The ability to examine thousands of genetic markers
with relative ease will make it possible to answer many
important questions in conservation that have been
intractable until now. Simply increasing the number of
neutral loci that we can screen will increase the power
and accuracy of estimating a variety of important
parameters in conservation (for example, kin rela-
tionships and inbreeding coefficients (F)). However,
the most exciting contributions of genomics to con-
servation are those that will allow new questions to
be addressed in a wide variety of species (BOX 1). For
instance, it should be possible to estimate the effect
size and distribution of loci affecting fitness across the
genome or to ask whether the loci are coincident across
populations1,2 (FIG. 1).
Genomic approaches are currently being used pri-
marily with a few species for which genomic informa-
tion and tools are available3; for example, wolves, bison
and bighorn sheep have been studied using genomic
tools developed in related domestic species4. However,
the range of species is expanding as new approaches are
developed that are not dependent on genomic infor-
mation from closely related species5,6. For example,
van Bers et al.7 obtained over 16 million short sequence
reads and conducted de novo assembly of 550,000 contigs
covering 2.5% of the genome to discover 20,000 novel
SNPs in the great tit (Parus major). These markers will
be used for quantitative trait locus mapping and whole
genome association studies.
In addition, multiple taxa can be combined in a sin-
gle sequencing analysis using genomic techniques that
can assay large amounts of variable DNA sequence8.
The application of metagenomics to conservation is still
in its early stages, but shows promise. First, functional
metagenomics of microbial communities provides a
novel perspective on ecosystem processes, such as
nutrient and energy flux. Although some studies have
compared functions across a broad scale of biomes9,
similar comparative approaches may identify aspects
of ecosystem function across sites within a habitat.
The second potential application of metagenomics to
conservation is in assessment of physiological con-
dition of individual organisms. For instance, Vega
Thurber et al.10 have found numerous shifts in the
endosymbiont community of corals in response to
multiple stressors, such as reduced pH, increased
nutrients and increased temperature. Third, a metage-
nomic analysis of human faecal samples catalogued
3.3 million microbial genomes and found substantial
differences in the microbial metagenome between
healthy individuals and those with inflammatory
bowel disease11. It may be possible in the future to
apply metagenomic techniques to faecal samples from
wildlife species to assess physiological states, such as
Genomics already has provided some interesting
surprises, such as the discovery of adaptive loci that
show extremely high genetic divergence between popu-
lations of marine fish for which there is virtually no
allele frequency divergence at neutral loci12 (BOX 2). In
addition, a multi-faceted genomic approach has pro-
vided important insights into the treatment of a facial
tumour disease that threatens the persistence of the
Tasmanian devil (Sarcophilus laniarius)13.
*Division of Biological
Sciences, University of
Montana 59812, USA.
‡School of Biological Sciences,
Victoria University of
§Center for Ecology and
University of Oregon, Eugene,
Oregon 97403, USA.
||Department of Zoology,
Oregon State University,
Corvallis, Oregon 97331, USA.
¶Flathead Lake Biological
Station, Division of Biological
Sciences, University of
Montana, Polson, Montana
#Centro de Investigação em
Biodiversidade e Recursos
Genéticos, Universidade do
Porto, 4485-661 Vairão,
A locus that has no effect
on adaptation because
all genotypes have the
Genomics and the future of
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.
NATURE REVIEWS | GENETICS
VOLUME 11 | OCTOBER 2010 | 697
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’).
An abbreviation for contiguous
sequence; used to indicate a
contiguous piece of DNA that
is assembled from shorter
overlapping sequence reads.
The study of the collective
genomic material contained in
an environmental sample of
microorganisms, facilitated by
technology that allows the
direct sequencing of
An organism that lives within
the cells of a host organism.
The loss of vigour and fitness
that is observed when
is increased by inbreeding.
There have been several excellent reviews on con-
servation genomics recently3,14–17. We have attempted to
build on these reviews and to distinguish ours by mak-
ing specific practical recommendations on how genomic
approaches can be applied to key problems in conserva-
tion (TABLE 1). For example, Ouborg et al.15 present a com-
prehensive view of how genomics will provide insights
into the mechanisms behind the interaction between
selectively important variation and environmental
conditions. Nevertheless, if we are to apply this under-
standing of fitness to conservation, we need to address
the population-level consequences of genetic variation,
which include population subdivision, demography and
population viability. We have incorporated population
structure and demographic effects into FIG. 1, and have
distinguished issues that only genomic approaches can
thoroughly address from issues that can be adequately
tackled with traditional techniques.
We have two primary objectives. The first is to iden-
tify those problems in conservation biology in which
genomics will be most valuable in providing new insights
and understanding. The second is to provide guidelines
as to which new genomics approaches will be most
appropriate for the different problems in conservation
that can benefit from genetic analysis.
