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Genomics and the future of conservation genetics

Key Points

  • We will soon have complete genome sequences from thousands of species. This coming explosion of information will transform our understanding of the amount, distribution and functional significance of genetic variation in natural populations.

  • We identify those problems in conservation biology in which genomics will be most valuable in providing new insights and understanding. We also provide guidelines as to which new genomics approaches will be most appropriate for the different problems in conservation that can benefit from genetic analysis.

  • The most straightforward contribution of genomics to conservation will be to enormously increase the precision and accuracy of estimation of crucial parameters that require neutral loci (for example, effective population size and migration rate).

  • Genomic approaches can address important questions about the molecular basis and genetic architecture of inbreeding depression. Recent work indicates that the intensity of inbreeding depression can differ greatly depending on which specific individuals are founders. This suggests that the genetic load is unevenly spread among founder genomes and supports the notion that inbreeding depression sometimes results from major effects at a few loci.

  • Anthropogenic challenges affect a wide range of species and habitats. Genomic approaches will allow the identification of adaptive genetic variation related to key traits for the response to climate change, such as phenology or drought tolerance, so that management may focus on maintaining adaptive genetic potential. The use of genomics to monitor genetic change caused by the harvesting of animals by humans could be extremely important because early detection of potentially harmful genetic change will maximize our ability to implement management to limit or reverse the effects before substantial or irreversible changes occur.

  • Genomics provides exciting opportunities to assess differential rates of introgression across different genomic regions following hybridization between native and introduced species. The differential introgression rates of genomic regions raise some difficult issues with regards to treating hybridized populations in conservation and bring into question the efficacy of using a few (that is, ten or so) neutral markers to detect hybridization.

  • Genomic tools will assist the management of ex situ populations and reintroductions by providing increased precision and accuracy of estimates of neutral population genetic parameters and by identifying specific loci of importance, which are essential for selecting select founder individuals.

  • There is increasing evidence that epigenetic processes can be important following hybridization. Therefore, an epigenetics perspective might be important for understanding the effects of hybridization and predicting outbreeding depression.

  • Improved basic scientific understanding through genomics will not necessarily lead to improved conservation. For example, understanding the relationship between genetic variation and fitness itself will not be sufficient to improve our estimates of population viability. Understanding the connections between individual fitness and population growth rates is perhaps the most important and difficult future challenge facing conservation genetics.

Abstract

We will soon have complete genome sequences from thousands of species, as well as from many individuals within species. This coming explosion of information will transform our understanding of the amount, distribution and functional significance of genetic variation in natural populations. Now is a crucial time to explore the potential implications of this information revolution for conservation genetics and to recognize limitations in applying genomic tools to conservation issues. We identify and discuss those problems for which genomics will be most valuable for curbing the accelerating worldwide loss of biodiversity. We also provide guidance on which genomics tools and approaches will be most appropriate to use for different aspects of conservation.

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Figure 1: Schematic diagram of interacting factors in conservation of natural populations.
Figure 2: Effects of proportion of individual admixture with introduced rainbow trout on the fitness of native westslope cutthroat trout.

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Acknowledgements

This article is based partially on work supported by the US National Science Foundation grants DEB 074218 to F.W.A. and G.L., and IOS 0843392 to P.A.H. G.L. also received support from the Walton Family Foundation and research grants PTDC/BIA-BDE/65625/2006 and PTDC/CVT/69438/2006 from the Portuguese Science Foundation. We thank D. E. Campton, R. Frankham, O. Gaggiotti, P. Hedrick, L. S. Mills, B. A. Payseur, K. M. Ramstad, M. K. Schwartz, P. Sunnucks and D. A. Tallmon for useful comments, and W. H. Lowe for endless EndNote tutoring to F.W.A.

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Supplementary Figure S1

The ability to detect local adaptation depends on gametic disequilibrium between the genotyped markers and loci under selection. (PDF 295 kb)

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Glossary

Neutral locus

A locus that has no effect on adaptation because all genotypes have the same fitness.

Inbreeding coefficient

The probability that two alleles in an individual are both descended from a single allele in an ancestor (that is, that they are 'identical-by-descent').

Contig

An abbreviation for contiguous sequence; used to indicate a contiguous piece of DNA that is assembled from shorter overlapping sequence reads.

Metagenomics

The study of the collective genomic material contained in an environmental sample of microorganisms, facilitated by high-throughput sequencing technology that allows the direct sequencing of heterogeneous samples.

Endosymbiont

An organism that lives within the cells of a host organism.

