Genomics and The Future of Conservation Genetics

REVIEWS
Genomics and the future of

conservation genetics
Fred W. Allendorf*‡, Paul A. Hohenlohe§|| and Gordon Luikart ¶#
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.
Neutral locus
The ability to examine thousands of genetic markers The application of metagenomics to conservation is still
A locus that has no effect with relative ease will make it possible to answer many in its early stages, but shows promise. First, functional
on adaptation because important questions in conservation that have been metagenomics of microbial communities provides a
all genotypes have the intractable until now. Simply increasing the number of novel perspective on ecosystem processes, such as
same fitness.
neutral loci that we can screen will increase the power nutrient and energy flux. Although some studies have
and accuracy of estimating a variety of important compared functions across a broad scale of biomes 9,
parameters in conservation (for example, kin rela- similar comparative approaches may identify aspects
*Division of Biological
Sciences, University of tionships and inbreeding coefficients (F)). However, of ecosystem function across sites within a habitat.
Montana, Missoula, the most exciting contributions of genomics to con- The second potential application of metagenomics to
Montana 59812, USA. servation are those that will allow new questions to conservation is in assessment of physiological con-
‡
School of Biological Sciences, be addressed in a wide variety of species (BOX 1). For dition of individual organisms. For instance, Vega
Victoria University of
Wellington, Wellington,
instance, it should be possible to estimate the effect Thurber et al. 10 have found numerous shifts in the
New Zealand. size and distribution of loci affecting fitness across the endosymbiont community of corals in response to
§
Center for Ecology and genome or to ask whether the loci are coincident across multiple stressors, such as reduced pH, increased
Evolutionary Biology, populations1,2 (FIG. 1). nutrients and increased temperature. Third, a metage-
University of Oregon, Eugene,
Genomic approaches are currently being used pri- nomic analysis of human faecal samples catalogued
Oregon 97403, USA.
||
Department of Zoology, marily with a few species for which genomic informa- 3.3 million microbial genomes and found substantial
Oregon State University, tion and tools are available3; for example, wolves, bison differences in the microbial metagenome between
Corvallis, Oregon 97331, USA. and bighorn sheep have been studied using genomic healthy individuals and those with inflammatory
¶
Flathead Lake Biological tools developed in related domestic species4. However, bowel disease 11. It may be possible in the future to
Station, Division of Biological
Sciences, University of
the range of species is expanding as new approaches are apply metagenomic techniques to faecal samples from
Montana, Polson, Montana developed that are not dependent on genomic infor- wildlife species to assess physiological states, such as
59860, USA. mation from closely related species 5,6. For example, starvation stress.
#
Centro de Investigação em van Bers et al.7 obtained over 16 million short sequence Genomics already has provided some interesting
Biodiversidade e Recursos
reads and conducted de novo assembly of 550,000 contigs surprises, such as the discovery of adaptive loci that
Genéticos, Universidade do
Porto, 4485‑661 Vairão, covering 2.5% of the genome to discover 20,000 novel show extremely high genetic divergence between popu-
Portugal. SNPs in the great tit (Parus major). These markers will lations of marine fish for which there is virtually no
e‑mails: be used for quantitative trait locus mapping and whole allele frequency divergence at neutral loci12 (BOX 2). In
[email protected]; genome association studies. addition, a multi-faceted genomic approach has pro-
hohenlop@science.
oregonstate.edu;
In addition, multiple taxa can be combined in a sin- vided important insights into the treatment of a facial
[email protected] gle sequencing analysis using genomic techniques that tumour disease that threatens the persistence of the
doi:10.1038/nrg2844 can assay large amounts of variable DNA sequence8. Tasmanian devil (Sarcophilus laniarius)13.
NATURE REVIEWS | GENETICS VOLUME 11 | O CTOBER 2010 | 697
© 2010 Macmillan Publishers Limited. All rights reserved

