus genus. It originated in Northwest Europe ~88 Ma and underwent a gradual range expansion. Phylogenetic diversity and species age are highest in Northwest Europe suggesting resilience to extreme climate change, and strongly contrasting the patterns seen in surface fauna. However, species diversity is highest in Southeast Europe indicating that once the genus spread to these areas (~ 25 Ma), geomorphological and climatic conditions enabled much higher diversification. Our study highlights that groundwater ecosystems provide an important contribution to biodiversity and offer insight into the interactions between biological and climatic processes.",
keywords = "groundwater, groundwater ecology, Niphargus, Ireland, Britain, Europe, glaciation, ancestral state reconstruction, Bayesian dating analysis, cave, phylogeography, glacial, survival, subterranean, crustacean, crustacea, amphipoda, climate change",
author = "Caitriona McInerney and Louise Maurice and Robertson, {Anne L.} and Knight, {Lee R.F.D.} and Joerg Arnscheidt and Chris Venditti and James Dooley and Thomas Mathers and Severine Matthijs and Karin Eriksson and Graham Proudlove and Bernd Haenfling",
note = "Reference text: Anderson MP (2005) Heat as a ground water tracer. Groundwater, 43, 951–968. B{\"o}hme M (2003) The Miocene Climatic Optimum: evidence from ectothermic vertebrates of Central Europe. Palaeogeography Palaeoclimatology Palaeoecology, 195, 389–401. B{\"o}hme M, Ilg A, Winklhofer M (2008) Late Miocene “washhouse” climate in Europe. Earth and Planetary Science Letters, 275, 393–401. Bouckaert R, Lemey P, Dunn M et al. (2012) Mapping the origins and expansion of the Indo-European language family. Science, 337, 957–960. Boulton GS, Caban PE, Vangijssel K (1995) Groundwater-flow beneath ice sheets. 1. Large-scale patterns. Quaternary Science Reviews, 14, 545–562. Busby J, Kingdon A, Williams J (2011) The measured shallow temperature field in Britain. Quarterly Journal of Engineering Geology and Hydrogeology, 44, 373–387. Chapin FS, Zavaleta ES, Eviner VT et al. (2000) Consequences of changing biodiversity. Nature, 405, 234–242.CrossRef, Cope JCW (1997) The Mesozoic and Tertiary history of the Irish Sea. In: Petroleum Geology of the Irish Sea and Adjacent Areas (eds Meadows NS, Trueblood SP, Hardman M, Cowan G), pp. 47–59. Geological Society of London, London. Dole-Olivier M-J, Castellarini JF, Coineau N et al. (2009) Towards an optimal sampling strategy to assess groundwater biodiversity: comparison across six European regions. Freshwater Biology, 54, 777–796. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. Plos Biology, 4, 699–710. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973. Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nature Reviews Microbiology, 6, 725–740. Dwyer GS, Chandler MA (2009) Mid-Pliocene sea level and continental ice volume based on coupled benthic Mg/Ca palaeotemperatures and oxygen isotopes. Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences, 367, 157–168. Eberhard SM, Halse SA, Williams MR, Scanlon MD, Cocking J, Barron HJ (2009) Exploring the relationship between sampling efficiency and short-range endemism for groundwater fauna in the Pilbara region, Western Australia. Freshwater Biology, 54, 885–901. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797. Englisch U, Coleman CO, W{\"a}gele JW (2003) First observations on the phylogeny of the families Gammaridae, Crangonyctidae, Melitidae, Niphargidae, Megaluropidae and Oedicerotidae (Amphipoda, Crustacea), using small subunit rDNA gene sequences. Journal of Natural History, 37, 2461–2486. Figura S, Livingstone DM, Hoehn E, Kipfer R (2011) Regime shift in groundwater temperature triggered by Arctic Oscillation. Geophysical Research Letters, 38, L23401. Fišer C, Sket B, Trontelj P (2008) A phylogenetic perspective on 160 years of troubled taxonomy of Niphargus (Crustacea: Amphipoda). Zoologica Scripta, 37, 665–680. Flot J (2010) Toward a molecular taxonomy of the amphipod genus Niphargus: examples of use of DNA sequences for species identification. Bulletin de la Soci{\'e}t{\'e} des sciences naturelles de l'Ouest de la France, 32, 62–68. Flot JF, Worheide G, Dattagupta S (2010) Unsuspected diversity of Niphargus amphipods in the chemoautotrophic cave ecosystem of Frasassi, central Italy. Bmc Evolutionary Biology, 10, 171. Foulquier A, Malard F, Lefebure T, Gibert J, Douady CJ (2008) The imprint of Quaternary glaciers on the present-day distribution of the obligate groundwater amphipod Niphargus virei (Niphargidae). Journal of Biogeography, 35, 552–564. Freckleton RP, Phillimore AB, Pagel M (2008) Relating traits to diversification: a simple test. American Naturalist, 172, 102–115. Galassi DMP, Stoch F, Fiasca B, Di Lorenzo T, Gattone E (2009) Groundwater biodiversity patterns in the Lessinian Massif of northern Italy. Freshwater Biology, 54, 830–847. Gibert J, Stanford JA, Dole-Olivier M-J, Ward JV (1994) Basic attributes of groundwater ecosystems and prospects for research. In: Groundwater Ecology (eds Gibert J, Danielopol DL & Standford JA), pp. 8–42. Academic Press, San Diego, California. Gupta S, Collier JS, Palmer-Felgate A, Potter G (2007) Catastrophic flooding origin of shelf valley systems in the English Channel. Nature, 448, U342–345.CrossRef, H{\"a}nfling B, Douterelo-Soler I, Knight L, Proudlove G (2008) Molecular studies on the Niphargus kochianus group (Crustacea: Amphipoda: Niphargidae) in Great Britain and Ireland. Cave and Karst Science, 35, 35–40. Hartke TR, Fišer C, Hohagen J, Klebera S, Hartmannd R, Koenemanne S (2011) Morphological and molecular analyses of closely related species in the stygobiontic genus Niphargus (Amphipoda). Journal of Crustacean Biology, 31, 701–709. Hay WH, DeConto RM, Wold CN, et al. (1999) Alternative global Cretaceous paleogeography. In: Evolution of the Cretaceous Ocean-Climate System Pages (eds Barrera E & Johnson CC), pp. 1–47. Geological Society of America, Boulder, Colorado. Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 359, 183–195. Hof C, Br{\"a}ndle M, Brandl R (2008) Latitudinal variation of diversity in European freshwater animals is not concordant across habitat types. Global Ecology and Biogeography, 17, 539–546. 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year = "2014",
month = "3",
doi = "10.1111/mec.12664",
language = "English",
volume = "23",
pages = "1153--1166",
number = "5",

