Jeff Johnson|R. Altwegg|Darren M. Evans|John G. Ewen|Iain J. Gordon|Nathalie Pettorelli|Julie K. Young
Is there a future for genome-editing technologies in conservation?
University of North Texas|University of Cape Town|Newcastle University|Zoological Society of London|James Cook University|Zoological Society of London|Utah State University
animal conservationvolume 19 issue 2 p 97101 editorialfree access future genomeediting technologies conservation j johnson corresponding author j johnson department biological sciences institute applied sciences university north texas denton tx usa correspondence jeff johnson department biological sciences institute applied sciences university north texas 1155 union circle 310559 denton tx 76203 usa email jajohnsonuntedusearch papers authorr altwegg r altwegg statistics ecology environment conservation department statistical sciences african climate development initiative university cape town cape town south africasearch papers authord evans evans school biology newcastle university newcastle upon tyne uksearch papers authorj g ewen j g ewen institute zoology zoological society london london uksearch papers authori j gordon j gordon division tropical environments societies james cook university townsville australiasearch papers authorn pettorelli n pettorelli institute zoology zoological society london london uksearch papers authorj k young j k young usdanwrcpredator research facility department wildland resources utah state university logan ut usasearch papers author j johnson corresponding author j johnson department biological sciences institute applied sciences university north texas denton tx usa correspondence jeff johnson department biological sciences institute applied sciences university north texas 1155 union circle 310559 denton tx 76203 usa email jajohnsonuntedusearch papers authorr altwegg r altwegg statistics ecology environment conservation department statistical sciences african climate development initiative university cape town cape town south africasearch papers authord evans evans school biology newcastle university newcastle upon tyne uksearch papers authorj g ewen j g ewen institute zoology zoological society london london uksearch papers authori j gordon j gordon division tropical environments societies james cook university townsville australiasearch papers authorn pettorelli n pettorelli institute zoology zoological society london london uksearch papers authorj k young j k young usdanwrcpredator research facility department wildland resources utah state university logan ut usasearch papers author first published 17 april 2016 httpsdoiorg101111acv12273citations 40aboutsectionspdf toolsrequest permissionexport citationadd favoritestrack citation shareshare give accessshare full text accessshare fulltext accessplease review terms conditions use check box share fulltext version articlei read accept wiley online library terms conditions useshareable linkuse link share fulltext version article friends colleagues learn morecopy url share linkshare onfacebooktwitterlinkedinredditwechat recent review pimm et al 2015 highlight emerging technologies protecting biodiversity list noteworthy authors exclusion innovations genomic research exception singlespecies dna barcoding methods surprising given recent advances genomeediting technology potential application conservation taylor gemmell 2016 address deficiency subsequent commentary identifying three avenues emerging genomic technologies great potential increasing ability conserve biodiversity areas include use nextgeneration sequencing technologies methods radseq monitoring genetic diversity effective population size introgression andrews et al 2016 use environmental dna edna metabarcoding approaches map species occurrence interaction networks evans et al 2016 use genomic data geneediting technology identify alter regions genome may impact fitness limit survival endangered taxa taylor gemmell 2016 extend theme additional discussion genomeediting technologies benefit conservation threatened endangered species genomeediting technologies referenced herein include methods insert delete replace dna within organisms genome one particular editing technique called crisprcas9 jinek et al 2012 gained considerable momentum past three years achieving sciences 2015 breakthrough year travis 2015 largely due simplicity relative low cost precise genomicediting capabilities mei et al 2016 crisprcas9 technique developed adaptive immune response bacteria archaea invading viruses plasmids jinek et al 2012 see also lander 2016 essentially rnaguided molecule programmed identify specific location within genome subsequently cut replace target dna ie rnaguided endonuclease see mei et al 2016 wright nuez doudna 2016 specific details crisprcas9 technology already shown great potential benefit humans variety ways including improving crops kim et al 2015 eliminating disease mclean jacobslorena 2016 targeted medical therapies savi schwank 2016 reason technology could used tool support biodiversity conservation acknowledge much needs done increase awareness within conservation community genomeediting technology benefit conservation practice easy task largely widely held negative perception genetically modified gm organisms used agriculture particularly forprofit commercial industry au 2015 see also redford et al 2014 however use gm pharmaceuticals human medicine received less negative attention locwin 2015 conservation community learn dichotomy identify tactful approaches advocacy conservation genomeediting technology benefit conservation first people agree prevention mitigation nonnative invasive organisms increasingly difficult costly due expanding global trade travel banks et al 2015 ability combat invasive species effectively relevant conserving biodiversity nonnative species significant contributor recent vertebrate extinctions bellard cassey blackburn 2016 genomicengineering technologies specifically utilize crisprcas9 gene drive methodologies alter reproductive capacity esvelt et al 2014 champer buchman akbari 2016 become valuable tool help prevent eliminate invasive species proper precautions place oye et al 2014 akbari et al 2015 webber raghu edwards 2015 champer et al 2016 example invasive rodents impacted endemic fauna flora many remote island ecosystems harper bunbury 2015 jones et al 2016 research currently underway develop genetic biocontrol methodologies reduce impact promising approach includes using genomicediting techniques alter sex determination pathway invasive species targeting sry gene larney bailey koopman 2014 using xchromosome shredder approach xshredder champer