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Box 1 | What is ‘conservation genomics’? proceed through issues that will become more feasible
in the future. We consider how genomic approaches will
Conservation genomics can be broadly defined as the use of new genomic techniques allow us to understand the genetic basis of inbreeding
to solve problems in conservation biology. Frankham72 recently reviewed the current depression and adaptation. We then apply these insights
status of conservation genetics and proposed 13 priorities for development in the field.
to important outstanding problems in conservation,
Many of these priorities have been intractable through traditional genetic techniques.
including understanding the effects of hybridization and
Although genomic techniques are not appropriate or necessary in all cases, we believe
that genomics will have an important role in addressing several research challenges predicting outbreeding depression, as well as predicting
over the next few years. evolutionary responses to climate change.
Genomic techniques will be more immediately applicable to some questions than to
others (TABLE 1). For example, in estimating neutral population parameters, such as ‘Neutral’ markers
effective population size, genomics simply provides a larger number of markers to an The most straightforward contribution of genomics to
analytical and conceptual framework that is already widely used in conservation conservation will be to enormously increase the pre-
genetics. Genomic identification of functionally important genes is now common in cision and accuracy of estimation of parameters that
other fields; conservation genomics can incorporate these approaches to study the require neutral loci (for example, effective population size
genetic basis of local adaptation or inbreeding depression. By contrast, predicting a
(Ne) and migration rate (m)) by genotyping hundreds
population’s viability or capacity to adapt to climate change based on genomic
to thousands of neutral loci in numerous individuals.
information will require not only the identification of relevant loci, but also a
quantitative estimate of their connection to fitness and demographic vital rates. The accuracy of parameter estimation will be improved
These challenges must be tackled by conservation genomics over the longer term. because examining several loci facilitates the identifica-
Understanding genomic approaches is crucial to the success of applying genomics tion and exclusion of loci under selection (outlier loci)
to conservation (FIG. 1). A growing list of techniques is available for detecting DNA that cause biased estimates of parameters. For example, a
sequence differences across individuals in natural populations, and these vary widely in small proportion (1–5%) of non-neutral loci can change
the density of markers across the genome, their ability to target candidate loci, the cost estimates of mean FST by 30–50%18–20, and change the
per sample, and so on. Genomic techniques can be roughly grouped into three classes: topology and branch lengths of evolutionary trees21,22.
marker-based genotyping, including a diversity of array-based SNP genotyping Similarly, the assessment of demographic parameters,
platforms; reduced-representation sequencing, which uses next-generation
such as population bottlenecks or growth rates, requires
sequencing technology to target a subset of orthologous regions across the genome of
many loci to identify outliers and reliably infer change
many individuals; and whole-genome sequencing. A crucial component of all genomic
techniques is bioinformatics. The tools for handling genomic data are changing as fast in population size. Selection can shrink (by bottlenecks)
as (and in response to) techniques for gathering the data, and we do not review the or expand genealogies at a locus23. Therefore, inferences
software and analytical issues here111. Nonetheless, researchers using genomic about population growth should be more robust if out-
techniques should plan on a substantial investment of time and resources devoted to lier loci are removed, for example by using a hierarchical
data storage and analysis. Bayesian model to assess the parameters of each locus
separately 24.
Increasing the number of markers will also facilitate
There have been several excellent reviews on con- estimation of directionality of migration (emigration
Inbreeding coefficient servation genomics recently 3,14–17. We have attempted to and immigration rates), especially if haplotypes can be
The probability that two alleles
build on these reviews and to distinguish ours by mak- inferred from linked loci25. Certain questions require
in an individual are both
descended from a single allele
ing specific practical recommendations on how genomic linked loci or can be vastly improved by using haplotype
in an ancestor (that is, that approaches can be applied to key problems in conserva- inference; for example, estimating relationships among
they are ‘identical-by-descent’). tion (TABLE 1). For example, Ouborg et al.15 present a com- individuals26, population structure27, admixture28, dates of
prehensive view of how genomics will provide insights historical bottlenecks and directionality of migration25.
Contig
An abbreviation for contiguous
into the mechanisms behind the interaction between Furthermore, it will become increasingly feasible to
sequence; used to indicate a selectively important variation and environmental jointly estimate multiple parameters, which generally
contiguous piece of DNA that conditions. Nevertheless, if we are to apply this under- requires more loci than single parameter estimation. For
is assembled from shorter standing of fitness to conservation, we need to address example, likelihood, Bayesian and approximate Bayesian
overlapping sequence reads.
the population-level consequences of genetic variation, estimators combined with coalescent approaches will
Metagenomics which include population subdivision, demography and allow the simultaneous estimation of multiple param-
The study of the collective population viability. We have incorporated population eters, such as Ne and m 25,29, or Ne and the selection
genomic material contained in structure and demographic effects into FIG. 1, and have coefficient (s)30. This is important because it will improve
an environmental sample of distinguished issues that only genomic approaches can parameter estimation, allow parameter estimation in
microorganisms, facilitated by
high-throughput sequencing
thoroughly address from issues that can be adequately metapopulations (not just in isolated populations with
technology that allows the tackled with traditional techniques. no gene flow), and facilitate investigations of the relative
direct sequencing of We have two primary objectives. The first is to iden- importance and interactions among drift, selection and
heterogeneous samples. tify those problems in conservation biology in which migration in populations of conservation concern.
genomics will be most valuable in providing new insights By contrast, simulations suggest that as the number
Endosymbiont
An organism that lives within
and understanding. The second is to provide guidelines of loci increases, the accuracy of parameter estima-
the cells of a host organism. as to which new genomics approaches will be most tion can decrease owing to non-independence or link-
appropriate for the different problems in conservation age among loci31. Failure to account for linkage could
Inbreeding depression that can benefit from genetic analysis. limit the utility of SNPs or multi-locus sequencing in
The loss of vigour and fitness
that is observed when
We begin by focusing on issues in conservation studies using genealogical information32. Markers are
genome-wide homozygosity genomics that are immediately accessible (for example, usually assumed to be independent. Failure to account
is increased by inbreeding. increasing the number of neutral markers) and then for non-independence can lead to overestimation of
698 | O CTOBER 2010 | VOLUME 11 www.nature.com/reviews/genetics

REVIEWS
Population size Population structure directly. Skare et al.26 conducted simulation power analy-
ses and showed that relatively distant relationships (for
example, cousins) can be inferred using 500,000 SNPs
Migration rates and likelihood-based relationship estimators.
Nonetheless, pedigrees often will not have sufficient
depth or completeness because it is difficult to sample
Genetic drift Inbreeding Hybridization most individuals in a population over many years. In
such cases, genotyping thousands of loci could poten-
tially give more reliable estimates of relationships and
Loss of genetic diversity Genotype-by-environment
interactions
Local adaptation individual heterozygosity (inbreeding) than pedigrees26,38
or at least greatly improve pedigree reconstruction37.
Future research is needed to quantify the trade-off point
Loss of adaptive variation Inbreeding depression Outbreeding depression between using pedigree inference versus thousands of
genetic markers to estimate individual inbreeding.
Demographic vital rates Individual-based population genetics. Individual-based