}

McInerney, C, Maurice, L, Robertson, AL, Knight, LRFD, Arnscheidt, J, Venditti, C, Dooley, J, Mathers, T, Matthijs, S, Eriksson, K, Proudlove, G & Haenfling, B 2014, 'The Ancient Britons: Groundwater fauna survived extreme climate changes over tens of millions of years across NW Europe', vol. 23, no. 5, pp. 1153-1166. https://doi.org/10.1111/mec.12664

The Ancient Britons: Groundwater fauna survived extreme climate changes over tens of millions of years across NW Europe. / McInerney, Caitriona; Maurice, Louise; Robertson, Anne L.; Knight, Lee R.F.D.; Arnscheidt, Joerg; Venditti, Chris; Dooley, James; Mathers, Thomas; Matthijs, Severine; Eriksson, Karin; Proudlove, Graham; Haenfling, Bernd.

Vol. 23, No. 5, 03.2014, p. 1153-1166.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The Ancient Britons: Groundwater fauna survived extreme climate changes over tens of millions of years across NW Europe

AU - McInerney, Caitriona

AU - Maurice, Louise

AU - Robertson, Anne L.

AU - Knight, Lee R.F.D.

AU - Arnscheidt, Joerg

AU - Venditti, Chris

AU - Dooley, James

AU - Mathers, Thomas

AU - Matthijs, Severine

AU - Eriksson, Karin

AU - Proudlove, Graham

AU - Haenfling, Bernd

N1 - Reference text: Anderson MP (2005) Heat as a ground water tracer. Groundwater, 43, 951–968. Böhme M (2003) The Miocene Climatic Optimum: evidence from ectothermic vertebrates of Central Europe. Palaeogeography Palaeoclimatology Palaeoecology, 195, 389–401. Böhme M, Ilg A, Winklhofer M (2008) Late Miocene “washhouse” climate in Europe. Earth and Planetary Science Letters, 275, 393–401. Bouckaert R, Lemey P, Dunn M et al. (2012) Mapping the origins and expansion of the Indo-European language family. Science, 337, 957–960. Boulton GS, Caban PE, Vangijssel K (1995) Groundwater-flow beneath ice sheets. 1. Large-scale patterns. Quaternary Science Reviews, 14, 545–562. Busby J, Kingdon A, Williams J (2011) The measured shallow temperature field in Britain. Quarterly Journal of Engineering Geology and Hydrogeology, 44, 373–387. Chapin FS, Zavaleta ES, Eviner VT et al. (2000) Consequences of changing biodiversity. Nature, 405, 234–242.CrossRef, Cope JCW (1997) The Mesozoic and Tertiary history of the Irish Sea. In: Petroleum Geology of the Irish Sea and Adjacent Areas (eds Meadows NS, Trueblood SP, Hardman M, Cowan G), pp. 47–59. Geological Society of London, London. Dole-Olivier M-J, Castellarini JF, Coineau N et al. (2009) Towards an optimal sampling strategy to assess groundwater biodiversity: comparison across six European regions. Freshwater Biology, 54, 777–796. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. Plos Biology, 4, 699–710. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973. Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nature Reviews Microbiology, 6, 725–740. Dwyer GS, Chandler MA (2009) Mid-Pliocene sea level and continental ice volume based on coupled benthic Mg/Ca palaeotemperatures and oxygen isotopes. Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences, 367, 157–168. Eberhard SM, Halse SA, Williams MR, Scanlon MD, Cocking J, Barron HJ (2009) Exploring the relationship between sampling efficiency and short-range endemism for groundwater fauna in the Pilbara region, Western Australia. Freshwater Biology, 54, 885–901. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797. Englisch U, Coleman CO, Wägele JW (2003) First observations on the phylogeny of the families Gammaridae, Crangonyctidae, Melitidae, Niphargidae, Megaluropidae and Oedicerotidae (Amphipoda, Crustacea), using small subunit rDNA gene sequences. Journal of Natural History, 37, 2461–2486. Figura S, Livingstone DM, Hoehn E, Kipfer R (2011) Regime shift in groundwater temperature triggered by Arctic Oscillation. Geophysical Research Letters, 38, L23401. Fišer C, Sket B, Trontelj P (2008) A phylogenetic perspective on 160 years of troubled taxonomy of Niphargus (Crustacea: Amphipoda). Zoologica Scripta, 37, 665–680. Flot J (2010) Toward a molecular