Inbreeding depression

The loss of vigour and fitness that is observed when genome-wide homozygosity is increased by inbreeding.

Adaptation

Heritable changes in genotype or phenotype that result in increased fitness.

Hybridization

Interbreeding of individuals from genetically distinct populations, regardless of the taxonomic status of the populations.

Outbreeding depression

Reduced fitness of F1 or F2 individuals after a cross between two species or populations. It can result from genetic incompatibility or reduced adaptation to local environmental conditions.

Effective population size

The size of the ideal population that would experience the same amount of genetic drift as the observed population.

Outlier locus

A genome location (or marker or base pair) that shows behaviour or a pattern of variation that is extremely divergent from the rest of the genome (locus-specific effects), as revealed by simulations or statistical tests.

F ST

A measure of population subdivision that indicates the proportion of genetic diversity found between populations relative to the amount within populations.

Population bottleneck

A marked reduction in population size followed by the survival and expansion of a small random sample of the original population. It often results in the loss of genetic variation and more frequent matings among closely related individuals.

Hierarchical Bayesian model

A Bayesian model in which the prior depends on another parameter that is not in the likelihood function and that can vary and have another prior.

Haplotype

A set of genetic markers that are present on a single chromosome and that show complete or nearly complete gametic disequilibrium. They are inherited through generations without being changed by crossing-over or other recombination mechanisms.

Admixture

The production of new genetic combinations in hybrid populations through recombination.

Coalescent approach

A means of investigating the shared genealogical history of genes. A genealogy is constructed backwards in time starting with the present-day sample. Lineages coalesce when they have a common ancestor.

Selection coefficient

A term that describes the difference in average fitness between genotypes when fitness is measured relative to the average fitness of one of the genotypes (known as the reference genotype).

Metapopulation

A collection of populations of a species found in differing geographic locations and with restricted gene flow (exchange of genes) between the populations.

Proportion of admixture

The proportion of alleles in a hybrid swarm or individual that comes from each of the hybridizing taxa.

Epistasis

The dependency of the effects of alleles at one locus on the genotypes at other loci in the genome.

Purging

The selective reduction in frequency of deleterious recessive alleles in small populations because the increase in homozygosity increases the ability of selection to act on recessive alleles.

Identical-by-descent

An allele shared by two related individuals is said to be identical-by-descent if the allele is inherited from the same common ancestor.

Gametic disequilibrium

A measure of whether alleles at two loci in a population occur in a non-random fashion.

Type I and type II errors

Statistical errors in which a true null hypothesis is rejected (type I) or a false null hypothesis is not rejected (type II).

Expressed sequence tag

A short DNA fragment (several hundred base pairs) produced by reverse transcription of mRNA into DNA.

Phenology

The timing of periodic biological phenomena that are usually correlated with climatic conditions.

Landscape genomics

The study of many markers, including markers in genes under selection, in spatially referenced samples collected across a landscape and often across selection gradients. It uses comparisons of adaptive and neutral variation to quantify the effects of landscape features and environmental variables on gene flow and spatial genetic variation.

Evolutionarily significant unit

A classification of populations that have substantial reproductive isolation which has led to adaptive differences so that the population represents a significant evolutionary component of the species.

Distinct population segment

A classification under the Endangered Species Act of the United States that allows for legal protection of populations that are distinct, relatively reproductively isolated and represent a significant evolutionary lineage to the species.

Management unit

A local population that is managed as a unit owing to its demographic independence.

Introgression

Gene flow between populations or species whose individuals hybridize.

Heterosis

When hybrid individuals have greater fitness than either of the parental types.

Marker-assisted selection

The use of molecular genetic markers to increase the response to selection in a population by the favouring of reproduction by individuals with a certain allele or genotype. The marker is closely linked to a quantitative trait locus.

Genetic rescue

The recovery in the average fitness of individuals through increased gene flow into small populations, typically following a fitness reduction due to inbreeding depression.

Chondrodystrophy

A genetically based skeletal disorder that affects the development of cartilage.

Community genomics

The study of the effect of individual alleles or genotypes on the species composition, diversity or functioning of a community or ecosystem.

Epigenetics

Changes in or gene expression caused by mechanisms other than changes in the underlying DNA sequence, such as DNA methylation and histone modifications.

Vital rates

Demographic values that affect population growth (for example, age-specific survival, fecundity and age at first reproduction).

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Allendorf, F., Hohenlohe, P. & Luikart, G. Genomics and the future of conservation genetics. Nat Rev Genet 11, 697–709 (2010). https://doi.org/10.1038/nrg2844

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