approaches can yield less biased delineation of popula-
tions than traditional population-based approaches that
Population growth or viability require somewhat subjective grouping of individuals39
(for example, based on morphology or geographic
Figure 1 | Schematic diagram of interacting factors in conservation of natural
Nature provides
Reviews | direct
Genetics origin). For population delineation, an empirical study
populations. Traditional conservation genetics, using neutral markers,
estimates of some interacting factors (blue). Conservation genomics can address a wider of 377 microsatellites in humans has shown that using
range of factors (red). It also promises more precise estimates of neutral processes (blue) greater numbers of loci can increase statistical power to
and understanding of the specific genetic basis of all of these factors. For example, resolve between closely related ethnic groups (FST < 0.05)
traditional conservation genetics can estimate overall migration rates or inbreeding and infer the proportion of admixture40,41.
coefficients, whereas genomic tools can assess gene flow rates that are specific to Individual-based approaches can give less biased
adaptive loci or founder-specific inbreeding coefficients. estimation of contemporary migration rates without
assumptions such as mutation–migration–drift equilib-
rium42. However, the power to estimate contemporary
precision and overconfidence in subsequent inferences. migration rates is low unless FST is relatively high (for
Fortunately, the problem is likely to be minor unless loci example, FST > 0.10) when using only 10–20 microsatel-
Adaptation
are tightly linked33. Failure to consider linkage could also lite loci43. Little is known about power when genotyp-
Heritable changes in genotype have other effects; for example, human loci in regions ing hundreds of loci, although Rannala and Mountain44
or phenotype that result in of lower recombination tend to have greater FST, appar- reported that an assignment test method using 50–100
increased fitness. ently because of the greater probability of being associ- loci gave reasonable power to identify individuals with
ated with selected loci in chromosomal regions with less grandparents from different countries, although the
Hybridization
Interbreeding of individuals recombination34. differentiation of allele frequencies among populations
from genetically distinct was low. Individual-based approaches are crucial for
populations, regardless Description of kin relationships and pedigrees. fine-scale spatial genetic analyses to localize genetic dis-
of the taxonomic status of Examining hundreds of loci will vastly increase the continuities (for example, barriers or secondary contact
the populations.
precision and accuracy of kinship estimates. For exam- zones) on a landscape. Individual-based approaches in
Outbreeding depression ple, Santure et al.35 showed that the average pair-wise landscape genetics45 also allow assessment of the influ-
Reduced fitness of F1 or F2 relatedness estimated from 771 SNPs closely brackets ence of landscape features on dispersal and gene flow
individuals after a cross known pedigree relationships for a pedigree population across spatial scales.
between two species or
of zebra finch. This suggests that assessments of correla-
populations. It can result from
genetic incompatibility or tions between phenotypes and genetic relatedness and Inbreeding depression
reduced adaptation to local thus estimation of heritability will be feasible in natural Genomic approaches can potentially address basic ques-
environmental conditions. populations. Nevertheless, the accuracy of estimating tions about the molecular basis and genetic architecture
individual levels of inbreeding is somewhat limited, and of inbreeding depression46. For instance, is inbreeding
Effective population size
The size of the ideal population
the variances for relatedness between individuals remain depression caused by a few loci with major effects or by
that would experience the substantial even with 771 SNPs36. many loci with small effects? How much of inbreeding
same amount of genetic drift Pedigree reconstruction will become feasible in some depression results from dominance (or partial domi-
as the observed population. wild populations with hundreds of loci33,37. This will nance) versus overdominace (heterozygous advan-
improve estimates of effects of inbreeding and outbreed- tage)? What is the contribution of epistasis to inbreeding
Outlier locus
A genome location (or marker ing on fitness and the detection of paternities or pol- depression? Understanding the number of loci involved
or base pair) that shows len flow between populations and over long distances, in inbreeding depression and the mechanism of their
behaviour or a pattern of if most individuals can be sampled over many years. effects would allow prediction of the potential efficacy
variation that is extremely Santure et al.35 suggested that using marker information of purging.
divergent from the rest of the
genome (locus-specific effects),
to reconstruct the pedigree, and then calculating relat- Recent work indicates that the intensity of inbreed-
as revealed by simulations or edness from the pedigree, is likely to give more accurate ing depression can differ greatly depending on which
statistical tests. relatedness estimates than using marker-based estimators specific individuals are founders47,48. This suggests that

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Box 2 | Detection of cryptic subdivision and local adaptation in marine species

There is little genetic drift in many marine fish and invertebrates because of their large population sizes121,122. As a
FST consequence, population genetic studies of many marine species have failed to detect genetic substructure even
A measure of population between geographically disjunct subpopulations for which there is evidence of reproductive isolation122. The absence
subdivision that indicates the of genetic differentiation at neutral markers, however, should not be taken to mean the absence of adaptive
proportion of genetic diversity
differences. The amount of genetic divergence among subpopulations at selectively neutral markers is largely a
found between populations
function of the number of migrants per generation (Nem) rather than the migration rate (m). With large population
relative to the amount
within populations.
sizes, even very low migration or dispersal rates can result in enough migrant individuals to eliminate genetic
evidence of population differentiation at neutral loci, but not at locally selected adaptive loci.
Population bottleneck We expect this effect to be greatest in marine species because of the large local population sizes, which allow
A marked reduction in selection to be more efficient because drift is weaker. The amount of divergence at selected loci is determined by the
population size followed by the relative values of migration and selection coefficient (s). Species with larger local populations (Ne) will have much
survival and expansion of a lower rates of migration than species with small population size with the same number of migrants and amount of
small random sample of the divergence at neutral loci. Therefore, even fairly weak selection may bring about genetic differentiation between
original population. It often
subpopulations in species with large local population sizes because s is much more likely to be greater than m.
results in the loss of genetic
This prediction is supported by a recent study123 of Atlantic cod (Gadus morhua) in which almost no genetic
variation and more frequent
matings among closely
differentiation (FST = 0.003) was found at nine microsatellite loci, but substantial differentiation (FST = 0.261) was found
related individuals. at the PanI locus, which previous studies have shown to be under natural selection105. Similarly, Haemmer-Hansen et al.124
reported an FST of 0.45 at a heat shock protein locus in comparison to a mean FST value of only 0.02 at nine
Hierarchical Bayesian model microsatellite loci in the European flounder (Platichthys flesus). This approach of simultaneously comparing many
A Bayesian model in which neutral and candidate gene markers has been highly successful in a range of species19.
the prior depends on another In addition, the absence of genetic differentiation in marine species should not be interpreted to indicate that
parameter that is not in the populations are demographically connected as a single management unit125. Demographic connectivity is
the likelihood function and
largely a function of the proportional amount of exchange. Therefore, low migration rates (m < 0.001) can result
that can vary and have
in a substantial number of migrant individuals when local population sizes are in the thousands, resulting in FST
another prior.
values near zero. Much greater exchange is necessary for demographic connectivity between populations.
Haplotype For example, Waples and Gaggiotti126 have suggested that m must be greater than 10% for populations to be
A set of genetic markers demographically interdependent.
that are present on a single
chromosome and that show
complete or nearly complete the genetic load is unevenly spread among founder affected by selection at a particular locus, but that fine-
gametic disequilibrium. genomes and supports the notion that inbreeding mapping of a selected locus will be more difficult. Ideally,
They are inherited through depression sometimes results from major effects at a few researchers would study populations with both long and
generations without being
loci49. The founder-specific partial F coefficient is the short chromosomal regions of gametic disequilibrium
changed by crossing-over
or other recombination identical-by-descent (IBD) probability (for an individual) to allow for initial coarse-mapping and subsequent
mechanisms. that is attributed to a particular founder. A study with fine-mapping of loci under selection.
Ripollesa domestic sheep found that most of the inbreed- In the future, it could be possible to identify loci that
Admixture ing depression resulted from individuals being IBD for contribute to inbreeding depression by sequencing the
The production of new
genetic combinations in
genes from just two of the nine founders49. Managing whole genomes of parents and offspring. For example,
hybrid populations through founder-specific inbreeding depression using partial Roach et al.53 analysed the complete genome sequence
recombination. inbreeding coefficients could be extremely effective in of two parents and their two children, who suffered
cases in which inbreeding depression results primarily from two clinical recessive disorders. They narrowed
Coalescent approach
from a few loci with major effects; such partial inbreed- down the candidate genes for both of these Mendelian
A means of investigating the
shared genealogical history ing coefficients could be useful when selecting potential disorders to four using family-based genome analysis.
of genes. A genealogy is matings in a captive population.
constructed backwards in time Local adaptation
starting with the present-day
Identifying alleles responsible for inbreeding depression. One of the most promising aspects of applying genomic
sample. Lineages coalesce
when they have a common
Genome scans of large numbers of markers can detect tools to conservation is the simultaneous estimation
ancestor. the signature of inbreeding depression. Deleterious reces- of neutral (that is, genome-wide average) processes
sive alleles related to inbreeding depression have been along with identification of specific genomic regions
Selection coefficient identified in a few species46,50,51. In general, attempts to responding to selection, such as adaptation to local
A term that describes the
identify loci responsible for inbreeding depression may conditions that vary across a metapopulation. These
difference in average fitness
between genotypes when be less successful than those aimed at positive selection specific genomic regions appear as outliers from the
fitness is measured relative to for a few reasons. First, detecting the multiple genetic patterns observed at the neutral genomic background,
the average fitness of one of mechanisms that may underlie inbreeding depression, which is determined primarily by genetic drift and gene
the genotypes (known as the
including epistasis and genotype-by-environment inter- flow. Researchers have developed multiple approaches
reference genotype).
action, may prove more difficult 52. Second, populations to detect these outliers54,55 (BOX 3). The utility of these
Metapopulation of interest are likely to be small, necessitating small approaches depends on the timescale over which selec-
A collection of populations sample sizes, which reduce power and accuracy. Third, tion has operated and the study’s taxonomic scale (for
of a species found in differing the longer regions of gametic disequilibrium expected example, the study might be investigating divergence
geographic locations and
in small inbred populations (observed in wolves by among species, differentiation among populations
with restricted gene flow
(exchange of genes) between Hagenblad et al.46) mean that genotyped anonymous within a species or evolutionary history within a single
the populations. markers are more likely to lie within a genomic region population), as well as on the techniques used55.

