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Genomics and Conservation Genetics Review TRENDS in Ecology and Evolution Vol.21 No.11 Genomics and conservation genetics Michael H. Kohn1, William J. Murphy2, Elaine A. Ostrander3 and Robert K. Wayne4 1 Department of Ecology & Evolutionary Biology, Rice University, MS 170, 6100 Main Street, Houston, TX 77005, USA 2 Department of Veterinary Integrative Biosciences, Texas A&M University, MS 4458, College Station, TX 77843-4458, USA 3 National Human Genome Research Institute, National Institute of Health, Comparative Cancer Section, 50 South Drive, MSC 8000, Bethesda, MD 20892-8000, USA 4 Department of Ecology & Evolutionary Biology, University of California, Los Angeles, CA 90095-1606, USA In large part, the relevance of genetics to conservation have often aided the management of rare and endangered rests on the premise that neutral marker variation in species. Consequently, given limited resources, there might populations reflects levels of detrimental and adaptive be little incentive to move from conservation genetics to genetic variation. Despite its prominence, this tenet has ‘conservation genomics’, particularly when traditional con- been difficult to evaluate, until now. As we discuss here, servation genetic issues in vertebrate animals and vascular genome sequence information and new technological plants are considered (Box 1). and bioinformatics platforms now enable comprehen- So which of the more traditional conservation genetics sive surveys of neutral variation and more direct infer- applications, if any, are in need of genomic tools and ences of detrimental and adaptive variation in species information? Clearly, many applications of molecular mar- with sequenced genomes and in ‘genome-enabled’ kers in conservation could be transformed by genomic endangered taxa. Moreover, conservation schemes approaches [12–15], and approaches such as metage- could begin to consider specific pathological genetic nomics could give rise to entirely novel conservation variants. A new conservation genetic agenda would research questions. However, one of the most immediate utilize data from enhanced surveys of genomic variation questions, in our view, is how genomic resources might be in endangered species to better manage functional used to test the implicit assumption of conservation genet- genetic variation. ics, that the observed levels of neutral genetic variation can be used to predict the levels of detrimental variation Introduction accrued and adaptive variation lost by endangered species Given the current and future capacity of genome centers, owing to population size decline [4,16]. Existing data sug- hundreds of species of animal, plant, fungi, bacteria and gest that the correlation of neutral with detrimental and viruses will eventually have their genome sequenced ([1]; c.f. adaptive variation is low, in large part, because this rela- TM GOLD , the Genomes OnLine Database v 2.0 at http:// tionship is contingent upon genomic sampling and popula- www.genomesonline.org/). Additionally, thousands of pre- tion-specific demographic history (Table 2). viously unknown microbial species will emerge from so- This concern suggests three research areas where geno- called ‘metagenomic’ sequencing projects [1]. As of 2006, mics could enhance traditional small-scale surveys of neu- more than 50 plant and 215 animal genome projects are tral marker variation. First, expanded neutral marker ongoing, covering at varying resolution >35 vascular plant surveys enable the more detailed reconstruction of the species, 135 invertebrates including sponges, echinoderms, demographic histories of species [17], thereby facilitating cnidarians and insects, and 75 vertebrate species. Close to more precise predictions regarding the increase and loss, 1000 red-listed mammal species alone are within the same respectively, of detrimental and adaptive genetic variation order or group to that containing a genome-sequenced spe- (Table 2). Second, expanded DNA sequence polymorphism cies. Most genera represented by genome-sequenced species surveys combined with bioinformatical analyses (Box 2) also contain endangered or vulnerable species, subspecies, [18] could be used to quantify levels of detrimental genetic or populations (Table 1). Thus, depending on phylogenetic variation that might diminish fitness and threaten popula- distance and the questions being addressed, the sequencing tion persistence and of adaptive variation, which enables a of one species, such as the dog Canis familiaris will result in genetic response to environmental change [11]. Under- numerous ‘genome-enabled’ taxa (e.g. Figure 1) [2,3]. standing the relationship of neutral variation with detri- In addition to demographic and environmental uncer- mental and adaptive variation is essential for the