taxonomy of the amphipod genus Niphargus: examples of use of DNA sequences for species identification. Bulletin de la Société des sciences naturelles de l'Ouest de la France, 32, 62–68. Flot JF, Worheide G, Dattagupta S (2010) Unsuspected diversity of Niphargus amphipods in the chemoautotrophic cave ecosystem of Frasassi, central Italy. Bmc Evolutionary Biology, 10, 171. Foulquier A, Malard F, Lefebure T, Gibert J, Douady CJ (2008) The imprint of Quaternary glaciers on the present-day distribution of the obligate groundwater amphipod Niphargus virei (Niphargidae). Journal of Biogeography, 35, 552–564. Freckleton RP, Phillimore AB, Pagel M (2008) Relating traits to diversification: a simple test. American Naturalist, 172, 102–115. Galassi DMP, Stoch F, Fiasca B, Di Lorenzo T, Gattone E (2009) Groundwater biodiversity patterns in the Lessinian Massif of northern Italy. Freshwater Biology, 54, 830–847. Gibert J, Stanford JA, Dole-Olivier M-J, Ward JV (1994) Basic attributes of groundwater ecosystems and prospects for research. In: Groundwater Ecology (eds Gibert J, Danielopol DL & Standford JA), pp. 8–42. Academic Press, San Diego, California. Gupta S, Collier JS, Palmer-Felgate A, Potter G (2007) Catastrophic flooding origin of shelf valley systems in the English Channel. Nature, 448, U342–345.CrossRef, Hänfling B, Douterelo-Soler I, Knight L, Proudlove G (2008) Molecular studies on the Niphargus kochianus group (Crustacea: Amphipoda: Niphargidae) in Great Britain and Ireland. Cave and Karst Science, 35, 35–40. Hartke TR, Fišer C, Hohagen J, Klebera S, Hartmannd R, Koenemanne S (2011) Morphological and molecular analyses of closely related species in the stygobiontic genus Niphargus (Amphipoda). Journal of Crustacean Biology, 31, 701–709. Hay WH, DeConto RM, Wold CN, et al. (1999) Alternative global Cretaceous paleogeography. In: Evolution of the Cretaceous Ocean-Climate System Pages (eds Barrera E & Johnson CC), pp. 1–47. Geological Society of America, Boulder, Colorado. Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 359, 183–195. Hof C, Brändle M, Brandl R (2008) Latitudinal variation of diversity in European freshwater animals is not concordant across habitat types. Global Ecology and Biogeography, 17, 539–546. Holsinger JR, Mort JS, Recklies AD (1983) The subterranean crustacean fauna of Castleguard Cave, Columbia icefields, Alberta, Canada, and its zoogeographic significance. Arctic and Alpine Research, 15, 543–549. Hou ZE, Sket B, Fišer C, Li S (2011) Eocene habitat shift from saline to freshwater promoted Tethyan amphipod diversification. Proceedings of the National Academy of Sciences of the United States of America, 108, 14533–14538. Hrbek T, Meyer A (2003) Closing of the Tethys Sea and the phylogeny of Eurasian killifishes (Cyprinodontiformes: Cyprinodontidae). Journal of Evolutionary Biology, 16, 17–36. Hutchinson JN, Thomas-Betts A (1990) Extent of permafrost in southern Britain in relation to geothermal flux. Quarterly Journal of Engineering Geology, 23, 387–390. Illies J (1978) Limnofauna Europaea, 2nd edn. Gustav Fischer Verlag, Stuttgart. Jarvis I, Mabrouk A, Moody RTJ, de Cabrera S (2002) Late Cretaceous (Campanian) carbon isotope events, sea-level change and correlation of the Tethyan and Boreal realms. Palaeogeography Palaeoclimatology Palaeoecology, 188, 215–248. Jiang X-W, Wang X-S, Wan L (2010) Semi-empirical equations for the systematic decrease in permeability with depth in porous and fractured media. Hydrogeology Journal, 18, 839–850. Karaman GS, Ruffo S (1986) Amphipoda: Niphargus group (Niphargidae sensu Bousfield, 1982). In: Stygofauna Mundi (ed. Botosaneanu L), pp. 514–534. E.J. Brill, Leiden. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059–3066. Klaus S, Gross M (2010) Synopsis of the fossil freshwater crabs of Europe (Brachyura: Potamoidea: Potamidae). Neues Jahrbuch für Geologie und Paläontologie-Abhandlungen, 256, 39–59. 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PY - 2014/3

