Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Genes in new environments: genetics and evolution in biological control

Key Points

  • New genetic technologies have positioned the field of biological control as a test bed for theories in evolutionary biology and for understanding practical aspects of the release of genetically manipulated material.

  • Purposeful introductions of pathogens, parasites, predators and herbivores, when considered as replicated semi-natural field experiments, show the unpredictable nature of biological colonization.

  • Genetics is now used in biological control in many important ways, including: the development of genetic markers to examine population origins and spread; the isolation of genes that are involved in development, reproduction and behaviour, with much progress from new genomic information; and the development of gene-transfer technology.

  • Evolutionary change associated with organisms that are introduced for biological control has been commonly observed for biological control involving microparasites, such as viruses and bacteria, but not for macroparasites, such as predators and insect parasitoids.

  • Introductions of genotypes in classical biological control can help inform researchers and policy makers as to the risks associated with releasing genetically modified organisms into the environment. Particularly difficult to address in this regard is the potential for evolutionary change.

Abstract

The availability of new genetic technologies has positioned the field of biological control as a test bed for theories in evolutionary biology and for understanding practical aspects of the release of genetically manipulated material. Purposeful introductions of pathogens, parasites, predators and herbivores, when considered as replicated semi-natural field experiments, show the unpredictable nature of biological colonization. The characteristics of organisms and their environments that determine this variation in the establishment and success of biological control can now be explored using genetic tools. Lessons from studies of classical biological control can help inform researchers and policy makers about the risks that are associated with the release of genetically modified organisms, particularly with respect to long-term evolutionary changes.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Co-evolution and biological control.

References

  1. Eilenberg, J., Hajek, A. & Lomer, C. Suggestions for unifying the terminology in biological control. BioControl 46, 387–400 (2001). A guide to the different types of biological control procedures and their uses.

    Google Scholar 

  2. Garcia, R., Caltagirone, L. E. & Gutierrez, A. P. Comments on a redefinition of biological control. Roundtable. BioScience 38, 692–694 (1988).

    Google Scholar 

  3. Kareiva, P. Contributions of ecology to biological control. Ecology 77, 1963–1964 (1996).

    Google Scholar 

  4. Simberloff, D. & Stiling, P. How risky is biological control? Ecology 77, 1965–1974 (1996). A rigorous assessment of the risks that are associated with biological control, including non-target effects.

    Google Scholar 

  5. Hufbauer, R. A. Evidence for nonadaptive evolution in parasitoid virulence following a biological control introduction. Ecol. Appl. 12, 66–78 (2002). A review of the ecological and evolutionary changes that are associated with biological control.

    Google Scholar 

  6. Hall, R. W. & Ehler, L. E. Rate of establishment of natural enemies in classical biological control. Bull. Entomol. Soc. Am. 25, 280–282 (1979).

    Google Scholar 

  7. Van Lenteren, J. C. The potential of entomophagous parasites for pest control. Agri. Ecosyst. Environ. 10, 143–158 (1983).

    Google Scholar 

  8. Crawley, M. J. The successes and failures of weed biocontrol using insects. Biocontrol News Info. 10, 213–223 (1989).

    Google Scholar 

  9. Lawton, J. H. in Alternative to the Chemical Control of Weeds: Proceedings of an International Conference (eds Bassett, C., Whitehouse, L. J. & Zabkiewicz, J. A.) (Ministry of Forestry, Rotorua, New Zealand, 1990). A food-web approach to assess the trophic relationships that are associated with biological control introductions in Hawaii.

    Google Scholar 

  10. Henneman, M. L. & Memmott, J. Infiltration of a Hawaiian community by introduced biological control agents. Science 293, 1314–1316 (2001).

    CAS  PubMed  Google Scholar 

  11. Louda, S. M., Pemberton, R. W., Johnson, M. T. & Follett, P. A. Nontarget effects — the Achilles' heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Annu. Rev. Entomol. 48, 365–396 (2003). An examination of non-target effects in 10 case studies of biological control.

