Article

Cradles and museums of Antarctic teleost biodiversity

  • Nature Ecology & Evolution 113791384 (2017)
  • doi:10.1038/s41559-017-0239-y
  • Download Citation
Received:
Accepted:
Published online:

Abstract

Isolated in one of the most extreme marine environments on Earth, teleost fish diversity in Antarctica’s Southern Ocean is dominated by one lineage: the notothenioids. Throughout the past century, the long-term persistence of this unique marine fauna has become increasingly threatened by regional atmospheric and, to a lesser extent oceanic, warming. Developing an understanding of how historical temperature shifts have shaped source–sink dynamics for Antarctica’s teleost lineages provides critical insight for predicting future demographic responses to climate change. We use a combination of phylogenetic and biogeographic modelling to show that high-latitude Antarctic nearshore habitats have been an evolutionary sink for notothenioid species diversity. Contrary to expectations from island biogeographic theory, lower latitude regions of the Southern Ocean that include the northern Antarctic Peninsula and peripheral island archipelagos act as source areas to continental diversity. These peripheral areas facilitate both the generation of new species and repeated colonization of nearshore Antarctic continental regions. Our results provide historical context to contemporary trends of global climate change that threaten to invert these evolutionary dynamics.

  • Subscribe to Nature Ecology & Evolution for full access:

    $99

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    Near, T. J. et al. Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proc. Natl Acad. Sci. USA 109, 3434–3439 (2012).

  2. 2.

    Clarke, A. & Alistair Crame, J. The origin of the Southern Ocean marine fauna. Geol. Soc. London Spec. Publ. 47, 253–268 (1989).

  3. 3.

    Dell, R. K. in Advances in Marine Biology Vol. 10 (eds Russell, F. S. & Yonge, M.) 1–216 (1972).

  4. 4.

    Thatje, S., Hillenbrand, C.-D. & Larter, R. On the origin of Antarctic marine benthic community structure. Trends Ecol. Evol. 20, 534–540 (2005).

  5. 5.

    Allcock, A. L. & Strugnell, J. M. Southern Ocean diversity: new paradigms from molecular ecology. Trends Ecol. Evol. 27, 520–528 (2012).

  6. 6.

    Fraser, C. I., Nikula, R., Ruzzante, D. E. & Waters, J. M. Poleward bound: biological impacts of Southern Hemisphere glaciation. Trends Ecol. Evol. 27, 462–471 (2012).

  7. 7.

    Goldberg, E. E., Roy, K., Lande, R. & Jablonski, D. Diversity, endemism, and age distributions in macroevolutionary sources and sinks. Am. Nat. 165, 623–633 (2005).

  8. 8.

    Constable, A. Managing fisheries to conserve the Antarctic marine ecosystem: practical implementation of the Convention on the Conservation of Antarctic Marine Living Resources (CCAMLR). ICES J. Mar. Sci. 57, 778–791 (2000).

  9. 9.

    Clarke, A., Andrew, C. & Johnston, I. A. Evolution and adaptive radiation of Antarctic fishes. Trends Ecol. Evol. 11, 212–218 (1996).

  10. 10.

    Matschiner, M., Hanel, R. & Salzburger, W. On the origin and trigger of the notothenioid adaptive radiation. PLoS ONE 6, e18911 (2011).

  11. 11.

    La Mesa, M., Eastman, J. T. & Vacchi, M. The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review. Polar Biol. 27, 321–338 (2004).

  12. 12.

    Hutsemekers, V. et al. Oceanic islands are not sinks of biodiversity in spore-producing plants. Proc. Natl Acad. Sci. USA 108, 18989–18994 (2011).

  13. 13.

    Clarke, A., Barnes, D. K. A. & Hodgson, D. A. How isolated is Antarctica? Trends Ecol. Evol. 20, 1–3 (2005).

  14. 14.

    Thatje, S., Hillenbrand, C.-D., Mackensen, A. & Larter, R. Life hung by a thread: endurance of Antarctic fauna in glacial periods. Ecology 89, 682–692 (2008).

  15. 15.

    Matzke, N. J. Model selection in historical biogeography reveals that founder-event speciation is a crucial process in Island Clades. Syst. Biol. 63, 951–970 (2014).

  16. 16.

    Patiño, J. et al. Approximate Bayesian computation reveals the crucial role of oceanic islands for the assembly of continental biodiversity. Syst. Biol. 64, 579–589 (2015).

  17. 17.

    Moon, K. L., Chown, S. L. & Fraser, C. I. Reconsidering connectivity in the sub-Antarctic. Biol. Rev. https://doi.org/10.1111/brv.12327 (2017).

  18. 18.