Y1 - 2014/3

N2 - Global climate changes during the Cenozoic (65.5 - 0 Ma) caused major biological range shifts and extinctions. In Northern Europe, for example, a pattern of few endemics and the dominance of wide-ranging species is thought to have been determined by the Pleistocene (2.59 – 0.01 Ma) glaciations. This study, in contrast, reveals an ancient subsurface fauna endemic to Britain and Ireland. Using a Bayesian phylogenetic approach we found that two species of stygobitic invertebrates (genus Niphargus) have not only survived the entire Pleistocene in refugia but have persisted for at least 19.5 million years. Other Niphargus species form distinct cryptic taxa that diverged from their nearest continental relative between 5.6 and 1.0 Ma. The study also reveals an unusual biogeographical pattern in the Niphargus genus. It originated in Northwest Europe ~88 Ma and underwent a gradual range expansion. Phylogenetic diversity and species age are highest in Northwest Europe suggesting resilience to extreme climate change, and strongly contrasting the patterns seen in surface fauna. However, species diversity is highest in Southeast Europe indicating that once the genus spread to these areas (~ 25 Ma), geomorphological and climatic conditions enabled much higher diversification. Our study highlights that groundwater ecosystems provide an important contribution to biodiversity and offer insight into the interactions between biological and climatic processes.

AB - Global climate changes during the Cenozoic (65.5 - 0 Ma) caused major biological range shifts and extinctions. In Northern Europe, for example, a pattern of few endemics and the dominance of wide-ranging species is thought to have been determined by the Pleistocene (2.59 – 0.01 Ma) glaciations. This study, in contrast, reveals an ancient subsurface fauna endemic to Britain and Ireland. Using a Bayesian phylogenetic approach we found that two species of stygobitic invertebrates (genus Niphargus) have not only survived the entire Pleistocene in refugia but have persisted for at least 19.5 million years. Other Niphargus species form distinct cryptic taxa that diverged from their nearest continental relative between 5.6 and 1.0 Ma. The study also reveals an unusual biogeographical pattern in the Niphargus genus. It originated in Northwest Europe ~88 Ma and underwent a gradual range expansion. Phylogenetic diversity and species age are highest in Northwest Europe suggesting resilience to extreme climate change, and strongly contrasting the patterns seen in surface fauna. However, species diversity is highest in Southeast Europe indicating that once the genus spread to these areas (~ 25 Ma), geomorphological and climatic conditions enabled much higher diversification. Our study highlights that groundwater ecosystems provide an important contribution to biodiversity and offer insight into the interactions between biological and climatic processes.

KW - groundwater

KW - groundwater ecology

KW - Niphargus

KW - Ireland

KW - Britain

KW - Europe

KW - glaciation

KW - ancestral state reconstruction

KW - Bayesian dating analysis

KW - cave

KW - phylogeography

KW - glacial

KW - survival

KW - subterranean

KW - crustacean

KW - crustacea

KW - amphipoda

KW - climate change

U2 - 10.1111/mec.12664

DO - 10.1111/mec.12664

M3 - Article

VL - 23

SP - 1153

EP - 1166

IS - 5

ER -