Skip to main content
SpringerLink
Log in

Rocks and clocks: linking geologic history and rates of genetic differentiation in anchialine organisms

  • ANCHIALINE ECOSYSTEMS
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The geologic history of a region can significantly impact the development of its flora and fauna, with past events shaping community patterns and evolutionary trajectories of species. In this context, islands are excellent “natural laboratories” for studying the fundamental processes of evolution due to their discrete geographical nature and dynamic geologic histories. An island system meeting these criteria is the Hawaiian Archipelago, which is ideal for testing how island geologic history influences the processes leading to population genetic variation and differentiation. One Hawaiian endemic whose evolutionary history is closely tied to the geology of the islands is the anchialine atyid shrimp Halocaridina, whose mitochondrial cytochrome oxidase I (COI) gene is hypothesized to be evolving at the rate of 20% per million years. To validate this rapid evolutionary rate, time since divergence estimates between geographically close, yet genetically distinct, populations were calculated for Halocaridina from anchialine habitats on the islands of Hawai’i, Maui, and O’ahu. On the younger (i.e., <1.5 million years) islands of Hawai’i and Maui, where all anchialine habitats occur in basalt, application of the Halocaridina molecular clock identified a strong correlation between levels of genetic divergence and the geologic age of the region inhabited by those populations. In contrast, this relationship weakened when similar analyses were conducted for Halocaridina from limestone anchialine habitats on the older (i.e., >2.75 million years) island of O’ahu. These results suggest geologic age, basin origin and/or composition are important factors that should be taken into consideration when conducting molecular clock analyses on anchialine flora and fauna as well as island populations in general.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Avise, J. C., 2004. Molecular markers, natural history, and evolution. Sinauer Associates Inc., Sunderland.

    Google Scholar 

  • Bailey-Brock, J. H. & R. E. Brock, 1993. Feeding, reproduction, and sense organs of the Hawaiian anchialine shrimp Halocaridina rubra (Atyidea). Pacific Science 47: 338–355.

    Google Scholar 

  • Brock, R. E., 1985. An assessment of the conditions and future of the anchialine pond resources of the Hawaiian Islands. Prepared for Transcontinental Development Co., Honolulu.

    Google Scholar 

  • Brock, R. E. & J. H. Bailey-Brock, 1998. A unique anchialine pool in the Hawaiian Islands. International Review of Hydrobiology 83: 65–75.

    Article  CAS  Google Scholar 

  • Brock, R. E. & A. K. H. Kam, 1997. Biological and water quality characteristics of anchialine resources in Kaloko-Honokohau National Historical Park. Technical report 112. Cooperative National Park Resources Studies Unit, University of Hawaii at Manoa.

  • Brower, A. V. Z., 1994. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proceedings of the National Academy of Science USA 91: 6491–6495.

    Article  CAS  Google Scholar 

  • Burridge, C. P., D. Craw & J. M. Waters, 2006. River capture, range expansion, and cladogenesis: the genetic signature of freshwater vicariance. Evolution 60: 1038–1049.

    CAS  PubMed  Google Scholar 

  • Burridge, C. P., D. Craw, D. Fletcher & J. M. Waters, 2008. Geological dates and molecular rates: fish DNA sheds light on time dependency. Molecular Biology and Evolution 25: 624–633.

    Article  CAS  PubMed  Google Scholar 

  • Carson, H. L. & D. A. Clague, 1995. Geology and biogeography of the Hawaiian Islands. In Wagner, W. L. & V. A. Funk (eds), Hawaiian Biogeography Evolution on a Hot Spot Archipelago. Smithsonian Institution Press, Washington: 14–29.

    Google Scholar 

  • Clement, M., D. Posada & K. A. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659.

    Article  CAS  PubMed  Google Scholar 

  • Craft, J. D., A. D. Russ, M. N. Yamamoto, T. Y. Iwai, S. Hau, J. Kahiapo, C. T. Chong, S. Ziegler-Chong, C. Muir, Y. Fujita, D. A. Polhemus, R. A. Kinzie & S. R. Santos, 2008. Islands under islands: The phylogeography and evolution of Halocaridina rubra Holthuis, 1963 (Crustacean: Decapoda: Atyidae) in the Hawaiian archipelago. Limnology and Oceanography 53: 675–689.

    Article  Google Scholar 

  • Emerson, B. C., 2002. Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Molecular Ecology 11: 951–966.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L. & S. Schneider, 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50.