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Table 1 | Primary genetic problems in conservation and how genomics can contribute to their solution*
Primary problem Possible genomic solution
Estimation of Ne, m and s Increasing the number of markers, reconstructing pedigrees and using
haplotype information will provide greater power to estimate and monitor Ne
and m, as well as to identify migrants, estimate the direction of migration and
estimate s for individual loci within a population
Reducing the amount of admixture Genome scanning of many markers will help to identify individuals with greater
in hybrid populations amounts of admixture so that they can be removed from the breeding pool
Identification of units of conservation: The incorporation of adaptive genes and gene expression will augment our
species, evolutionarily significant understanding of conservation units based on neutral genes. The use of
units and management units individual-based landscape genetics will help to identify boundaries between
conservation units more precisely
Minimizing adaptation to captivity Numerous markers throughout the genome could be monitored to detect
whether populations are becoming adapted to captivity
Predicting harmful effects of Understanding the genetic basis of inbreeding depression will facilitate the
inbreeding depression prediction of the effectiveness of purging. Genotyping of individuals at loci
associated with inbreeding depression will allow the selection of individuals as
founders or mates in captive populations. Pedigree reconstruction will allow
more powerful tests of inbreeding depression
Predicting the intensity of Understanding the divergence of populations at adaptive genes will help
outbreeding depression to predict effects on fitness when these genes are combined. Detecting
chromosomal rearrangements will help to predict outbreeding depression
Predicting the viability of local Incorporating genotypes that affect vital rates and the genetic architecture of
populations inbreeding depression will improve population viability models
Proportion of admixture Predicting the ability of populations Understanding adaptive genetic variation will help to predict the response
The proportion of alleles in a to adapt to climate change and other to a rapidly changing environment or to harvesting by humans and allow the
hybrid swarm or individual anthropogenic challenges selection of individuals for assisted migration
that comes from each of
*These problems are listed from top to bottom in sequence of those that can be immediately addressed to those that will become
the hybridizing taxa. more feasible to address in the future. m, migration rate; Ne, effective population size; s, selection coefficient.
Epistasis
The dependency of the For most conservation purposes, only a subset of Genomic databases may even come from related species,
effects of alleles at one locus
on the genotypes at other
these tools will be most appropriate, and application so that rare species of conservation concern are ‘genome-
loci in the genome. of the wrong approach could result in type I and type II enabled’ by the resources of better-studied, related taxa3.
errors. Specifically, detecting genomic regions that are A growing variety of genomic tools can also be used
Purging responsible for local adaptation in a species relies on directly to genotype individuals at up to thousands of
The selective reduction in
comparisons among related populations that may or candidate loci (TABLE 2).
frequency of deleterious
recessive alleles in small may not be linked by ongoing gene flow. In this case, The second major approach to detecting local adap-
populations because the the most appropriate analyses often will focus on dif- tation searches the genome for signatures of selection
increase in homozygosity ferentiation in allele frequencies among populations using anonymous markers66,67. A limitation here is that
increases the ability of selection (that is, FST20). Within a single population, the allele fre- markers must be in gametic disequilibrium with selected
to act on recessive alleles.
quency spectrum can indicate regions under selection55. loci to exhibit a signature of selection, and the signa-
Identical-by-descent By contrast, techniques for detecting historical selection ture can be quite small depending on the nature of the
An allele shared by two based on fixed sequence divergence between species or selection. In particular, local adaptation with ongoing
related individuals is said to the relationship between divergence and polymorphism gene flow between populations subject to differential
be identical-by-descent if
are likely to have only limited applications in conser- selection is expected to produce a soft sweep; such a
the allele is inherited from the
same common ancestor. vation because of the longer timescale of selection that signature of selection can have a very narrow footprint
can be detected (but see Garrigan and Hedrick56). Here along the genome and be difficult to detect, even given
Gametic disequilibrium we focus on the first case — local adaptation among strong selection68. Nonetheless, the density of markers
A measure of whether alleles at populations within a species. along the genome allowed by high-throughput genomic
two loci in a population occur
in a non-random fashion.
techniques can be sufficient to identify these regions,
Methods for assessing local adaptation. There are two especially when replicate populations subject to simi-
Type I and type II errors general ways to assess local adaptation in the genome lar selection pressures can be sampled66. The array of
Statistical errors in which (BOX 3): the first starts with a list of candidate loci or genomic techniques covers the range of trade-offs
a true null hypothesis is
genomic regions and asks whether these lie in the tails of between density of markers and number of individuals
rejected (type I) or a false
null hypothesis is not the genome-wide distribution of population differentia- or populations sampled. Any information on the overall
rejected (type II). tion57–60. Genomics can augment these studies indirectly amount of gametic disequilibrium can inform the exper-
by providing a list of candidates; for example, expressed imental design of genome scans (see Supplementary
Expressed sequence tag sequence tag (EST) databases allow for the bioinformatic information S1 (figure)).
A short DNA fragment (several
hundred base pairs) produced
identification of microsatellites or other traditional There are trade-offs between the two general
by reverse transcription of markers closely linked with target genes, and primers or approaches outlined above. The first allows targeting
mRNA into DNA. probes can be developed from these EST sequences61–65. of particular loci, which can be valuable if selection is

