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  • Review Article
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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.

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Figure 1: Co-evolution and biological control.

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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.

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Correspondence to George K. Roderick.

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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.

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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

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