    CAS  Google Scholar 

  • Fletcher III, C. H., C. V. Murrary-Wallace, C. R. Glenn, C. E. Sherman, B. Popp & A. Hessler, 2006. Age and origin of late Quaternary Eolianite, Kaiehu Point (Moomomi), Molokai, Hawaii. Journal of Coastal Research 42: 97–112.

    Google Scholar 

  • Finston, T. L., M. S. Johnson, W. F. Humphreys, S. M. Ebergard & S. A. Halse, 2007. Cryptic speciation in two widespread subterranean amphipod genera reflects historical drainage patterns in an ancient landscape. Molecular Ecology 16: 355–365.

    Article  CAS  PubMed  Google Scholar 

  • Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.

    CAS  PubMed  Google Scholar 

  • Fu, Y., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925.

    CAS  PubMed  Google Scholar 

  • Fukatsu, T., 1999. Acetone preservation: a practical technique for molecular analysis. Molecular Ecology 8: 1935–1945.

    Article  CAS  PubMed  Google Scholar 

  • Funk, V. A. & W. L. Wagner, 1995. Biogeographic patterns in the Hawaiian Islands. In Funk, V. A. & W. L. Wagner (eds), Hawaiian Biogeography: Evolution on a Hot Spot Archipelago. Smithsonian Institution Press, Washington: 379–419.

    Google Scholar 

  • Grossman, E. E. & C. H. Fletcher III, 2004. Holocene reef development where wave energy reduces accommodation space, Kailua Bay, windward Oahu, Hawaii, U.S.A. Journal of Sedimentary Research 74: 49–63.

    Article  CAS  Google Scholar 

  • Hasegawa, M., H. Kishino & T. Yano, 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160–174.

    Article  CAS  PubMed  Google Scholar 

  • Ho, S. Y. W. & G. Larson, 2006. Molecular clocks: when times are a-changin’. Trends in Genetics 22: 79–83.

    Article  CAS  PubMed  Google Scholar 

  • Ho, S. Y. W., U. Saarma, R. Barnett, J. Haile & B. Shapiro, 2008. The effect of inappropriate calibration: three case studies in molecular ecology. PLoS ONE 3: e1615.

    Article  PubMed  Google Scholar 

  • Holthuis, L. B., 1973. Caridean shrimps found in land-locked saltwater pools at four Indo-West Pacific localities (Sinai Peninsula, Funafuti Atoll, Maui and Hawai’i islands), with the description of one new genus and four new species. Zoologische Verhandelingen (Leiden) 128: 1–48.

    Google Scholar 

  • Hudson, R. R., 2000. A new statistic for detecting genetic differentiation. Genetics 155: 2011–2014.

    CAS  PubMed  Google Scholar 

  • Ivey, J. L. & S. R. Santos, 2007. The complete mitochondrial genome of the Hawaiian anchialine shrimp Halocaridina rubra Holthuis, 1963 (Crustacea: Decapoda: Atyidae). Gene 394: 35–44.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S., K. Tamura & M. Nei, 2004. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5: 150–163.

    Article  CAS  PubMed  Google Scholar 

  • Lau, L. S. & J. F. Mink, 2006. Hydrology of the Hawaiian Islands. University of Hawaii Press, Honolulu.

    Google Scholar 

  • MacArthur, R. H. & E. O. Wilson, 1967. The Theory of Island Biogeography. Princeton University Press, Princeton.

    Google Scholar 

  • Macdonald, G. A., A. T. Abbott & F. L. Peterson, 1983. Volcanoes in the Sea: The Geology of Hawaii. University of Hawaii Press, Honolulu.

    Google Scholar 

  • Maciolek, J. A., 1983. Distribution and biology of Indo-Pacific insular hypogeal shrimp. Bulletin of Marine Science 33: 606–618.

    Google Scholar 

  • Maciolek, J.A. & R.E. Brock, 1974. Aquatic survey of the Kona coast ponds, Hawaii Island. Sea Grant Advisory Report, UNIHI-SEAGRANT-AR-74-04.

  • Nei, M., 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.

    Google Scholar 

  • Nielsen, R. & W. Wakeley, 2001. Distinguishing migration from isolation: an MCMC approach. Genetics 158: 885–896.

    CAS  PubMed  Google Scholar 

  • Page, T. J. & J. M. Hughes, 2007. Phylogeographic structure in an Australian freshwater shrimp largely pre-dates the geological origins of its landscape. Heredity 98: 222–231.