    CAS  PubMed  Google Scholar 

  12. Boettner, G. H., Elkinton, J. S. & Boettner, C. J. Effects of a biological control introduction on three nontarget native species of saturniid moths. Conserv. Biol. 14, 1798–1806 (2000).

    Google Scholar 

  13. Howarth, F. G. Environmental impacts of classical biological control. Annu. Rev. Entomol. 36, 485–511 (1991). A highly publicized synthesis of the environmental effects that are associated with classical biological control.

    Google Scholar 

  14. Hoddle, M. S. Is the anti-GMO stance warrented in Australia and New Zealand? Myrmecia May 10–11 (2003).

  15. Unruh, T. R. & Woolley, J. B. in Handbook of Biological Control (eds Bellows, T. S. & Fisher, T. W.) 57–85 (Academic Press, San Diego, California, 1999).

    Google Scholar 

  16. Ehler, L. E., Sforza, R. & Mateille, T. (eds.) Genetics, Evolution, and Biological Control 288 (CABI, New York, in the press). An up-to-date review of genetics and evolutionary biology as applied to biological control.

  17. Ashburner, M., Hoy, M. A. & Peloquin, J. J. Prospects for the genetic transformation of arthropods. Insect Mol. Biol. 7, 201–213 (1998).

    CAS  PubMed  Google Scholar 

  18. Navajas, M., Lagnel, J., Gutierrez, J. & Boursot, P. Species wide homogeneity of nuclear ribosomal ITS2 sequences in the spider mite Tetranychus urticae contrasts with extensive mitochondrial COI polymorphism. Heredity 80, 742–752 (1998).

    CAS  PubMed  Google Scholar 

  19. Roderick, G. K. in Genetics, Evolution, and Biological Control (ed. Mateille, T.) (CABI, New York, in the press).

  20. Waage, J. in Critical Issues in Biological Control (eds Mackauer, M., Ehler, L. E. & Roland, J.) 135–157 (Intercept, Andover, United Kingdom, 1990).

    Google Scholar 

  21. Slatkin, M. Gene flow and the geographic structure of natural populations. Science 236, 787–792 (1987).

    CAS  PubMed  Google Scholar 

  22. Roderick, G. K. Geographic structure of insect populations: gene flow, phylogeography, and their uses. Annu. Rev. Entomol. 41, 263–290 (1996).

    Google Scholar 

  23. Holder, M. & Lewis, P. O. Phylogeny estimation: traditional and bayesian approaches. Nature Rev. Genetics 4, 275–284 (2003).

    CAS  Google Scholar 

  24. Rosenberg, N. A. & Nordborg, M. Genealogical trees, coalescent theory and the analysis of genetic polymorphisms. Nature Rev. Genetics 3, 380–390 (2002).

    CAS  Google Scholar 

  25. Lanciotti, R. S. et al. Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286, 2333–2337 (1999).

    CAS  PubMed  Google Scholar 

  26. Gaskin, J. F. & Schaal, B. A. Hybrid Tamarix widespread in U.S. invasion and undetected in native Asian range. Proc. Natl Acad. Sci. USA 99, 11256–11259 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Estoup, A., Wilson, I. J., Sullivan, C., Cornuet, J. M. & Moritz, C. Inferring population history from microsatellite and enzyme data in serially introduced cane toads, Bufo marinus. Genetics 159, 1671–1687 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Davies, N., Villablanca, F. X. & Roderick, G. K. Determining the sources of individuals in recently founded populations: multilocus genotyping in non-equilibrium genetics. Trends Ecol. Evol. 14, 17–21 (1999).

    CAS  PubMed  Google Scholar 

  29. Cornuet, J. M. & Luikart, G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Hufbauer, R. A., Bogdanowicz, S. M. & Harrison, R. G. The population genetics of a biological control introduction: mtDNA and microsatellite variation in native and introduced populations of Aphidius ervi, a parasitoid wasp. Mol. Ecol. (in the press).

