Meetings

Genetics and genomics in wildlifestudies: Implications for ecology,evolution, and conservation biology

Introduction

The meeting ‘‘Genetics and Genomicsin Wildlife Studies: Implications forEcology, Evolution, and ConservationBiology’’ was held in Seville, Spain,on October 20–21, 2011. The event high-lighted the potential applications ofcutting-edge genomic approaches forecological, evolutionary, and conserva-tion genetics research. The current rev-olution in next generation sequencing(NGS) technologies is destined to add agenomic dimension to biological diver-sity studies. Twelve leading researcherswere invited to give talks on the appli-cation of genomic tools to address evol-utionary, ecological, and conservationquestions. Talks covered work currentlybeing done using genomic approaches,either in species with a referencegenome or in non-model organisms,to tackle a wide array of evolutionaryquestions. The event raised interestingnovel insights into the applicability ofgenomics to conserve biodiversity.

Comparative genomics

The increasing number of species withavailable genomes has enabled compara-tive studies of genome structure, func-tion, and evolution. Indeed, WarrenJohnson (Center for Cancer Research,Bethesda, USA) announced that 200new genome assemblies are about tobe released, as part of the Genome 10KProject to sequence 10,000 vertebrate

genomes. As an example of comparativeapproaches, Matthew Webster (UppsalaUniversity, Sweden) presented his workon the Prdm9 gene, known to play a keyrole in mammalian recombination. Hefound that this gene is not functionalin the canid lineage. Scott Edwards(Harvard University, USA) has combinedvery different sources of information aspart of his comparative genomics inves-tigations of mammals, reptiles, and birds.His phylogenomic analyses of reptiles’bacterial artificial chromosomes (BACs)demonstrated a reduction of genome sizefrom the common ancestor of amniotesthrough reptiles, culminating in tiny birdgenomes. Additional analyses of osteo-cytes in dinosaur fossils, a proxy forgenome size, showed an associationbetween small genomes and flight.

The NGS revolution allows new inte-grative approaches combining compara-tive and population genomics. RasmusNielsen (University of Copenhagen,Denmark) emphasized how a single dip-loid genome can inform about ancientdemographic events and assign popu-lation ancestry using appropriateanalyses. Comparing the genome ofone ancient human with single nucleo-tide polymorphisms (SNPs) in modernhumans, he inferred that the Saqqaq, anextinct culture from Greenland, wasrelated to North Eastern Siberian popu-lations. Similarly, Mattias Jakobsson(Uppsala University) spoke about popu-lation genomics and human evolution-ary history. He used a combination ofsimulations and principal componentanalyses (PCA) projecting extant humanvariation onto PC axes defined byDenisovan (a hominid from Siberia),Neanderthal, and chimpanzee genomes.

He found that contemporary East Asianpopulations exhibited close geneticaffinity with the Denisovan genome.Jakobsson also noted that the analysisof copy number variation (CNV) in thehuman genome is as important as SNPvariation analyses. Tomas Marques-Bonet (Evolutionary Biology InstituteUPF-CSIC, Barcelona, Spain) focusedon ape comparative genomics andmapped CNVs and segmental dupli-cations. Marques-Bonet has sequenced91 primate genomes and is using thehuman genome as a reference forreliable identification of CNVs. He alsoexplained the efficiency of their proto-cols for detecting homozygous blocks inthe genome of captive animals. Forexample, the study of ‘‘Snowflake’’, analbino captive gorilla, revealed a similarmutation to the one responsible foralbinism in humans.

Adaptation genomics

The NGS explosion has promoted theuse of genomics to study adaptationand selection in far more detail thanpreviously possible, which has potentialimplications for conservation. Indeed,genome-wide selection scans often ana-lyze the allele frequency spectrum toidentify positive selection. Nielsenclearly explained how selective sweepsproduce an excess of high frequencyalleles in positively selected genes. Forexample, comparing whole exomes of50 Tibetans and 40 Han Chinesesamples, he detected a strong signalof selection on EPAS1, a gene possiblyassociated with high altitude adapta-tion in Tibetans. Additionally, regions

DOI 10.1002/bies.201100171

Bioessays 34: 245–246,� 2011 WILEY Periodicals, Inc. www.bioessays-journal.com 245

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affected by a selective sweep typicallyshow high levels of linkage disequili-brium (LD). Comparison of 40 light-coverage genomes of silkworm allowedNielsen to identify a region of high LDsurrounding the silk gland factor-1(SGF-1).

Other genome scans frequently lookfor regions showing strong geneticdifferentiation. For example, Webstergenotyped more than 170,000 SNPs in46 dog breeds. High FST values betweencertain breeds indicated selectivesweeps in particular genomic regionsthat could be associated with distinctivephenotypic traits. Similarly, WilliamCresko (University of Oregon, USA) usedgenotyping of high throughput restric-tion-site-associated DNA (RAD) tags toinvestigate genomic patterns of adap-tation associated with transition fromoceanic to freshwater environments insticklebacks. His data showed howselection repeatedly targeted similargenomic regions associated with pheno-typic adaptations to these aquaticenvironments showing how genomesmight be shaped by ecological factors.