et al 2016 producing allmale offspring would effectively eliminate reproduction without need pesticides poisons negatively impact nontarget species eg pitt et al 2015 see also campbell et al 2015 applications strong potential resulting positive outcomes using best practices framework already established long history biological control applications addressing biosecurity concerns prerelease assessment nontarget effects focused attention preventing spread geneedited organism unintended areas see webber et al 2015 additional options allowed applying genetic biocontrol approach include incorporating killswitch modified organism would permit intentional elimination environment prevent undesired horizontal gene transfer wild populations eg mandell et al 2015 yet research required address feasibility associated risks nature redford et al 2014 schmidt de lorenzo 2016 second recent genomic research domestic wild canids highlights severe bottleneck events increase frequency deleterious genetic variants remaining population marsden et al 2016 results important implications management species experienced significant decline abundance bottlenecked populations may experience increase disease susceptibility pathogens hale briskie 2007 tompkins 2007 increased frequency genetic disorders negatively impact survival within remaining population eg rikknen et al 2009 founding population california condor gymnogyps californianus captive breeding program example based 14 individuals among three genetic groups assumed include halfsiblings ralls ballou 2004 genetic disorder called chondrodystrophy increased frequency within founding population restricting breeding pairs avoid producing offspring condition ralls et al 2000 romanov et al 2009 despite pessimistic outlook presented shafer et al 2015 geneediting technology could used alter remove genetic disorder also particular diseasecausing pathogen completely population similar methods proposed human clinical applications eg white hu khalili 2015 tabebordbar et al 2016 although ambitious crispr technologies also used supplement genomic diversity bottlenecked populations increase pathogen resistance eg savage zamudio 2011 adaptive potential changing environment facilitated adaptation thomas et al 2013 harrisson et al 2014 preservation cryptic genetic diversity increasingly recognized important feature allowing populations adapt faster environmental change hayden ferrada wagner 2011 paaby rockman 2014 similar recent success using cryopreserved semen supplementing genomic diversity blackfooted ferret mustela nigripes population howard et al 2016 crispr technology could used purpose targeting genomic regions reduced diversity identified wholegenome sequences obtained preserved tissues extinct lineages eg hofman et al 2015 holmes et al 2016 crispr technologies also proposed resurrect extinct species eg shapiro 2015 recent methods capable altering genome extent required produce living individual extinct species research currently underway using crisprcas9 modify phenotypically relevant genes extant species reflect existed closely related extinct species trait resurrection example researchers identified successfully altered genes wooly mammoth mammuthus primigenius closest living relative asian elephant elephas maximus associated adaptations cold environment lynch et al 2015 see also shapiro 2015 crispr technologies could used modify specific genes within critically endangered elephant species thereby decreasing habitat restrictions necessary likely technology impact conservation science practice international union conservation nature iucn species survival commission established deextinction task force drafting set guiding principles deextinction conservation benefit p seddon pers comm would remiss acknowledge however targeting genes genomic regions editing may always sufficient phenotypic change least way intended conservation increasing number studies shown genetic architecture many fitnessrelated traits largely control many genes small effect polygenic including influence genetic epistatic interactions functional intergenic regions harrisson et al 2014 taylor ehrenreich 2015 therefore significant challenges exist altering phenotype using genomicediting techniques yet new genomic technologies crisprcas9 great promise also making much easier link genotypes phenotypes fitness nonmodel species bono olesnicky matzkin 2015 notable advances using crispr technologies human health commercial agriculture occurred quickly past years wellestablished foundation already existed linking many genomic variants observed phenotypic traits eg ainsworth 2015 harper nayee topol 2015 tabebordbar et al 2016 wholegenome sequencing technologies become accessible allowing generation genomic datasets multiple individuals species conservation concern ability decipher genomic architecture complex traits important species persistence undoubtedly improve see also bono et al 2015 research focused topic certainly warranted necessary advancing genomicediting tool conservation management furthermore significant concerns exist genomeediting technologies crisprcas9 may also cause harm individual population community due uncertainties altering genome processes potential subsequent nontarget effects eg lander 2015 webber et al 2015 concerns arise fact much remains learned information encoded genome transcribed function agree much left learned eg harrisson et al 2014 think possibilities offered technique ignored certainly crisis discipline conservation fact support already exists use crispr technology human somatic cellbased gene therapies eg national academy sciences 2015 british regulatory agency oversees reproductive biology recently allowed research proceed using crisprcas9 alter human embryos ie germline manipulation developmental biology research siddique 2016 undoubtedly practical ethical legal considerations need addressed genomicediting technologies integrated active conservation practice researchers practitioners policy makers must work together identify best approaches utilizing technology also acknowledging great care must taken avoid irreversible harm rapid adoption crisprcas9 similar genomicediting technologies addressing human healthrelated issues unprecedented reflected growing number applications described scientific literature popular press past 2 years similar level enthusiasm needed explore develop implement technology biodiversity conservation disclaimer information presented editorial authors necessarily represent views respective affiliations references ainsworth c 2015 agriculture new breed edits 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