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Review
. 2014 Oct 17;346(6207):1245993.
doi: 10.1126/science.1245993. Epub 2014 Sep 11.

Applying evolutionary biology to address global challenges

Affiliations
Review

Applying evolutionary biology to address global challenges

Scott P Carroll et al. Science. .

Abstract

Two categories of evolutionary challenges result from escalating human impacts on the planet. The first arises from cancers, pathogens, and pests that evolve too quickly and the second, from the inability of many valued species to adapt quickly enough. Applied evolutionary biology provides a suite of strategies to address these global challenges that threaten human health, food security, and biodiversity. This Review highlights both progress and gaps in genetic, developmental, and environmental manipulations across the life sciences that either target the rate and direction of evolution or reduce the mismatch between organisms and human-altered environments. Increased development and application of these underused tools will be vital in meeting current and future targets for sustainable development.

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Figures

Fig. 1
Fig. 1
The two central paradigms of applied evolution are managing contemporary evolution and phenotype-environment mismatch. Managing contemporary evolution is critical for rapidly reproducing organisms with large population sizes, such as the methicillin-resistant Staphylococcus aureus (MRSA) pictured in the upper left. Altering phenotype-environment mismatch is most relevant for organisms with relatively long generation times and low population sizes, such the large mammals shown the lower right. Labels in ovals refer to example organisms, viruses or cell types in specified management sectors. ‘All’ indicates relevance to all management sectors (food, health and environment).
Fig. 2
Fig. 2
Phenotype-environment mismatch. (A) Mismatch between phenotypes and an environment occurs when a population's phenotypic trait distribution differs from the optimum; greater mismatch increases selection for adaptation, but also implies greater costs through reduced survival and reproduction. (B) Genotypic manipulations reduce mismatch by managing existing genetic variation or introducing new genes. For example, conventional corn is damaged by insect pests (left) that are killed by bacterial proteins produced by genetically engineered Bt corn (right). Alternatively, evolutionary mismatch can also be managed by (C) Developmental manipulations of phenotypes, such as vaccination to enhance immunity against pathogens, or (D) Environmental manipulations, such as habitat restoration. These examples demonstrate methods to reduce mismatch, but these same tactics can be reversed to impose greater mismatch where beneficial to human interests (e.g., pest eradication).
Fig. 3
Fig. 3
Two management intervention categories of applied evolutionary biology: 1. Controlling adversaries and 2. Protecting valued populations. Together they are enabled by four strategies (boldface). A core set of eight evolutionary principles guides the execution of these strategies and underlies tactics (left hand columns) used to meet management objectives in the food and fiber production, health and environmental sectors (right hand columns). Colored squares show different treatments; curves show frequency distributions of phenotypes; double helices are genomes; green arrows show change through space or time; green wedges show point interventions using selection or GE. Semicolons separate multiple management examples. Hypothetical applications are given in two cases that lack empirical examples. Expanded treatments for each cell and references are provided in Supplementary Table S2.
Fig. 4
Fig. 4
Emerging pathogens such as zoonoses (black arrows) and resistant bacteria (gray arrows) illustrate interdependencies generated by gene flow among the economic sectors of food, health and the environment. In zoonoses, vertebrates such as birds act as reservoirs for pathogens that can infect humans. Through direct transmission or via domesticated animals, zoonoses are passed to humans and cause regular local and rare global epidemics (such as the flu outbreaks of H5N1-2004 and H1N1-2009). ‘Reverse zoonoses’ are transmitted from infected humans to wildlife (179). Antimicrobial resistance in bacterial stains associated with livestock evolves in response to widespread use of antibiotics in agriculture and to a lesser degree due to treatment in humans. Via food items, industry workers and waste disposal, resistant strains enter other human contexts. In a public health context resistant strains constitute a growing extra risk during treatment of illnesses, e.g., in hospitals. Antibiotics in human effluent cause widespread resistance selection in natural and semi-natural environments, which together with resistance reservoirs in natural environments further increase the risks of resistant pathogens in humans. In the figure, the dashed line indicates a variety of poorly known interactions among wild species.

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