  31. Cornuet, J. M., Piry, S., Luikart, G., Estoup, A. & Solignac, M. New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153, 1989–2000 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Rannala, B. & Mountain, J. L. Detecting immigration using multilocus genotypes. Proc. Natl Acad. Sci. USA 94, 9197–9201 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Navajas, M. et al. Field releases of the predatory mite Neoseiulus fallacis (Acari: Phytoseiidae) in Canada, monitored by pyrethroid resistance and allozyme markers. Biol. Control 20, 191–198 (2001).

    CAS  Google Scholar 

  35. Bohonak, A. J., Davies, N., Villablanca, F. X. & Roderick, G. K. Invasion genetics of New World medflies: testing alternative colonization scenarios. Biol. Invasions 3, 103–111 (2001).

    Google Scholar 

  36. Beerli, P. & Felsenstein, J. Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc. Natl. Acad. Sci. USA 98, 4563–4568 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Nielsen, R. & Wakeley, J. Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158, 885–896 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Navajas, M. et al. Genetic structure of the greenhouse population of the spider mite Tetranychus urticae: spatio-temporal analysis with microsatellite markers. Insect Mol. Biol. 11, 157–165 (2002).

    CAS  PubMed  Google Scholar 

  39. Storz, J. F. & Beaumont, M. A. Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56, 154–166 (2002).

    CAS  PubMed  Google Scholar 

  40. Roush, R. T. & Hopper, K. R. Use of single-family lines to preserve genetic-variation in laboratory colonies. Ann. Entomol. Soc. Am. 88, 713–717 (1995).

    Google Scholar 

  41. Hopper, K. R., Roush, R. T. & Powell, W. Management of genetics of biological control introductions. Annu. Rev. Entomol. 38, 27–51 (1993).

    Google Scholar 

  42. Perez-Maluf, R., Kaiser, L. & Wajnberg, E. Genetic variability of conditioned probing responses to a fruit odor in Leptopilina boulardi (Hymenoptera: Eucoilidae), a Drosophila parasitoid. Behav. Genet. 28, 67–73 (1998).

    CAS  PubMed  Google Scholar 

  43. Bidochka, M. J. et al. Fate of biological control introductions: monitoring an Australian fungal pathogen of grasshoppers in North America. Proc. Natl Acad. Sci. 93, 918–921 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Handler, A. M. & Beeman, R. W. United States Department of Agriculture Agricultural Research Service: advances in the molecular genetic analysis of insects and their application to pest management. Pest Manag. Sci. 59, 728–735 (2003). A summary of the ways in which molecular genetic approaches are used in pest management.

    CAS  PubMed  Google Scholar 

  45. Whitten, M. J. & Hoy, M. in Handbook of Biological Control (eds Bellows, T. S. & Fisher, T. W.) 271–296 (Academic Press, San Diego, California, 1999).

    Google Scholar 

  46. Ding, X. et al. Insect resistance of transgenic tobacco expressing an insect chitinase gene. Transgenic Res. 7, 77–84 (1998).

    CAS  PubMed  Google Scholar 

  47. Federici, B. A. in Handbook of Biological Control (eds Bellows, T. S. & Fisher, T. W.) 575–593 (Academic Press, San Diego, California, 1999).

    Google Scholar 

  48. Hilbeck, A. Implications of transgenic, insecticidal plants for insect and plant biodiversity. Perspect. Plant Ecol. Evol. Syst. 4, 43–61 (2001).

    Google Scholar 

  49. Possee, R. D., Barnett, A. L., Hawtin, R. E. & King, L. A. Engineered baculoviruses for pest control. Pestic. Sci. 51, 462–470 (1997).

    CAS  Google Scholar 

  50. Holloway, A. J., Van Laar, R. K., Tothill, R. W. & Bowtell, D. D. L. Options available — from start to finish — for obtaining data from DNA microarrays. Nature Genet. 32 (Suppl.), 481–489 (2002).

    CAS  PubMed  Google Scholar 

  51. Hui, D. et al. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata: V. Microarray analysis and further characterization of large-scale changes in herbivore-induced mRNAs. Plant Physiol. 131, 1877–1893 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Sinkins, S. P., Curtis, C. F. & O'Neill, S. L. in Influential Passengers: Inherited Microorganisms and Arthropod Reproduction (eds O'Neill, S. L., Hoffmann, A. A. & Werren, J. H.) 155–208 (Oxford Univ. Press, Oxford, 1997).