We begin by focusing on issues in conservation
genomics that are immediately accessible (for example,
increasing the number of neutral markers) and then
proceed through issues that will become more feasible
in the future. We consider how genomic approaches will
allow us to understand the genetic basis of inbreeding
depression and adaptation. We then apply these insights
to important outstanding problems in conservation,
including understanding the effects of hybridization and
predicting outbreeding depression, as well as predicting
evolutionary responses to climate change.
The most straightforward contribution of genomics to
conservation will be to enormously increase the pre-
cision and accuracy of estimation of parameters that
require neutral loci (for example, effective population size
(Ne) and migration rate (m)) by genotyping hundreds
to thousands of neutral loci in numerous individuals.
The accuracy of parameter estimation will be improved
because examining several loci facilitates the identifica-
tion and exclusion of loci under selection (outlier loci)
that cause biased estimates of parameters. For example, a
small proportion (1–5%) of non-neutral loci can change
estimates of mean FST by 30–50%18–20, and change the
topology and branch lengths of evolutionary trees21,22.
Similarly, the assessment of demographic parameters,
such as population bottlenecks or growth rates, requires
many loci to identify outliers and reliably infer change
in population size. Selection can shrink (by bottlenecks)
or expand genealogies at a locus23. Therefore, inferences
about population growth should be more robust if out-
lier loci are removed, for example by using a hierarchical
Bayesian model to assess the parameters of each locus
Increasing the number of markers will also facilitate
estimation of directionality of migration (emigration
and immigration rates), especially if haplotypes can be
inferred from linked loci25. Certain questions require
linked loci or can be vastly improved by using haplotype
inference; for example, estimating relationships among
individuals26, population structure27, admixture28, dates of
historical bottlenecks and directionality of migration25.
Furthermore, it will become increasingly feasible to
jointly estimate multiple parameters, which generally
requires more loci than single parameter estimation. For
example, likelihood, Bayesian and approximate Bayesian
estimators combined with coalescent approaches will
allow the simultaneous estimation of multiple param-
eters, such as Ne and m25,29, or Ne and the selection
coefficient (s)30. This is important because it will improve
parameter estimation, allow parameter estimation in
metapopulations (not just in isolated populations with
no gene flow), and facilitate investigations of the relative
importance and interactions among drift, selection and
migration in populations of conservation concern.
By contrast, simulations suggest that as the number
of loci increases, the accuracy of parameter estima-
tion can decrease owing to non-independence or link-
age among loci31. Failure to account for linkage could
limit the utility of SNPs or multi-locus sequencing in
studies using genealogical information32. Markers are
usually assumed to be independent. Failure to account
for non-independence can lead to overestimation of
Box 1 | What is ‘conservation genomics’?
Conservation genomics can be broadly defined as the use of new genomic techniques
to solve problems in conservation biology. Frankham72 recently reviewed the current
status of conservation genetics and proposed 13 priorities for development in the field.
Many of these priorities have been intractable through traditional genetic techniques.
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
over the next few years.
Genomic techniques will be more immediately applicable to some questions than to
others (TABLE 1). For example, in estimating neutral population parameters, such as
effective population size, genomics simply provides a larger number of markers to an
analytical and conceptual framework that is already widely used in conservation
genetics. Genomic identification of functionally important genes is now common in
other fields; conservation genomics can incorporate these approaches to study the
genetic basis of local adaptation or inbreeding depression. By contrast, predicting a
population’s viability or capacity to adapt to climate change based on genomic
information will require not only the identification of relevant loci, but also a
quantitative estimate of their connection to fitness and demographic vital rates.
These challenges must be tackled by conservation genomics over the longer term.
Understanding genomic approaches is crucial to the success of applying genomics
to conservation (FIG. 1). A growing list of techniques is available for detecting DNA
sequence differences across individuals in natural populations, and these vary widely in
the density of markers across the genome, their ability to target candidate loci, the cost
per sample, and so on. Genomic techniques can be roughly grouped into three classes:
marker-based genotyping, including a diversity of array-based SNP genotyping
platforms; reduced-representation sequencing, which uses next-generation
sequencing technology to target a subset of orthologous regions across the genome of
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
as (and in response to) techniques for gathering the data, and we do not review the
software and analytical issues here111. Nonetheless, researchers using genomic
techniques should plan on a substantial investment of time and resources devoted to
data storage and analysis.
698 | OCTOBER 2010 | VOLUME 11
118. Richards, C. L. et al. Plasticity in salt tolerance traits
allows for invasion of novel habitat by Japanese
knotweed s. l. (Fallopia japonica and F. bohemica,
Polygonaceae). Am. J. Bot. 95, 931–942 (2008).
119. Allendorf, F. W. & Lundquist, L. L. Introduction:
population biology, evolution, and control of invasive
species. Conserv. Biol. 17, 24–30 (2003).