    Chown, S. L. et al. Continent-wide risk assessment for the establishment of nonindigenous species in Antarctica. Proc. Natl Acad. Sci. USA 109, 4938–4943 (2012).

  19. 19.

    Byrne, M., Gall, M., Wolfe, K. & Agüera, A. From pole to pole: the potential for the Arctic seastar Asterias amurensis to invade a warming Southern Ocean. Glob. Change Biol. 22, 3874–3887 (2016).

  20. 20.

    Aronson, R. B. et al. Climate change and invasibility of the Antarctic benthos. Annu. Rev. Ecol. Evol. Syst. 38, 129–154 (2007).

  21. 21.

    Smith, C. R. et al. A large population of king crabs in Palmer Deep on the West Antarctic Peninsula shelf and potential invasive impacts. Proc. R. Soc. B. 279, 1017–1026 (2012).

  22. 22.

    Aronson, R. B., Frederich, M., Price, R. & Thatje, S. Prospects for the return of shell-crushing crabs to Antarctica. J. Biogeogr. 42, 1–7 (2014).

  23. 23.

    Helmus, M. R., Mahler, D. L. & Losos, J. B. Island biogeography of the Anthropocene. Nature 513, 543–546 (2014).

  24. 24.

    Pecl, G. T. et al. Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355, eaai9214 (2017).

  25. 25.

    Martinson, D. G., Stammerjohn, S. E., Iannuzzi, R. A., Smith, R. C. & Vernet, M. Western Antarctic Peninsula physical oceanography and spatio–temporal variability. Deep-Sea Res. II 55, 1964–1987 (2008).

  26. 26.

    Roemmich, D. et al. Unabated planetary warming and its ocean structure since 2006. Nat. Clim. Change 5, 240–245 (2015).

  27. 27.

    Mulvaney, R. et al. Recent Antarctic Peninsula warming relative to Holocene climate and ice-shelf history. Nature 489, 141–144 (2012).

  28. 28.

    Kawaguchi, S. et al. Risk maps for Antarctic krill under projected Southern Ocean acidification. Nat. Clim. Change 3, 843–847 (2013).

  29. 29.

    McNeil, B. I. & Matear, R. J. Southern Ocean acidification: a tipping point at 450-ppm atmospheric CO2. Proc. Natl Acad. Sci. USA 105, 18860–18864 (2008).

  30. 30.

    Bilyk, K. T. & Devries, A. L. Heat tolerance and its plasticity in Antarctic fishes. Comp. Biochem. Physiol. A 158, 382–390 (2011).

  31. 31.

    Li, C., Orti, G., Zhang, G. & Lu, G. A practical approach to phylogenomics: the phylogeny of ray-finned fish (Actinopterygii) as a case study. BMC Evol. Biol. 7, 44 (2007).

  32. 32.

    Near, T. J., Pesavento, J. J. & Cheng, C. H. C. Mitochondrial DNA, morphology, and the phylogenetic relationships of Antarctic icefishes (Notothenioidei: Channichthyidae). Mol. Phylogenet. Evol. 28, 87–98 (2003).

  33. 33.

    Kocher, T. D., Conroy, J. A., McKaye, K. R., Stauffer, J. R. & Lockwood, S. F. Evolution of NADH dehydrogenase subunit 2 in east African cichlid fish. Mol. Phylogenet. Evol. 4, 420–432 (1995).

  34. 34.

    Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

  35. 35.

    Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).

  36. 36.

    Drummond, A. J. & Bouckaert, R. R. Bayesian Evolutionary Analysis with BEAST (Cambridge Univ. Press, Cambridge, 2015).

  37. 37.

    Near, T. J. et al. Identification of the notothenioid sister lineage illuminates the biogeographic history of an Antarctic adaptive radiation. BMC Evol. Biol. 15, 109 (2015).

  38. 38.

    Rutschmann, S. et al. Parallel ecological diversification in Antarctic notothenioid fishes as evidence for adaptive radiation. Mol. Ecol. 20, 4707–4721 (2011).

  39. 39.

    Dornburg, A., Townsend, J. P., Friedman, M. & Near, T. J. Phylogenetic informativeness reconciles ray-finned fish molecular divergence times. BMC Evol. Biol. 14, 169 (2014).

  40. 40.

    Near, T. J. Estimating divergence times of notothenioid fishes using a fossil-calibrated molecular clock. Antarct. Sci. 16, 37–44 (2004).

  41. 41.

    Near, T. J. et al. Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes. Proc. Natl Acad. Sci. USA 110, 12738–12743 (2013).

  42. 42.

    Drummond, A. J., Ho, S. Y. W., Phillips, M. J. & Rambaut, A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006).

  43. 43.

    Terauds, A. et al. Conservation biogeography of the Antarctic. Divers. Distrib. 18, 726–741 (2012).

  44. 44.