    Google Scholar 

  53. Stouthamer, R. in Genetics, Evolution, and Biological Control (eds. Ehler, L. E., Sforza, R. & Mateille, T.) 235–252 (CABI, New York, in the press).

  54. Holt, R. D. & Hochberg, M. E. When is biological control evolutionarily stable (or is it)? Ecology 78, 1673–1683 (1997).

    Google Scholar 

  55. Fenner, F. Biological control as exemplified by small pox eradication and myxomatosis. Proc. R. Soc. Lond. B 218, 259–285 (1983).

    CAS  PubMed  Google Scholar 

  56. Fenner, F. Adventures with poxviruses of vertebrates. FEMS Microbiol. Rev. 24, 123–133 (2000).

    CAS  PubMed  Google Scholar 

  57. Best, S. M., Collins, S. V. & Kerr, P. J. Coevolution of host and virus: cellular localization of virus in myxoma virus infection of resistant and susceptible European rabbits. Virology 277, 76–91 (2000).

    CAS  PubMed  Google Scholar 

  58. Zúñiga, M. C. A pox on thee! Manipulation of the host immune system by myxoma virus and implications for viral–host co-adaptation. Virus Res. 88, 17–33 (2002). An update outlining the present understanding of the genetic mechanisms that are associated with myxoma/rabbit co-evolution.

    PubMed  Google Scholar 

  59. Thompson, J. N. Evolutionary ecology and the conservation of biodiversity. Trends Ecol. Evol. 11, 300–303 (1996).

    CAS  PubMed  Google Scholar 

  60. van Lenteren, J. C. et al. Environmental risk assessment of exotic natural enemies used in inundative biological control. Biocontrol 48, 3–38 (2003).

    Google Scholar 

  61. Hajek, A. E., Humber, R. A. & Elkinton, J. S. Mysterious origins of Entomophaga maimaiga in North America. Am. Entomolog. 41, 31–42 (1995).

    Google Scholar 

  62. Amarger, N. Genetically modified bacteria in agriculture. Biochimie 84, 1061–1072 (2002).

    CAS  PubMed  Google Scholar 

  63. van Klinken, R. D. & Edwards, O. R. Is host-specificity of weed biological control agents likely to evolve rapidly following establishment? Ecol. Lett. 5, 590–596 (2002).

    Google Scholar 

  64. Willis, A. J., Memmott, J. & Forrester, R. I. Is there evidence for the post-invasion evolution of increased size among invasive plant species? Ecol. Lett. 3, 275–283 (2000).

    Google Scholar 

  65. Cromartie, W. J. Is adaptation after release necessary for successful classical biological control? Entomol. News 108, 252, 258, 304 (1997).

    Google Scholar 

  66. Tsutsui, N. D., Suarez, A. V., Holway, D. A. & Case, T. J. Reduced genetic variation and the success of an invasive species. Proc. Natl Acad. Sci. USA 97, 5948–5953 (2000). An elegant study of the effects of reduced genetic diversity, which led to changes in behaviour that were associated with the invasion biology of Argentine ants.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. De Jong, D. D., Morse, R. A. & Eickwort, G. C. Mite pests of honey bees. Annu. Rev. Entomol. 27, 229–252 (1982).

    Google Scholar 

  68. Anderson, D. L. & Trueman, J. W. H. Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp. App. Acarol. 24, 165–189 (2000).

    CAS  Google Scholar 

  69. Elzen, P. J., Eischen, F. A., Baxter, J. R., Elzen, G. W. & Wilson, W. T. Detection of resistance in US Varroa jacobsoni Oud. (Mesostigmata: Varroidae) to the acaricide fluvalinate. Apidologie 30, 13–17 (1999).

    CAS  Google Scholar 

  70. Nei, M., Maruyama, T. & Chakraborty, R. The bottleneck effect and genetic variability in populations. Evolution 29, 1–10 (1975).