As an alternative to genome-widescans, a focus on a more restricted setof candidate genes is still useful andalso facilitated by NGS technologies.Robert Wayne (University ofCalifornia, Los Angeles, USA) identifieda gene responsible for black color indogs that introgressed into NorthAmerican wolves only a few thousandyears ago. Follow-up studies showedhow the black coat color polymorphismis maintained in wolves through trade-offs between lower fecundity and highersurvival, possibly due to enhancedimmunity. Victoria Sork (University ofCalifornia) used a landscape genomicsapproach combining ecological,genetic, and spatial information to bet-ter understand how gene flow and selec-tion shape diversity in Californiansavanna oaks. She genotyped 194SNPs in 50 genes likely related toenvironmental response. She found sig-nals of climate adaptation by means ofmultivariate analyses corrected forspatial genetic structure. Following thistrend, Craig Primmer (University ofTurku, Finland) developed and ana-lyzed 16 microsatellites linked toimmune related genes in Atlantic sal-mon populations and found a negativerelationship between genetic diversity

and latitude. This is consistent withincreasing pathogen-driven selectionunder higher temperatures. In the con-text of a global-warming scenario, theresponse of natural variation to climaticconditions is of conservation concern.

Although we can now identify somegenes involved in the adaptation to aspecific environment, natural selectionacts on phenotypes. A first step towardlinking genotype and phenotype couldinvolve a proteomic or transcriptomicapproach that does not require a refer-ence genome. For example, RobertEkblom (Uppsala University) used tran-scriptomic characterization to comparemale mating behavior with associatedplumage polymorphisms in the ruff, alekking bird. Additionally, he geno-typed SNPs identified from transcrip-tome sequences to search for geneticdivergence due to mating strategies.Gene expression studies in differentdomestic chicken breeds (egg-layersand gamecocks) allowed Judith Mank(Oxford University, UK) to better under-stand the evolution of genes controllingsexual dimorphism. Her results showedthat genes influencing sexual dimor-phism are located on both sex chromo-somes and autosomes. She also foundhow sex-biased gene expression andselection changed during developmentassociated with periods of peak sex-hor-mone production.

Implications

The meeting ended discussing the statusand upcoming needs of conservationgenomics. A range of important needswere identified including: cost-effectivegenotyping methods at a populationlevel, sequencing methods for lowquantity or poor quality DNA, and theassembly of duplicated genomes (e.g.amphibian, fish, and plant species).

Data storage is becoming a demand-ing issue. The burst of whole genomedata requires improvements in our stor-age strategies, such as format standard-ization and data exchange capacitiesthrough public virtual museums or com-mercial cloud computing platforms.Collaborative projects, such as theGenome 10K, are required to maximallyrepresent phylogenetic diversity withthe added benefit of genome-enablingclosely related species. It is also necess-

ary to enhance sequencing effortsincluding other large groups such asarthropods, fungi, and plants. Thisinformation would be invaluable forstudying the evolution and conservationof extant biodiversity.

There is a continuing need for theor-etical, statistical, and bioinformaticdevelopments because of the hugeamount of NGS information becomingavailable. For example, genome-wideassociation studies (GWAS) have hadmixed success in accounting for the totalheritability of traits or identifying genesof relatively small phenotypic effect.Future studies require new ways to com-bine information about genealogies,interactomics, gene regulation, andclear-cut phenotype characterization.

NGS is dramatically increasing ouranalytical power and accuracy.However, discussion at the end of themeeting cautioned against overuse ofNGS if the same questions could beanswered with less genetic data. Weshould carefully consider our researchpriorities and justification for a genomicapproach when resources dedicated toconservation are limited. Genomics willdefinitely increase our understanding ofadaptation and fitness components in aconservation context, but this mightsometimes be overshadowed by thepriority of preserving processes andhabitats in the immediate short termfor highly threatened species.

AcknowledgmentsWe thank fellow meeting organizers: GiuliaCrema, Jose A. Godoy, Jennifer A. Leonard,and Carles Vila. We are grateful to allinvited speakers for their thought-provokingcontributions. We also thank Foro de laBiodiversidad and EBD-CSIC staff for assist-ance. This meeting was financially supportedby the EcoGenes project (Ref.: 264125) of theEU FP7-REGPOT-2010-1 program.

Fernando Cruz�

Adrian C. Brennany

Alejandro Gonzalez-Voyery

Violeta Munoz-Fuentesy

Muthukrishnan Eaaswarkhanthy

Severine Roquesy

F. Xavier Pico

Estacion Biologica de Donana(EBD-CSIC), Seville, Spain�E-mail: fernando.cruz@ebd.csic.es

yThese authors contributed equally to thiswork.

246 Bioessays 34: 245–246,� 2011 WILEY Periodicals, Inc.

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