    Tyler, P. & Paul, T. in Biogeographic Atlas of the Southern Ocean (eds de Broyer, C. & Koubbi, P.) 328–362 (Scientific Committee on Antarctic Research, Cambridge, 2014).

  45. 45.

    Miller, R. G. History and Atlas of the Fshes of the Antarctic Ocean (Foresta Institute for Ocean and Mountain Studies, Carson City, 1993).

  46. 46.

    Ree, R. H. & Smith, S. A. Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst. Biol. 57, 4–14 (2008).

  47. 47.

    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, Cambridge, 2007).

  48. 48.

    Bostock, M., Ogievetsky, V. & Heer, J. D3: data-driven documents. IEEE Trans. Vis. Comput. Graph. 17, 2301–2309 (2011).

  49. 49.

    Smith, S. A. Taking into account phylogenetic and divergence-time uncertainty in a parametric biogeographical analysis of the Northern Hemisphere plant clade Caprifolieae. J. Biogeogr. 36, 2324–2337 (2009).

  50. 50.

    Claeskens, G. & Hjort, N. L. Model Selection and Model Averaging (Cambridge Univ. Press, Cambridge, 2008).

  51. 51.

    Li, W. L. S. & Drummond, A. J. Model averaging and Bayes factor calculation of relaxed molecular clocks in Bayesian phylogenetics. Mol. Biol. Evol. 29, 751–761 (2012).

  52. 52.

    Alfaro, M. E. & Huelsenbeck, J. P. Comparative performance of Bayesian and AIC-based measures of phylogenetic model uncertainty. Syst. Biol. 55, 89–96 (2006).

  53. 53.

    Dornburg, A., Santini, F. & Alfaro, M. E. The influence of model averaging on clade posteriors: an example using the triggerfishes (Family Balistidae). Syst. Biol. 57, 905–919 (2008).

  54. 54.

    Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2011).

  55. 55.

    Waters, J. M., Fraser, C. I. & Hewitt, G. M. Founder takes all: density-dependent processes structure biodiversity. Trends Ecol. Evol. 28, 78–85 (2013).

  56. 56.

    Ettinger, A. & HilleRisLambers, J. Competition and facilitation may lead to asymmetric range shift dynamics with climate change. Glob. Change Biol. https://doi.org/10.1111/gcb.13649 (2017).

  57. 57.

    Jablonski, D., Roy, K. & Valentine, J. W. Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient. Science 314, 102–106 (2006).

  58. 58.

    Kennicutt, M. C. II et al. Polar research: six priorities for Antarctic science. Nature 512, 23–25 (2014).

  59. 59.

    Meredith, M. P. & King, J. C. Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys. Res. Lett. 32, L19604 (2005).

  60. 60.

    Somero, G. N. The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J. Exp. Biol. 213, 912–920 (2010).

Download references

Acknowledgements

We thank the NCSM ichthyology research unit, members of the Donoghue and Near Laboratory groups and attendees of the 2016 Verrill Medal Symposium at the Peabody Museum of Natural History for helpful discussions of this work, and K. Zapfe for help with illustrations. A.D.L was supported by a North Carolina State University undergraduate research fellowship. T.J.N was supported by the National Science Foundation (ANT-1341661) and the Bingham Oceanographic Fund of the Peabody Museum of Natural History, Yale University, and the students, staff and fellows of Saybrook College.

Author information

Affiliations

  1. North Carolina Museum of Natural Sciences, Raleigh, NC, 27601, USA

    • Alex Dornburg
    •  & April D. Lamb
  2. Department of Ecology and Evolutionary Biology, Yale Universitsy, New Haven, CT, 06520, USA

    • Sarah Federman
    •  & Thomas J. Near
  3. Department of Biological Sciences, North Carolina State University, Raleigh, NC, 27695, USA

    • April D. Lamb
  4. Southwest Fisheries Science Center, National Marine Fisheries Service, NOAA, La Jolla, CA, 92037, USA

    • Christopher D. Jones
  5. Peabody Museum of Natural History, Yale University, New Haven, CT, 06520, USA

    • Thomas J. Near

Authors

  1. Search for Alex Dornburg in:

  2. Search for Sarah Federman in:

  3. Search for April D. Lamb in:

  4. Search for Christopher D. Jones in:

  5. Search for Thomas J. Near in:

Contributions

A.D. and T.J.N. designed the study. C.D.J. and T.J.N. collected data. A.D., A.D.L. and T.J.N. performed analyses. A.D., A.D.L., S.F. and T.J.N. wrote the initial manuscript. C.D.J. contributed to the subsequent writing and development of the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Alex Dornburg.

Electronic supplementary material

  1. Supplementary Information

    Supplementary Figures 1–3 and Supplementary Table 1