Rapid evolutionary dynamics and disease threats to biodiversity

https://doi.org/10.1016/j.tree.2003.08.013Get rights and content

Abstract

Existing and emerging pathogens pose unusual challenges for conservation because of their potential to drive rapid changes in the numerical abundance and genetic composition of wild host populations. An increasing number of studies indicate that host genetic diversity plays an important role in buffering populations against widespread epidemics, and that parasites represent powerful selective agents in natural populations. The observation that infectious diseases might be both mitigated by and rapidly change the genetic composition of host populations gives new significance to the role of host genetic diversity in species conservation. Less clear is the role that pathogen evolutionary change plays in the emergence and spread of new diseases, but recent examples indicate that humans might be selecting unknowingly for rapid changes in pathogen biology through habitat fragmentation, climate shifts and environmental pollution. Although the risks they pose to endangered species are apparent, pathogens and other natural enemies can be a driving force behind species and genetic diversity in natural populations, and preserving interacting networks of coevolving populations should enable hosts to respond better to future disease threats.

Section snippets

Patterns in wild populations

Parasites are likely to be powerful selective agents in natural populations, and host species exposed to a diverse array of parasites should harbor a variety of resistance alleles or a repertoire of inducible defenses. Many studies have underscored the importance of genetic variation in host resistance in causing disease patterns in both field and experimental settings (Table 1). Parasites infecting sheep, snails, fish, moths and other animals have been implicated in the maintenance of allelic

Pathogen evolution and emerging diseases

The evolutionary potential of pathogens sets them apart from other major threats to wildlife, in part because of the unpredictable and irreversible effects of introduced diseases. Most pathogens have short generation times and large population sizes, and strong selection pressures following ecological changes might accelerate pathogen evolution. Human-imposed selection deriving from the widespread application of chemical controls is responsible largely for the emergence of drug-resistant

Full coevolutionary dynamics

Most examples from wild host–parasite systems point to neither host nor parasite evolution operating alone, but to joint coevolutionary dynamics (Table 1). Long-term studies of model host–parasite systems emphasize multiple coevolutionary processes and outcomes (see example in Box 3), including directional selection in favour of increased host resistance and shifts in parasite virulence [74], frequency-dependent selection leading to time-lagged cycles in host and parasite abundance and genotype

Consequences for biodiversity and conservation

Although habitat loss and overexploitation remain major factors in host population declines and extinctions, infectious diseases have become increasingly important factors in wildlife conservation 1, 2. ‘Virgin ground’ epidemics following novel introductions progress rapidly through previously unexposed populations, often causing high case fatality rates and stunning reductions in host abundance 5, 6. Introduced diseases have been implicated in the declines and, in some cases, extinctions of

Acknowledgements

This work was initiated as part of the ‘Disease and Conservation’ working group organized by Andy Dobson and supported by the National Center for Ecological Analysis and Synthesis, a Center funded by NSF (Grant #DEB–94–21535), the University of California at Santa Barbara, and the State of California. We thank Amy Pedersen, Leslie Real, Andrew Davis, Peter Thrall, Priyanga Amarasekare, Peter Hudson, and three anonymous reviewers for helpful discussion and comments.

References (98)

  • S. Culloty

    An investigation into the relative resistance of Irish flat oysters Ostrea edulis L. to the parasite Bonamia ostreae (Pichot et al. 1980)

    Aquaculture

    (2001)
  • C.D. Harvell

    Emerging marine diseases – climate links and anthropogenic factors

    Science

    (1999)
  • P. Daszak

    Emerging infectious diseases of wildlife –threats to biodiversity and human health

    Science

    (2000)
  • K. Lafferty et al.

    Good medicine for conservation biology: the intersection of epidemiology and conservation theory

    Conserv. Biol.

    (2002)
  • M.E. Roelke-Parker

    A canine distemper virus epidemic in Serengeti lions (Panthera leo)

    Nature

    (1996)
  • T. Jensen

    Another phocine distemper outbreak in Europe

    Science

    (2002)
  • W.M. Hochachka et al.

    Density-dependent decline of host abundance resulting from a new infectious disease

    Proc. Natl. Acad. Sci. U. S. A.

    (2000)
  • S.M. Funk

    The role of disease in carnivore ecology and conservation

  • A.M. Lyles et al.

    Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites

    J. Zoo Wildl. Med.

    (1993)
  • L.H. Taylor

    Risk factors for human disease emergence

    Proc. R. Soc. Lond. Ser. B

    (2001)
  • A. Dobson et al.

    Emerging infectious pathogens of wildlife

    Philos. Trans. R. Soc. London Ser. B

    (2001)
  • R. Lande

    Genetics and demography in biological conservation

    Science

    (1988)
  • S.M. Scheiner et al.

    Measuring natural selection on phenotypic plasticity

    Evolution

    (1999)
  • D.N. Reznick

    Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata)

    Science

    (1997)
  • J.J. Burdon et al.

    Changed patterns of resistance in a population of Linum marginale attacked by the rust pathogen Melampsora lini

    J. Ecol.

    (1995)
  • M.F. Dybdahl et al.

    Host parasite coevolution: evidence for rare advantage and time-lagged selection in a natural population

    Evolution

    (1998)
  • T.J. Little et al.

    Temporal patterns of genetic variation for resistance and infectivity in a Daphnia-microparasite system

    Evolution

    (2001)
  • T.J. Little et al.

    Associations between parasitism and host genotype in natural populations of Daphnia (Crustacea: Cladocera)

    J. Anim. Ecol.

    (1999)
  • S. Cleaveland

    Diseases of humans and their domestic mammals: pathogen characteristics, host range, and the risk of emergence

    Philos. Trans. R. Soc. London Ser. B

    (2001)
  • G. Dwyer

    Host heterogeneity and the dynamics of infectious disease: tests of a mathematical model

    Am. Nat.

    (1997)
  • J. Jokela et al.

    Spatial variation for infection by digenetic trematodes in a population of freshwater snails (Potamopyrgus antipodarum)

    Oecologia

    (1995)
  • D.W. Coltman

    Parasite-mediated selection against inbred Soay sheep in a free-living island population

    Evolution

    (1999)
  • P.W. Hedrick

    Parasite resistance and genetic variation in the endangered Gila topminnow

    Anim. Conserv.

    (2001)
  • M.A. Parker

    Disease and plant population genetic structure

  • H.M. Alexander

    Population dynamics and genetics of plant diseases: a case study of anther-smut disease of Silene alba caused by the fungus Ustilago violacea

    Ecology

    (1996)
  • J.J. Burdon et al.

    Spatial and temporal patterns in coevolving plant and pathogen associations

    Am. Nat.

    (1999)
  • P. Thrall et al.

    Evolution of virulence in a plant host–pathogen metapopulation

    Science

    (2003)
  • J. Seger et al.

    Parasites and sex

  • C.M. Lively et al.

    Genetic diversity in host–parasite interactions

  • K. Acevedo-Whitehouse

    Disease susceptibility in California sea lions

    Nature

    (2003)
  • C.M. Lively

    The Red Queen hypothesis supported by parasitism in sexual and clonal fish

    Nature

    (1990)
  • J. Antonovics et al.

    The cost of resistance and the maintenance of genetic polymorphism in host–pathogen systems

    Proc. R. Soc. Lond. Ser. B

    (1994)
  • T. Mitchell-Olds et al.

    Genetics of Brassica rapa. 3. Costs of disease resistance to three fungal pathogens

    Evolution

    (1996)
  • T. Koskela

    Resistance and tolerance in a host plant-holoparasitic interaction: genetic variation and costs

    Evolution

    (2002)
  • C.M. Lively

    Parthenogenesis in a freshwater snail: reproductive assurance versus parasitic release

    Evolution

    (1992)
  • V. Apanius

    Island and taxon effects in parasitism and resistance of lesser Antillean birds

    Ecology

    (2000)
  • D. Ebert

    Within and between population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa

    Proc. R. Soc. Lond. Ser. B

    (1998)
  • J.A. Shykoff

    Anther smut disease in Dianthus silvester (Caryophyllaceae): natural selection on floral traits

    Evolution

    (1997)
  • R. Medel

    Assessment of parasite-mediated selection in a host–parasite system in plants

    Ecology

    (2000)
  • Cited by (412)

    • Use of Trait Surrogates to Conserve the Nameless: A Meta-Analysis

      2022, Imperiled: The Encyclopedia of Conservation: Volume 1-3
    View all citing articles on Scopus
    View full text