    Article  CAS  PubMed  Google Scholar 

  • Page, T. J., W. F. Humphreys & J. M. Hughes, 2008. Shrimps down under: evolutionary relationships of subterranean crustaceans from Western Australia (Decapoda: Atyidae: Stygiocaris). PLoS ONE 3: e1618.

    Article  PubMed  Google Scholar 

  • Penny, D., 2005. Relativity for molecular clocks. Nature 426: 183–184.

    Article  Google Scholar 

  • Rozas, J., J. Sanchez-DelBarrio, X. Messeguer & R. Rozas, 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496–2497.

    Article  CAS  PubMed  Google Scholar 

  • Santos, S. R., 2006. Patterns of genetic connectivity among anchialine habitats: a case study of the endemic Hawaiian shrimp Halocaridina rubra on the Island of Hawai’i. Molecular Ecology 15: 2699–2718.

    Article  CAS  PubMed  Google Scholar 

  • Sherrod, D.R., J.M. Sinton, S.E. Watkins & K.M. Brunt, 2007. Geologic map of the State of Hawaii: U.S. Geological Survey Open-File Report 2007-1089. http://pubs.usgs.gov/of/2007/1089/.

  • Sket, B., 1996. The ecology of anchialine caves. Trends in Ecology and Evolution 11: 221–225.

    Article  CAS  PubMed  Google Scholar 

  • Szabo, B. J., K. R. Ludwidg, D. R. Muhs & K. R. Simmons, 1994. Thorium-230 ages of corals and duration of the last interglacial sea-level high stand on Oahu, Hawaii. Science 266: 93–96.

    Article  CAS  PubMed  Google Scholar 

  • Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

    CAS  PubMed  Google Scholar 

  • Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526.

    CAS  PubMed  Google Scholar 

  • Vandergast, A. G., R. G. Gillespie & G. K. Roderick, 2004. Influence of volcanic activity on the population genetic structure of Hawaiian Tetragnatha spiders: fragmentation, rapid population growth and the potential for accelerated evolution. Molecular Ecology 13: 1729–1743.

    Article  CAS  PubMed  Google Scholar 

  • Waters, J. M., D. L. Rowe, S. Apte, T. M. King, G. P. Wallis, L. Anderson, R. J. Norris, D. Craw & C. P. Burridge, 2007. Geological dates and molecular rates: rapid divergence of rivers and their biotas. Systematic Biology 56: 271–282.

    Article  CAS  PubMed  Google Scholar 

  • Weese, D. A. & S. R. Santos, 2009. Genetic identification of source populations for an aquarium-traded invertebrate. Animal Conservation 12: 13–19.

    Article  Google Scholar 

  • Williams, S. T. & N. Knowlton, 2001. Mitochondrial pseudogenes are pervasive and often insidious in the snapping shrimp genus Alpheus. Molecular Biology and Evolution 18: 1484–1493.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Dr. Bill Gilmartin for allowing sampling of Halocaridina from the anchialine habitats at Wai’ohinu, Skippy Hau (State of Hawai’i Division of Aquatic Resources, Maui) and John Kahiapo (State of Hawai’i Division of Aquatic Resources, Hawaii) for additional assistance in field collections and Dr. Ken M. Halanych for suggestions leading to the title of this manuscript. Dr. Timothy J. Page (Griffith University, Australia) and one anonymous reviewer provided valuable comments that improved this contribution. This work was funded in part by National Science Foundation grant DEB-0949855 (SRS) and represents contributions #73 and #1 to the Auburn University (AU) Marine Biology Program and Molette Biology Laboratory for Environmental and Climate Change Studies, respectively.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Cell & Molecular Biosciences Peak Program and Molette Biology Laboratory for Environmental and Climate Change Studies, Auburn University, 101 Life Sciences Building, Auburn, AL, 36849-5407, USA

    Scott R. Santos & David A. Weese

Authors
  1. Scott R. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David A. Weese
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Scott R. Santos.

Additional information

Guest editors: C. Wicks & W. F. Humphreys / Anchialine Ecosystems: reflections and prospects

Rights and permissions

Reprints and permissions

About this article

Cite this article

Santos, S.R., Weese, D.A. Rocks and clocks: linking geologic history and rates of genetic differentiation in anchialine organisms. Hydrobiologia 677, 53–64 (2011). https://doi.org/10.1007/s10750-010-0588-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-010-0588-x

Keywords

Search

Navigation