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suspected to act on particular phenotypic traits and func-

Box 3 | Genome scans to detect local adaptation
tional genetic information is available from related spe-
a 0.14 cies. This approach can also be applied to a larger number
of individuals or populations for the same overall effort.
0.12
By contrast, the second approach is most useful in the
0.10 absence of a priori hypotheses about specific loci or selec-
tive pressures and can provide quantitative information,
0.08
such as estimates of how many regions of the genome are
FST
0.06 subject to selection, as well as test whether selection is

acting on similar genomic regions across populations.
0.04 These approaches can also be combined; for example,
0.02 genotyping arrays can be printed with a combination
of probes for candidate and anonymous loci.
0
0 0.10 0.20 0.30 0.40 0.50
Expected heterozygosity Climate change and other anthropogenic challenges.
b 0.8 An important component of conservation genetics is
0.6 understanding how to maintain the ability to evolve in
0.4 anticipation of environmental change; for example, cli-
FST
0.2 mate change will affect a wide range of species and habi-
0 tats. Genomic approaches may allow the identification
–0.2 of adaptive genetic variation related to key traits, such as
0.8 phenology or drought tolerance, so that management may
0.6 focus on maintaining adaptive genetic potential. In this
FST
0.4
context, a landscape genomics approach allows the map-
0.2
ping of associations between adaptive genome regions69
0
and environmental gradients in space and time. This
–0.2
0.8 could allow forecasting of the effects of environmental
0.6 change on gene flow of adaptive alleles by predicting
FST
0.4 spatial–temporal landscape change and modelling gene

0.2 flow across landscapes expected in the future.
0 The harvest of phenotypically desirable animals from
–0.2 wild populations imposes selection that can reduce the
0.8
0.6
frequencies of those desirable phenotypes70. In addition,
genetic changes in response to the harvesting of animals
FST
0.4
0.2 by humans threaten the persistence of many species71.
0 The use of genomics to monitor these genetic changes
–0.2 could be extremely important because early detection of
potentially harmful changes will maximize our ability to
0 50 100 150 200 250 300 350 400
Position (Mb) implement management to limit or reverse the effects
before substantial or irreversible changes occur 71.
Nature Reviews | Genetics
Genome scans for selection can focus on either candidate loci or anonymous loci.
Namroud et al.62 sampled white spruce (Picea glauca) from 6 populations in Quebec and Units of conservation and hybridization
genotyped 534 SNPs located on 345 candidate genes. Part a of the figure shows their FST Describing units of conservation is one of the most
outlier analysis of these data, based on the relationship between FST and expected important contributions of genetics to conservation72.
heterozygosity59; the grey and red lines represent the 95% and 99% confidence levels, The identification of appropriate taxonomic and popu-
respectively. Against a background of little population differentiation (FST = 0.006), this
lation units for protection and management is essential
analysis identified 20 SNPs (circled dots) in 19 genes above the 95% confidence level. New
genomic tools also allow anonymous markers to be assayed across the genome to identify
for the conservation of biological diversity. For species
local adaptation; for example, Hohenlohe et al.66 sampled 100 threespine stickleback identification and classification, genetic principles and
individuals across 5 populations in Alaska. They used sequencing of restriction-site- methods are relatively well developed. Nevertheless,
associated DNA (RAD) tags127 to simultaneously identify and genotype over 45,000 SNPs species identification remains controversial, and agree-
across the genome. This density of markers allows population genetic statistics, such as FST, ing upon a uniform definition of species is Frankham’s
to be visualized as continuous distributions along chromosomes. In part b of the figure, number two priority for conservation genetics72.
the top panel shows FST between the two marine populations. The next three panels show A great deal of effort is currently involved in describ-
differentiation between each of the three freshwater populations and the two marine ing units within species that are distinct enough to
populations. Coloured bars above each graph show regions of significantly elevated FST, require separate management: these units include
as indicated by bootstrap resampling (blue, p ≤ 10–5; red, p ≤ 10–7). Vertical grey shading
evolutionarily significant units (ESUs), distinct population
indicates the chromosomes, and yellow shading indicates the nine most significant and
segments and management units. The identification of
consistent peaks of freshwater-versus-marine differentiation. Common patterns of
population differentiation (yellow shading shared among the three populations) population units is necessary so that management and
indicate genomic regions that have responded to divergent selection in parallel across monitoring programmes can be efficiently targeted
populations.The image in part a is reproduced, with permission, from REF. 62 © John towards distinct or independent populations; such
Wiley and Sons. The image in part b is reproduced from REF. 66. methods could be used to effectively plan harvesting