120. Coulson, T. et al. Estimating individual contributions
to population growth: evolutionary fitness in ecological
time. Proc. Biol. Sci. 273, 547–555 (2006).
121. Palsbøll, P. J., Berube, M. & Allendorf, F. W.
Identification of management units using population
genetic data. Trends Ecol. Evol. 22, 11–16 (2007).
122. Waples, R. S. Separating the wheat from the chaff:
patterns of genetic differentiation in high gene flow
species. J. Hered. 89, 438–450 (1998).
An important paper that considers how to interpret
the low genetic differentiation observed between
marine populations that are apparently
123. Pampoulie, C. et al. The genetic structure of Atlantic
cod (Gadus morhua) around Iceland: insight from
microsatellites, the PanI locus, and tagging
experiments. Can. J. Fish. Aquat. Sci. 63, 2660–2674
124. Hemmer-Hansen, J., Nielsen, E. E., Frydenberg, J. &
Loeschcke, V. Adaptive divergence in a high gene flow
environment: Hsc70 variation in the European
flounder (Platichthys flesus L.). Heredity 99,
125. Lowe, W. H. & Allendorf, F. W. What can genetics tell
us about population connectivity? Mol. Ecol. 19,
126. Waples, R. S. & Gaggiotti, O. What is a population?
An empirical evaluation of some genetic methods
for identifying the number of gene pools and their
degree of connectivity. Mol. Ecol. 15, 1419–1439
An extremely valuable paper that considers the
fundamental problem of defining ‘population’ in
127. Baird, N. A. et al. Rapid SNP discovery and genetic
mapping using sequenced RAD markers. PLoS ONE 3,
128. Perkel, J. SNP genotyping: six technologies that keyed
a revolution. Nature Methods 5, 447–453 (2008).
129. Decker, J. E. et al. Resolving the evolution of extant
and extinct ruminants with high-throughput
phylogenomics. Proc. Natl Acad. Sci. USA 106,
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.
Competing interests statement
The authors declare no competing financial interests.
Fred W. Allendorf’s homepage: http://www.cas.umt.edu/
See online article: S1 (figure)
ALL LINKS ARE ACTIVE IN THE ONLINE PDF
NATURE REVIEWS | GENETICS
VOLUME 11 | OCTOBER 2010 | 709
000 Genomics and the future of conservation
Fred W. Allendorf, Paul A. Hohenlohe and Gordon
This article discusses how genomic techniques are
expected to provide new insights into important
problems in conservation and to allow questions to
be addressed that have previously not been tractable.
The authors also offer advice on choosing the most
appropriate genomic approaches for studying
different aspects of conservation.
??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 signifi-
cance 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 genom-
ics approaches will be most appropriate for the different problems
in conservation that can benefit from genetic analysis.
??The most straightforward contribution of genomics to conserva-
tion 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 habi-
tats. 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 manage-
ment 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 differ-
ential introgression rates of genomic regions raise some difficult
issues with regards to treating hybridized populations in conserva-
tion 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 iden-
tifying specific loci of importance, which are essential for selecting
select founder individuals.
??There is increasing evidence that epigenetic processes can be impor-
tant 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, under-
standing the relationship between genetic variation and fitness
itself will not be sufficient to improve our estimates of population
viability. Understanding the connections between individual fit-
ness and population growth rates is perhaps the most important
and difficult future challenge facing conservation genetics.
Fred W. Allendorf received his Ph.D. from the University of
Washington, Seattle, USA, and was a postdoctoral fellow at Aarhus
University, Denmark, and the University of Nottingham, UK. He has
been at the University of Montana, Missoula, USA, since 1976 and cur-
rently has a partial appointment at Victoria University of Wellington,
New Zealand. He recently has held fellowships at the University of
Western Australia in Perth and Australia’s Commonwealth Scientific
and Industrial Research Organisation (CSIRO) in Hobart. His pri-
mary research focus is the application of population genetics to
Paul A. Hohenlohe received his Ph.D. from the University of
Washington and worked as a conservation biologist for the US Bureau
of Land Management and Forest Service under the Northwest Forest
Plan. He is currently a research associate at the University of Oregon,
Eugene, USA, and Oregon State University, Corvallis, USA. His
research is focused on population genomics approaches to questions
in conservation and evolution.
Gordon Luikart received his Ph.D. at the University of Montana,
was a Fulbright fellow at LaTrobe University, Victoria, Australia, a
research scientist at the Centre National de la Recherche Scientifique
(CNRS), Grenoble, France, and a research scientist at the Centro
de Investigação em Biodiversidade e Recursos Genéticos (CIBIO),
Vairão, Portugal. He is a research associate professor at the Flathead
Lake Biological Station, University of Montana. His research is aimed
at developing molecular and computational approaches to bridge the
gaps between theory, basic science and practical applications in con-
servation biology and evolutionary ecology.