    PubMed  Google Scholar 

  71. Luikart, G. & Cornuet, J. M. Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv. Biol. 12, 228–237 (1998).

    Google Scholar 

  72. Stouthamer, R. & Kazmer, D. J. Cytogenetics of microbe-associated parthenogenesis and its consequences for gene flow in Trichogramma wasps. Heredity 73, 317–327 (1994).

    Google Scholar 

  73. Dres, M. & Mallet, J. Host races in plant-feeding insects and their importance in sympatric speciation. Phil. Trans. R. Soc. Lond. B 357, 471–492 (2002).

    Google Scholar 

  74. Farrell, B. D. “Inordinate fondness” explained: why are there so many beetles? Science 281, 555–559 (1998).

    CAS  PubMed  Google Scholar 

  75. Berlocher, S. H. & Feder, J. L. Sympatric speciation in phytophagous insects: moving beyond controversy? Annu. Rev. Entomol. 29, 403–433 (2002).

    Google Scholar 

  76. Zimmerman, E. C. Possible evidence of rapid evolution in Hawaiian moths. Evolution 14, 137–138 (1960).

    Google Scholar 

  77. Gillespie, R. G. & Roderick, G. K. Arthropods on islands: colonization, speciation, and conservation. Annu. Rev. Entomol. 47, 595–632 (2002).

    CAS  PubMed  Google Scholar 

  78. Sorci, G., Moller, A. P. & Boulinier, T. Genetics of host–parasite interactions. Trends Ecol. Evol. 12, 196–200 (1997).

    CAS  PubMed  Google Scholar 

  79. Thompson, J. N. The Coevolutionary Process (Univ. of Chicago Press, Chicago, 1994).

    Google Scholar 

  80. Tuda, M. & Bonsall, M. B. Evolutionary and population dynamics of host–parasitoid interactions. Res. Popul. Ecol. 41, 81–91 (1999).

    Google Scholar 

  81. Morin, S. et al. Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc. Natl Acad. Sci. USA 100, 5004–5009 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Genissel, A. et al. Initial frequency of alleles conferring resistance to Bacillus thuringiensis poplar in a field population of Chrysomela tremulae. Proc. R. Soc. Lond. B 270, 791–797 (2003).

    Google Scholar 

  83. Hufbauer, R. A. Pea aphid–parasitoid interactions: have parasitoids adapted to differential resistance? Ecology 82, 717–725 (2001).

    Google Scholar 

  84. Hufbauer, R. A. & Via, S. Evolution of an aphid–parasitoid interaction: variation in resistance to parasitism among aphid populations specialized on different plants. Evolution 53, 1435–1445 (1999).

    PubMed  Google Scholar 

  85. Vaughn, T. T. & Antolin, M. F. Population genetics of an opportunistic parasitoid in an agricultural landscape. Heredity 80, 152–162 (1998).

    Google Scholar 

  86. Kraaijeveld, A. R. & Godfray, H. C. J. Geographic patterns in the evolution of resistance and virulence in Drosophila and its parasitoids. Am. Nat. 153, 61–74 (1999).

    Google Scholar 

  87. Lapchin, L. Host–parasitoid association and diffuse coevolution: when to be a generalist? Am. Nat. 160, 245–254 (2002).

    PubMed  Google Scholar 

  88. Baker, D. A. The significance of host specialization in the parasitoid wasp, 'Diaeretiella rapae' (M'Intosh). Thesis, Univ. of Western Australia (2002).

  89. O'Neill, S. L., Hoffmann, A. A. & Werren, J. H. (eds). Influential Passengers: Inherited Microorganisms and Arthropod Reproduction (Oxford Univ. Press, Oxford, 1997).

    Google Scholar 

  90. Hokkanen, H. M. T. & Pimentel, D. New associations in biological control: theory and practice. Can. Entomol. 121, 829–840 (1989).

    Google Scholar 

  91. Neuhauser, C. et al. Community genetics: expanding the synthesis of ecology and genetics. Ecology 84, 545–558 (2003).

    Google Scholar 

  92. Ricklefs, R. E. Genetics, evolution, and ecological communities. Ecology 84, 588–591 (2003).

    Google Scholar 

  93. Palumbi, S. R. Evolution — humans as the world's greatest evolutionary force. Science 293, 1786–1790 (2001). A review that documents the role of evolution in human civilization.