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Table 2 | Major techniques for detecting DNA sequence variation and considerations for conservation applications
Traditional qPCR-based SNP High-density Targeted DNA Anonymous DNA Whole-genome
markers chips SNP chips sequencing sequencing resequencing
Summary Various techniques Hybridizing array; High-density Fragment High-throughput Sequencing of
for small to genotyping by oligonucleotide capture with sequencing whole genome
moderate numbers real-time qPCR hybridizing array oligonucleotide of reduced for multiple
of markers with fluorescent array; genotyping representation individuals in a
probes by next-generation genomic DNA sample
sequencing fragments
Examples Microsatellites; Fluidigm Affymetrix Exon capture110 RAD sequencing127 Next-generation
exon-priming dynamic arrays; GeneChip; and future
intron-crossing Illumina Golden Illumina sequencing
markers Gate; Applied BeadChip129 technologies
Biosystems
OpenArray128
General considerations
Cost per sample Variable US$10–50 $200–500 $200–1,000 $50–150 $500–5,000
Number of markers 10 –10 1 2
10 –10
2 3
10 –10
4 5
10 –10
4 5
10 –10
4 6
Complete genome
Applicability to Moderate Low Low Low–moderate High Low
new taxa
Ability to target Yes Yes Yes Yes No Yes
candidate loci (bioinformatically)
DNA quality Low Low High High Low–moderate High
required
Equipment PCR machine; $100,000 platform $150,000 platform $5,000 for PCR machine; Next-generation
needed traditional equipment; next-generation sequencer,
sequencer next-generation sequencer bioinformatics
sequencer resources
Utility
Pedigree/kin in Limited Limited–moderate Yes Yes Yes Data overkill in
wild populations; most cases
individual-based
population
genetics
Neutral Yes, but variance Yes, but variance Increased Increased Increased More data than
(genome-wide due to few markers due to moderate accuracy; can accuracy; can accuracy; no needed
average) number of markers include candidate include candidate previous genomic
landscape loci loci resources
genetics
Detecting loci Useful after Useful after Allows genome Allows genome Dense genome Most appropriate
of interest markers at markers at scanning along scanning along coverage for in family-based
(inbreeding candidate loci candidate loci with candidate loci with candidate de novo mapping studies
depression, have been have been loci and targeting
outbreeding identified identified chromosome
depression, local regions
adaptation)
Marker-assisted Efficient screening Efficient screening Allows genomic Overkill after Overkill after Overkill after
restoration of few known of few known selection key markers are key markers are key markers are
markers markers approaches identified identified identified
qPCR, quantitative PCR; RAD, restriction-site-associated DNA.
quotas (to avoid overharvesting, for example) or to modifications by humans. Hybridization has contributed
devise ways to translocate and reintroduce individuals to the extinction of many species73,74. Genomics could
(to avoid, for example, the mixing of adaptively dif- have an important role in distinguishing between natural
ferentiated populations). It is sometimes necessary to and anthropogenic hybridization73. Also, genomics pro-
prioritize population units for conservation owing to vides the potential to predict the effects of hybridization
limited financial resources. on fitness (heterosis or outbreeding depression).
Hybridization is one of the major threats to con-
Phenology servation of many plant and animal species73. Rates Units of conservation. The description of conserva-
The timing of periodic
biological phenomena
of hybridization and introgression have increased dra- tion units generally requires two steps: estimating the
that are usually correlated matically worldwide because of widespread intentional amount of gene flow among populations and evaluat-
with climatic conditions. and incidental translocations of organisms and habitat ing the amount of adaptive divergence. The ability to

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genotype many neutral loci will provide much better 12 Atlantic salmon (Salmo salar) populations to exam-
estimates of the patterns of reproductive isolation and ine global patterns of gene expression and found they
demographic history of populations to address the first were concordant with patterns of divergence at seven
step. Genomic approaches for studying functional genes microsatellite loci. These results support the notion that
will provide the opportunity to evaluate the amount of patterns of divergence at neutral loci reflect patterns of
adaptive divergence among populations required in the adaptive variation in gene expression.
second step, and its distribution across the genome.
Conservation units have been described on the Detection of hybridization. Molecular detection of
basis of divergence at loci that are assumed to be selec- hybridization and estimation of the proportion of admix-
tively neutral. It has been suggested that this could be ture between genetically divergent populations can be
improved by including genetic divergence at adaptive accomplished accurately with tens of loci73,82. However,
markers along with the divergence at neutral loci75–77. accurate description of the dynamics of hybridization
Adaptive markers could enhance and help set priori- and introgression can require hundreds of loci83. In addi-
ties for the identification and management of units of tion, estimation of the proportion of admixture within
conservation. However, a complete understanding individuals will require many more markers.
of adaptive divergence is unattainable. Moreover, a For example, Halbert and Derr 84 found that 7 of 11
recent comparison of assumed neutral and putatively US federal bison (Bos bison) populations contained
selected alleles in over 640,000 autosomal SNPs in introgression from domestic cattle (Bos taurus) based
humans concluded that average allele frequency diver- on 14 nuclear loci. The conservation value of admixed
gence is highly predictive of adaptive divergence and populations has been controversial 73,85,86, and some
that neutral processes (population history, migration believe that these herds should not be considered as
and effective population size) exert powerful influences bison for conservation purposes87. However, this posi-
Landscape genomics
The study of many markers,
over the geographic distribution of selected alleles78. tion has not been generally accepted87. Regardless, the
including markers in genes This result supports the use of neutral loci to provide potential to estimate the proportion of cattle alleles in
under selection, in spatially useful descriptions of the patterns of divergence at individual bison will allow the selection of individuals
referenced samples collected adaptive loci. to reduce the magnitude of introgression from cattle in
across a landscape and often
There are pitfalls in focusing on individual adap- managed bison herds.
across selection gradients. It
uses comparisons of adaptive tive loci rather than neutral patterns or genome-wide Genomics provides exciting opportunities to assess
and neutral variation to quantify averages. Genes important for contemporary or past differential rates of introgression across different
the effects of landscape adaptations might not be those that will be crucial genomic regions following hybridization88. For exam-
features and environmental for adaptation in future environments. In addition, much ple, Fitzpatrick et al. 89 found that 3 of 68 markers
variables on gene flow and
spatial genetic variation.
effort has been devoted recently to genome-wide asso- spread rapidly into native California tiger salamanders
ciation studies for detecting the genetic basis of com- (Ambystoma californiense), whereas the other 65 markers
Evolutionarily significant unit plex traits, particularly disease in humans, using large show little evidence of spread beyond the region where
A classification of populations samples of individuals and genetic markers. Although introductions of non-native barred tiger salamanders
that have substantial
many candidate genes have been identified, often a large (Ambystoma tigrinum mavortium) occurred. Differential
reproductive isolation which has
led to adaptive differences so proportion of the heritability remains unexplained79. A introgression rates of genomic regions raises some dif-
that the population represents focus on detectable adaptive genomic regions could ficult issues with regards to treating hybridized popu-
a significant evolutionary result in loss of important genetic variation at other lations in conservation89 and brings into question the
component of the species. regions. Moreover, even when the same genomic regions efficacy of using a few (that is, ten or so) neutral markers
Distinct population segment
are implicated in, for example, local adaptation across to detect hybridization.
A classification under the populations, the particular alleles involved may be dif-
Endangered Species Act ferent and perhaps even result in outbreeding depression Outbreeding depression. Concerns about the possibility
of the United States that when combined. of outbreeding depression have restricted, perhaps
allows for legal protection of
Landscape genomics will help to identify manage- unnecessarily, the use of managed gene flow to avoid
populations that are distinct,
relatively reproductively ment units by providing sufficient power to localize increased risks of extinction caused by loss of genetic
isolated and represent a boundaries on the landscape that separate demograph- variation because of habitat fragmentation and isola-
significant evolutionary ically independent groups. Examination of hundreds tion. Frankham72 has identified the development of
lineage to the species. to thousands of loci in hundreds of individuals across methods for predicting outbreeding depression as the
Management unit
landscapes will improve assessments of the interac- top priority in conservation genetics. Outbreeding
A local population that is tions of gene flow, genetic drift and natural selection depression can result from either chromosomal or genic
managed as a unit owing to its in influencing the evolution and persistence of popula- incompatibilities between hybridizing taxa (intrinsic
demographic independence. tions. Landscape genomics will help to identify ESUs outbreeding depression) or reduced adaptation to
(and spatial locations of boundaries between them) by local environmental conditions (extrinsic outbreeding
Introgression
Gene flow between including both neutral and adaptive variation. depression)90. Genomic approaches can potentially
populations or species Recent papers have explored the potential of tran- provide valuable empirical information for predicting
whose individuals hybridize. scriptomic analysis of gene expression to assess func- the probability of either of these sources of outbreeding
tional genetic divergence among populations80; for depression; for example, next-generation sequencing
Heterosis
When hybrid individuals
example, Tymchuk et al.81 hybridized a microarray using paired-end reads can be used to detect chromosomal
have greater fitness than with 16,000 salmonid cDNAs (16K cDNA microarray) rearrangements91, such as large inversions or gene copy
either of the parental types. to RNA extracted from whole fry raised in captivity in number variation92.