effective tainties, genetic uncertainties (see Glossary) such as foun- use of genetic data in conservation [4]. Finally, information der effects, genetic drift and inbreeding, threaten about neutral and adaptive variation could be used to endangered species [4–11]. Conservation genetics addresses preserve population distinctiveness within a framework these issues and numerous others with limited surveys of of genetic and ecological exchangeability (sensu Temple- neutral marker variation (Box 1). The results of these ton) [19–21]. studies have a well-established role in conservation and Genetic variation considered in conservation Each of the three types of genetic variation in nature Corresponding author: Kohn, M.H. ([email protected]). (neutral, detrimental and adaptive) has specific uses and Available online 5 September 2006. conceptual implications for conservation. www.sciencedirect.com 0169-5347/$ – see front matter ß 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2006.08.001 630 Review TRENDS in Ecology and Evolution Vol.21 No.11 Glossary and adaptive variation and underestimates population differentiation in quantitative traits [4,20,23]. Hence, Adaptive genetic variation: genetic variation that affects fitness. A population might be fixed for an adaptive variant or polymorphic because the variant is limited neutral marker surveys might result in misconcep- newly arisen or is maintained by balancing selection. tions about levels of detrimental and adaptive variation in Comparative genomics: evolutionary relationship between the genes and endangered species. proteins of different species, and applications that draw upon these relation- ships to infer structure and function. Demographic uncertainty: uncertainty of population persistence resulting from Detrimental variation the effects of random events on the survival and reproduction of individuals, such as extremely skewed sex ratio or threshold effects (e.g. Allee effect). Among the genetic variants that can adversely affect fitness Detrimental genetic variation: variation that has a negative affect on fitness, are those that alter the protein sequence of genes (Box 2) often brought into the population by mutation or gene flow and sometimes [24,25]. The dynamics of such mutations varies: selection is increased by drift; can be strongly detrimental (recessive) mutations that can cause inbreeding depression in the homozygous state, or weakly detrimental most efficient in large populations and, consequently, even mutations whose aggregate effect reduces population fitness as genetic load. detrimental mutations of small effect are eliminated or kept Ecological exchangeability: factors that define the fundamental niche and the at low frequencies such that the genetic load is low [26–29]. limits of spread of new genetic variants through genetic drift and natural selection. Exchangeability is rejected when there is evidence for population In small populations, weakly selected mutations, in the differentiation owing to genetic drift or natural selection. range of À1/2N < s < 1/2N (where N is the genetically effec- Environmental uncertainty: unpredictable events (e.g. variation in food supply tive population size and s the selection coefficient) behave as or exposure to parasites or competitors) that adversely affect the long-term survival of the population as a whole. although they are neutral and therefore can increase in Functional variation: characterization of genes and proteins with respect to frequency owing to drift. This increase in small populations function. Examples of functional properties include the structure of the lowers the mean fitness and, even in a constant environ- resulting protein or the levels of the expression of the gene. Functional properties can be predicted (e.g. by reconstructing the 3D structure of proteins ment, can lead to a ‘mutation meltdown’ [6,7]. based on the gene sequence, or by predicting gene expression based on Inbreeding depression caused by increased probability regulatory sequence motifs on the promoter). Finally, other approaches merely of homozygosity for detrimental alleles is a more immedi- infer function (e.g. based on the conservation of gene sequences between species, the type and location of a SNP, or the signature of natural selection on ate concern [4,30]. Under some demographic scenarios, a gene sequence). strongly detrimental mutations are likely to be purged Gene annotation: database entries that describe what the gene or genomic region is, provide its boundaries and functional elements (e.g. transcription during population-size declines (Table 2) [4,16]. For exam- factor binding sites), background information about the expression of the gene ple, populations that have long persisted at a small size and disease-causing
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