    CAS  PubMed  Google Scholar 

  94. Wilcove, D. S., Rothstein, D., Dubow, J., Phillips, A. & Losos, E. Quantifying threats to imperiled species in the United States. BioScience 48, 607–615 (1998).

    Google Scholar 

  95. Pimentel, D., Lack, L., Suniga, R. & Morrison, D. Environmental and economic costs of nonindigenous species in the United States. Bioscience 50, 53–65 (2000).

    Google Scholar 

  96. Hoy, M. A. Transgenic arthropods for pest management programs: risks and realities. Exp. App. Acarol. 24, 463–495 (2000).

    CAS  Google Scholar 

  97. Soboleva, T. K., Shorten, P. R., Pleasants, A. B. & Rae, A. L. Qualitative theory of the spread of a new gene into a resident population. Ecol. Modell. 163, 33–44 (2003).

    Google Scholar 

  98. Richards, A., Matthews, M. & Christian, P. Ecological considerations for the environmental impact evaluation of recombinant baculovirus insecticides. Annu. Rev. Entomol. 43, 493–517 (1998).

    CAS  PubMed  Google Scholar 

  99. Jung, C. & Croft, B. A. Aerial dispersal of phytoseiid mites (Acari: Phytoseiidae): estimating falling speed and dispersal distance of adult females. Oikos 94, 182–190 (2001).

    Google Scholar 

  100. Pearson, D. E. & Callaway, R. M. Indirect effects of host-specific biological control agents. Trends Ecol. Evol. 18, 456–461 (2003).

    Google Scholar 

  101. Dushoff, J. & Dwyer, G. Evaluating the risks of engineered viruses: modeling pathogen competition. Ecol. Appl. 11, 1602–1609 (2001).

    Google Scholar 

  102. Li, J. & Hoy, M. A. Adaptability and efficacy of transgenic and wild-type Metaseiulus occidentalis (Acari: Phytoseiidae) compared as part of a risk assessment. Exp. App. Acarol. 20, 563–573 (1996).

    Google Scholar 

  103. Capalbo, D. M. F. et al. Brazil and the development of international scientific biosafety testing guidelines for transgenic crops. J. Invertebr. Pathol. 83, 104–106 (2003).

    PubMed  Google Scholar 

  104. Hoddle, M. in Encyclopedia of Insects (eds Resh, V. H. & Cardé, R.) (Academic Press, San Diego, California, 2003).

    Google Scholar 

  105. Ravesberg, W. J. in Advances in Insect Rearing for Research and Pest Management (eds Anderson, T. E. & Leppla, N. C.) 465–487 (Westview, Boulder, Colorado, 1992).

    Google Scholar 

  106. Whitlock, M. C. & McCauley, D. E. Indirect measures of gene flow and migration: FST not equal to 1/(4Nm+1). Heredity 82, 117–125 (1999).

    PubMed  Google Scholar 

  107. Dwyer, G., Levin, S. A. & Buttel, L. A simulation-model of the population-dynamics and evolution of myxomatosis. Ecol. Monogr. 60, 423–447 (1990).

    Google Scholar 

Download references

Acknowledgements

We thank R. Gillespie, R. Hufbauer, O. Edwards, B. Croft, M. Hoddle, L. Smith and three anonymous reviewers for valuable insights and suggestions. This work is supported by grants from the National Science Foundation, the United States Department of Agriculture, the California Department of Food and Agriculture, the University of California and the French Institut National de la Recherche Agronomique.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to George K. Roderick.

Related links

Related links

DATABASES

SwissProt

M11L

M-T1

M-T4

M-T5

M-T7

MGF

SERP1

SERP2

SERP3

TxPI

FURTHER INFORMATION

Berkeley Natural History Museums

Biological control: a guide to natural enemies in North America

CABI-Bioscience

French Institut National de la Recherche Agronomique in Montpellier

International Organisation for Biological Control (IOBC)

University of California Berkeley's Gump South Pacific Research Station in Moorea, French Polynesia

Glossary

HOSTS

Prey for organisms that are introduced for biological control.