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Genomic approaches will also be increasingly Minimizing adaptation to captivity. The emphasis of
used to detect outbreeding depression by estimating captive breeding protocols has been to reduce genetic
the number of progeny produced by individuals with drift by maximizing effective population size98, which
different proportions of admixture. For example, is appropriate for captive breeding programmes of
Muhlfeld et al. 93 estimated the individual propor- mammals and birds in zoos that have a relatively small
tion of admixture between introduced rainbow trout number of individuals that are managed using pedigrees.
(Oncorhynchus mykiss) and native westslope cutthroat
trout (Oncorhynchus clarkii lewisi) (FIG. 2).
a
16
Captive breeding and assisted migration
Mean number of offspring per female

Genomic tools may assist the management of ex situ 14
populations and reintroductions by providing increased 12
precision and accuracy of estimates of neutral popula-
tion genetic parameters and by identifying specific loci 10
of importance, which is essential for selecting founder 8
individuals. First, many neutral loci could be used to
construct a more precise pedigree of the captive popula- 6
tion and determine whether the founders from the wild 4
are kin. Second, screening of the founders for known
deleterious recessive alleles could substantially reduce 2
any subsequent inbreeding depression in the captive 0
population. In addition, screening of the founders for 0 0.2 0.4 0.6 0.8 1.0
known adaptive alleles could increase the evolutionary Proportion of rainbow trout admixture
potential of the captive population. b
5
Managing inbreeding depression. The overarching goal
Mean number of offspring per male
of maintaining genetic diversity in an ex situ population 4
pre-dates genomic techniques. Nonetheless, genome
scans may produce better estimates of genome-wide het-
3
erozygosity and genetic diversity than smaller numbers
of traditional markers, such as microsatellites94. Methods
are being developed to maximize the sampling of genetic 2
variation for founders of captive breeding colonies
based on genomic data95. A caveat here is that the rela-
1
tionship between genome-wide average heterozygosity
and inbreeding depression is not always strong. As a
result, a more powerful application of genomics may be 0
to estimate pedigrees and degrees of relatedness among 0 0.2 0.4 0.6 0.8 1.0
Proportion of rainbow trout admixture
captive or founding individuals35,96, allowing captive
management plans to minimize inbreeding per se. Figure 2 | Effects of proportion of individual admixture
The ability to use genomics to identify specific loci Nature Reviews | Genetics
with introduced rainbow trout on the fitness of native
related to local adaptation or inbreeding depression and westslope cutthroat trout. Sixteen microsatellite loci
Marker-assisted selection the success of marker-assisted selection in livestock were used to estimate the individual proportion of
The use of molecular genetic and crops97 raise the possibility of managing specific admixture between introduced rainbow trout and native
markers to increase the
loci in some conservation situations. For example, westslope cutthroat trout93. These same loci were used to
response to selection in a identify the parents of progeny produced in a stream over
population by the favouring of individuals with particular adaptive genetic variants
a 5-year period. The bubble plots show the mean number
reproduction by individuals could be chosen for reintroduction or genetic rescue. of offspring per individual identified plotted against the
with a certain allele or In captive breeding programmes, particular genetic proportion of rainbow trout admixture for females (a) and
genotype. The marker is variants could be selected against. In one example, the
closely linked to a quantitative
males (b). In a bubble plot, the size of the bubble is
trait locus.
small population of the California condor (Gymnogyps proportional to the number of observations with that
californianus) has a relatively high frequency of a recessive value. The mean values for first-generation hybrids are
Genetic rescue lethal allele causing chondrodystrophy. A condor genom- shown as triangles; these points were not included in the
The recovery in the average ics project is seeking a marker to identify carriers of the regression. These results are striking in two ways. First,
fitness of individuals through
chondrodystrophy allele, and members of this project there was a strong reduction in the number of progeny
increased gene flow into small produced as the amount of admixture with introduced
populations, typically following have therefore developed several genomic resources,
rainbow trout increased in both females and males.
a fitness reduction due to including a bacterial artificial chromosome library
Second, first-generation hybrids had much greater
inbreeding depression. and a fibroblast cell line for transcriptomic analysis17, reproductive success than other individuals with 50%
with the goal of designing breeding programmes to admixture. This suggests a strong heterotic effect in the
Chondrodystrophy
A genetically based skeletal
select against heterozygotes for the chondrodystrophy first-generation hybrids caused by sheltering of
disorder that affects the allele while minimizing loss of genetic diversity deleterious recessive alleles. Figure is reproduced, with
development of cartilage. elsewhere in the genome. permission, from REF. 93 © (2009) The Royal Society.

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However, adaptation to captivity is a serious problem Choosing genomic approaches

associated with captive breeding programmes for many The diverse and growing list of genomic techniques
species99,100. This will inevitably reduce the fitness of provides a range of options for experimental design
individuals reintroduced to wild or natural conditions. (TABLE 2). Currently, array-based techniques (SNP chips)
For example, tameness in response to humans is gener- can efficiently genotype markers across many individuals
ally advantageous in captivity but can have serious con- for a range of conservation applications. As the cost of
sequences in the wild. In addition, increasing effective sequencing continues to fall, reduced-representation
population size for some captive species (for example, sequencing may replace SNP chips as a preferred method
fish and plants) may increase the rate of adaptation to in many cases110. Sequence data can provide additional
captive conditions. Genetic monitoring 101 of many loci information for functional assessment of candidate
throughout the genome should become a standard tool genes or detection of haplotype structure or inversion
for detecting adaptation to captivity (that is, rapid, locus- polymorphisms, and sequencing is easily applied to taxa
specific change in allele frequencies) in species for which without any existing genomic resources. However, at
adaptation to captivity is a concern100. least in the near term, array techniques will retain their
advantage of having a highly standardized protocol for
Restoration. The condor example highlights the com- genotyping a fixed set of markers. This makes them well-
plexity of identifying specific loci to allow targeted suited to, for example, long-term genetic monitoring
genetic management of populations, even when a single of populations.
Mendelian locus is implicated. However, the success of It is becoming feasible to sequence complete genomes
marker-assisted selection in livestock is due in part to in a reasonable research timeline and budget 111. Whole-
the fact that specific alleles and their functional roles genome resequencing of all individuals in a study will
need not be determined; rather a correlation between become an option in conservation112. However, while
phenotype and genotype at multiple markers is estab- there are potential uses for whole-genome resequenc-
lished, and selection on genotype produces a correlated ing, such as detection of Mendelian inherited traits in
response in phenotype (for example, growth rate or dis- families53, in most situations it is likely to create more
ease resistance). Given the ability to identify genomic challenges than it solves. First, because of linkage dis-
regions correlated with local adaptation (BOX 3), con- equilibrium, dense marker genotyping already provides
servation genomics could similarly use this informa- a nearly complete view of genomic variation113. Such
tion in, for example, selecting source populations for genomic structure is likely to be even more pronounced
translocation or reintroduction. A general risk in such in small populations of conservation concern than in
efforts is outbreeding depression as a result of differ- traditional model organisms46; whole-genome rese-
ent and incompatible genetic bases of adaptation in the quencing is thus data overkill. Moreover, whole-genome
two populations. The choice of source population can resequencing introduces many challenges for compu-
now be informed by four factors: ecological similar- tational bioinformatics; the resources simply to store,
ity, phenotypic similarity, genome-wide similarity as assemble and analyse such large data sets may outweigh
indicated by neutral markers, and genetic similarity at their benefits, at least for the near future.
adaptive loci. We envision an emerging standard for conservation
Genetic rescue has been used as an effective res- genomics in which the starting point will be a reference
toration tool to avoid or reverse the consequences of genome sequence. A rapidly growing number of species,
inbreeding depression102. However, the identification of particularly vertebrates, have reference sequences avail-
individual loci with major adaptive effects (for exam- able already 114, or an initial investment can be made to
ple, major histocompatibility complex in animals103 and produce one. From this point, genotyping of multiple
self-incompatibility loci in plants104) raises the possibility individuals from population samples would be done
of allele-specific genetic rescue. Interestingly, other loci with array-based or reduced-representation sequenc-
with exceptionally strong fitness effects are being found ing techniques, with the reference sequence providing a
in a number of species, such as PanI105 in the cod family valuable resource for sequence alignment and candidate
(Gadidae) and Pgi in butterflies and other insects106. It gene identification and annotation.
remains to be seen whether such loci are unusual or are
present in most species. Perspective
Research in community genomics suggests that indi- This is an exciting and challenging time for conserva-
vidual alleles can affect community diversity and com- tion genetics. Genomic approaches have the potential
position107–109. For example, alleles at tannin loci in to transform the management of populations for con-
cottonwood trees increase the palatability and decay servation in various ways, from estimates of pedigrees
rate of leaves, which in turn influences the abundance and inbreeding based on large numbers of markers to
of soil microbes, fungi and arboreal insects and birds108. identification of loci responsible for local adaptation
Loss or restoration of such alleles to populations could and outbreeding depression. Genomics also provides the
Community genomics thus influence community diversity and ecosystem potential to understand the genetic basis of interactions
The study of the effect of function108. Nevertheless, the complexity of these inter- among species, which could greatly enhance our abil-
individual alleles or genotypes
on the species composition,
actions presents real challenges before it will be pos- ity to manage communities rather than just individual
diversity or functioning of a sible to use this information in a practical conservation species. Perhaps the greatest contribution of genomics
community or ecosystem. situation. to conservation will be the precise genomic monitoring

REVIEWS
Epigenetics
of changes in allelic frequency to quantify the effects of the paradox of invasive species that have lost genetic
Changes in or gene expression genetic drift, natural selection and hybridization in wild variation during a bottleneck associated with their
caused by mechanisms and captive populations. introduction but are nonetheless able to adapt to new
other than changes in the Although we have focused on genomic techniques environmental conditions119.
underlying DNA sequence,
that detect variation in DNA sequences, emerging tech- Recognizing the limitations of new techniques is
such as DNA methylation
and histone modifications. niques also allow the study of epigenetics, which may also essential. Improved basic scientific understanding
have an important role in conservation genetics in the through genomics will not necessarily lead to improved
Vital rates future115,116. There is increasing evidence that epigenetic conservation. For example, genomics will make it pos-
Demographic values that processes can be important following hybridization and sible to provide genome-wide estimates of functional
affect population growth
(for example, age-specific
in outbreeding depression115,117. In addition, epigenetic genetic variation and fitness1. Nevertheless, this will
survival, fecundity and age effects might be an important source of variation for not be sufficient to improve our estimates of popula-
at first reproduction). invasive species. Richards et al.118 have shown that the tion viability unless we are able to make the connec-
invasive Japanese knotweed (Fallopia spp.), which has tions between individual fitness and population growth
little variation in DNA sequence, maintains substantial rates120 (FIG. 1). To make these connections will require
phenotypic variation even under controlled environ- long-term studies of individual fitness and of the effects
mental conditions. Epigenetic effects associated with this of fitness differences among individuals on demographic
phenotypic variation might enhance knotweed’s ability to vital rates . This is perhaps the most important and
invade novel environments. This could partially explain difficult future challenge facing conservation genetics.
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REVIEWS

Genomics and the future of

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Demographic vital rates Individual-based population genetics. Individual-based

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Box 2 | Detection of cryptic subdivision and local adaptation in marine species

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suspected to act on particular phenotypic traits and func-

0.06 subject to selection, as well as test whether selection is

0.4 spatial–temporal landscape change and modelling gene

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Mean number of offspring per female

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However, adaptation to captivity is a serious problem Choosing genomic approaches

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