ADAPTATION

Evolution as a result of selection.

SOURCE POPULATION

Ancestral population; the pest might have descended from this population recently or many generations in the past.

GENETIC DRIFT

The random change in allele frequencies.

MIGRATION–DRIFT GENETIC EQUILIBRIUM

The balance between the loss of alleles through genetic drift and the gain of alleles through migration.

PHYLOGEOGRAPHIC APPROACH

The use of estimated gene genealogies to study the geographical history and structure of populations or species.

MULTI-LOCUS GENETIC APPROACHES

Genetic methods that make use of information from many loci; such approaches use nuclear loci because mitochondrial genes are typically inherited as one locus.

ASSIGNMENT TESTS

Statistical procedures in which individuals can be assigned to probable source populations.

CO-DOMINANT MARKERS

Genetic markers that allow the determination of both alleles at a diploid locus (for example, microsatellites, allozymes and single nucleotide polymorphisms); these differ from dominant markers in which the determination of heterozygotes is not always possible (or example, RAPDs and AFLPs).

MICROSATELLITES

Co-dominant nuclear DNA markers that consist of sets of repeated short nucleotide sequences.

ALLOZYMES

Co-dominant nuclear DNA markers that consist of enzymes that differ in their mobility on a charged gel.

MARKOV-CHAIN MONTE CARLO

A computational technique for the efficient numerical calculation of likelihoods.

BAYESIAN APPROACH

A statistical perspective that focuses on the probability distribution of parameters before and after observing the data.

EFFECTIVE POPULATION SIZE

The population size that responds identically to that modelled genetically; that is, the size of the population that matters for genetic concerns.

DIAPAUSE

A resting stage for insects, typically during winter or dry periods.

MAXIMUM LIKELIHOOD

A procedure in phylogenetic reconstruction in which a tree is chosen that maximizes the probability of the data given the model and the tree hypothesis.

PARSIMONY

A procedure in phylogenetic reconstruction in which a tree is chosen because it requires the fewest possible mutations to explain the data.

NESTED CLADE ANALYSIS

A statistical parsimony procedure that constructs sets of nested clades. With knowledge of geographic distribution, the clades can be examined for evidence of processes that are associated with geographic structure, such as isolation by distance, allopatric fragmentation and long-distance colonization.

AUTOCIDAL CONTROL

The introduction of an organism that causes its own population to decline without interaction with other species.

PARASITOID

An insect that kills only one host individual in its lifetime and has a free-living adult stage; this differs from a predator, which kills many host individuals in its lifetime, and from a parasite, which typically does not kill the host and can persist for several generations in one host.

SERPINS

Irreversible inhibitors of serine proteases that regulate a diverse array of physiological processes, including apoptosis, inflammation, angiogenesis, complement activation, fibrinolysis and coagulation.

EPIZOOTICS

Outbreaks of organisms that feed on other organisms.

VIRULENCE GRADES

Categories of virus virulence that are based on host (rabbit) survival (measured in days) and case mortality (expressed as a percentage).

FUNDAMENTAL HOST RANGE

The actual host range of a species before any evolutionary change.

COMMON GARDEN EXPERIMENTS

Ecological transplant studies in which organisms are reared under identical conditons.

APICULTURE

The practice of bee domestication.

HAPLOTYPE

The allelic configuration of multiple genetic markers that is present on a single chromosome of a given individual.

MICROBE-ASSOCIATED PARTHENOGENESIS

The occurrence of reproduction without males, which is caused by the presence of a microbe.

SYMPATRIC SPECIATION

Genetic divergence that leads to species formation in the same habitat.

KEYSTONE SPECIES

Species in ecological communities that have disproportional direct and indirect effects on other species, which are usually regulated through top-down processes, such as predation.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Roderick, G., Navajas, M. Genes in new environments: genetics and evolution in biological control. Nat Rev Genet 4, 889–899 (2003). https://doi.org/10.1038/nrg1201

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrg1201

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing