HYPOTHESIS AND THEORY
published: 21 Oc obe 2015
doi: 10.3389/ gene.2015.00314
F on ie s in Gene ics | www. on ie sin.o g 1Oc obe 2015 | Volume 6 | A icle 314
Edi ed by:
Pe e Do c,
Uni e si y o Ljubljana, Slo enia
Re iewed by:
Juan S eibel,
Michigan S a e Uni e si y, USA
John B. Cole,
Uni ed S a es Depa men o
Ag icul u e, USA
*Co espondence:
Michael W. B u o d
[email p o ec ed]
Special y sec ion:
This a icle was submi ed o
Li es ock Genomics,
a sec ion o he jou nal
F on ie s in Gene ics
Recei ed: 26 May 2015
Accep ed: 05 Oc obe 2015
Published: 21 Oc obe 2015
P ospec s and challenges o he
conse a ion o a m animal genomic
esou ces, 2015-2025
Michael W. B u o d1, 2*, Ca a ina Ginja3, 4, I ene Ho mann5, S éphane Joos 6,
Pablo O ozco- e Wengel1, Flo ian J. Albe o7, And eia J. Ama al8, Ma io Ba ba o1,
Filippo Bisca ini9, Licia Colli10, Ma alda Cos a1, Ino Cu ik11, Solange Du uz6,
Maja Fe enˇ
cako i´
c11, Daniel Fische 12, Robe Fi ak13, Linn F. G oene eld14,
S ephen J. G. Hall15, Oli ie Hano e16, Faiz-ul Hassan16, 17, Philippe Helsen18,
Lau a Iacolina19, Juha Kan anen12, 20, Ke in Leempoel6, Johannes A. Lens a21,
Paolo Ajmone-Ma san10, Cha les Masembe22, Hend ik-Jan Megens23, Ma a Miele24,
Ma kus Neudi schko25, Ezequiel L. Nicolazzi9, F ançois Pompanon7, Ju a Roosen26,
Na alia Se ane27, Anama ija Sme ko28, Anama ia Š ambuk29, Ian S ee e 30,
Syl ie S ucki6, China Supako n16, 31, Luis Telo Da Gama32, Michèle Tixie -Boicha d33,
Daniel Wegmann34 and Xiangjiang Zhan35, 36
1School o Biosciences, Ca di Uni e si y, Ca di , UK, 2Sus ainable Places Resea ch Ins i u e, Ca di Uni e si y, Ca di , UK,
3Faculdade de Ciências, Cen o de Ecologia, E olução e Al e ações Ambien ais (CE3C), Uni e sidade de Lisboa, Lisboa,
Po ugal, 4Cen o de In es igação em Biodi e sidade e Recu sos Gené icos (CIBIO-InBIO), Uni e sidade do Po o, Campus
Ag á io de Vai ão, Po ugal, 5Food and Ag icul u e O ganiza ion o he Uni ed Na ions, Animal Gene ic Resou ces B anch,
Animal P oduc ion and Heal h Di ision, Rome, I aly, 6Labo a o y o Geog aphic In o ma ion Sys ems (LASIG), School o Ci il
and En i onmen al Enginee ing (ENAC), Ecole Poly echnique Fédé ale de Lausanne, Lausanne, Swi ze land, 7Labo a oi e
d’Ecologie Alpine, Uni e si é G enoble Alpes, G enoble, F ance, 8Facul y o Sciences, BioISI- Biosys ems and In eg a i e
Sciences Ins i u e, Uni e si y o Lisbon, Campo G ande, Po ugal, 9Pa co Tecnologico Padano, Lodi, I aly, 10 BioDNA Cen o
di Rice ca sulla Biodi e si à a sul DNA An ico, Is i u o di Zoo ecnica, Uni e si à Ca olica del Sac o Cuo e di Piacenza, I aly,
11 Facul y o Ag icul u e, Uni e si y o Zag eb, Zag eb, C oa ia, 12 Na u al Resou ces Ins i u e Finland (Luke), G een
Technology, Jokioinen, Finland, 13 Ins i u ü Popula ionsgene ik, Ve meduni, Vienna, Aus ia, 14 No dGen -The No dic Gene ic
Resou ce Cen e , Ås, No way, 15 Li es ock Di e si y L d., Lincoln, UK, 16 School o Li e Sciences, Uni e si y o No ingham,
No ingham, UK, 17 Depa men o Animal B eeding and Gene ics, Uni e si y o Ag icul u e, Faisalabad, Pakis an, 18 Cen e o
Resea ch and Conse a ion, Royal Zoological Socie y o An we p, An we p, Belgium, 19 Depa men o Chemis y and
Bioscience, Aalbo g Uni e si y, Aalbo g, Denma k, 20 Depa men o Biology, Uni e si y o Eas e n Finland, Kuopio, Finland,
21 Facul y o Ve e ina y Medicine, U ech Uni e si y, U ech , Ne he land, 22 Ins i u e o he En i onmen and Na u al
Resou ces, Make e e Uni e si y, Kampala, Uganda, 23 Animal B eeding and Genomics Cen e, Wageningen Uni e si y,
Wageningen, Ne he lands, 24 School o Planning and Geog aphy, Ca di Uni e si y, Ca di , UK, 25 Ag oscope, Swiss Na ional
S ud Fa m, A enches, Swi ze land, 26 TUM School o Managemen , Technische Uni e si ä München, Munich, Ge many,
27 Depa men o Animal P oduc ion, Ve e ina y Facul y, Uni e sidad Complu ense de Mad id, Mad id, Spain, 28 C oa ian
Ag icul u al Agency, Zag eb, C oa ia, 29 Depa men o Biology, Facul y o Science, Uni e si y o Zag eb, Zag eb, C oa ia,
30 Eu opean Molecula Biology Labo a o y, Eu opean Bioin o ma ics Ins i u e, Wellcome T us Genome Campus, Hinx on,
Camb idge, UK, 31 School o Ag icul u al Technology, Walailak Uni e si y, Tha Sala, Thailand, 32 Cen e o Resea ch in Animal
Heal h (CIISA) – Facul y o Ve e ina y Medicine, Uni e si y o Lisbon, Lisbon, Po ugal, 33 INRA, Ag oPa isTech, UMR GABI,
Jouy-en-Josas, F ance, 34 Depa men o Biology, Uni e si y o F ibou g, F ibou g, Swi ze land, 35 Key Labo a o y o Animal
Ecology and Conse a ion Biology, Ins i u e o Zoology, Chinese Academy o Sciences, Beijing, China, 36 Ca di Uni e si y –
Ins i u e o Zoology, Join Labo a o y o Biocomplexi y Resea ch, Beijing, China
Li es ock conse a ion p ac ice is changing apidly in ligh o policy de elopmen s,
clima e change and di e si ying ma ke demands. The las decade has seen a s ep
change in echnology and analy ical app oaches a ailable o de ine, manage and
conse e Fa m Animal Genomic Resou ces (FAnGR). Howe e , hese apid changes
pose challenges o FAnGR conse a ion in e ms o echnological con inui y, analy ical
capaci y and in eg a i e me hodologies needed o ully exploi new, mul idimensional
da a. The inal con e ence o he ESF Genomic Resou ces p og am aimed o add ess
B u o d e al. Challenges in li es ock conse a ion
hese in e disciplina y p oblems in an a emp o con ibu e o he agenda o esea ch
and policy de elopmen di ec ions du ing he coming decade. By 2020, acco ding
o he Con en ion on Biodi e si y’s Aichi Ta ge 13, signa o ies should ensu e ha
“… he gene ic di e si y o … a med and domes ica ed animals and o wild ela i es …is
main ained, and s a egies ha e been de eloped and implemen ed o minimizing gene ic
e osion and sa egua ding hei gene ic di e si y.” Howe e , he eal ex en o gene ic
e osion is e y di icul o measu e using cu en da a. The e o e, his challenging a ge
demands be e co e age, unde s anding and u iliza ion o genomic and en i onmen al
da a, he de elopmen o op imized ways o in eg a e hese da a wi h social and
o he sciences and policy analysis o enable mo e lexible, e idence-based models o
unde pin FAnGR conse a ion. A he con e ence, we a emp ed o iden i y he mos
impo an p oblems o e ec i e li es ock genomic esou ce conse a ion du ing he
nex decade. Twen y p io i y ques ions we e iden i ied ha could be b oadly ca ego ized
in o challenges ela ed o me hodology, analy ical app oaches, da a managemen and
conse a ion. I should be acknowledged he e ha while he ocus o ou mee ing was
p edominan ly a ound gene ics, genomics and animal science, many o he p ac ical
challenges acing conse a ion o genomic esou ces a e socie al in o igin and a e
p edica ed on he alue (e.g., socio-economic and cul u al) o hese esou ces o a me s,
u al communi ies and socie y as a whole. The o e all conclusion is ha despi e he ac
ha he li es ock sec o has been ela i ely well-o ganized in he applica ion o gene ic
me hodologies o da e, he e is s ill a la ge gap be ween he cu en s a e-o - he-a
in he use o ools o cha ac e ize genomic esou ces and i s applica ion o many
non-comme cial and local b eeds, hampe ing he consis en u iliza ion o gene ic and
genomic da a as indica o s o gene ic e osion and di e si y. The li es ock genomic sec o
he e o e needs o make a conce ed e o in he coming decade o enable o he
democ a iza ion o he powe ul ools ha a e now a i s disposal, and o ensu e ha
hey a e applied in he con ex o b eed conse a ion as well as de elopmen .
Keywo ds: a m animal gene ic esou ces, li es ock gene ic esou ces, genomic di e si y, li es ock popula ion
p io i iza ion, e ec i e conse a ion policy
INTRODUCTION
Unde s anding cu en echnical, in as uc u al and policy
challenges and assessing he likely bene i s o o e coming hem
in he u u e is essen ial o any ield o scien i ic endea o and
especially hose wi h clea socie al consequences and po en ial
bene i s. In his con ex , he concep o ho izon scanning has
been de eloped and applied annually in he ield o biodi e si y
conse a ion since 2009 (Su he land and Wood oo , 2009), using
a a ie y o sys ema ic and semi-sys ema ic me hods o mine
ending issues om web engines and social media and by
analyzing ocused ques ionnai es. Simila app oaches ha e also
been aken o iden i y eme ging issues in ag icul u e (P e y e al.,
2010) and ela ed ields such as soil science, ood sys ems and
pollina ion (Dicks e al., 2013; Ing am e al., 2013; Adewopo
e al., 2014). Such exe cises ha e iden i ied a numbe o issues o
ele ance o he conse a ion o FAnGR, such as gene ic con ol
o in asi e species (Su he land e al., 2014) and sus ainable
in ensi ica ion o high yielding ag icul u e (Su he land e al.,
2015). In 2010, P e y e al.’s a icle pinpoin ing he “Top
100 ques ions o impo ance o he u u e o global ag icul u e”
iden i ied gene ic issues in c op imp o emen (e.g., gains in
imp o emen ha could esul om b eeding o s ess ole ance)
bu iden i ied no such p essing agendas o li es ock genomic
esou ces. Since Ca dellino and Boyazoglu (2009) no a emp
has been published o iden i y esea ch p io i ies o FAnGR
conse a ion, despi e gene ic e osion (sensu Aichi Ta ge 13)
con inuing apace (e.g., Be houly-Salaza e al., 2012; FAO,
2015a) and he s ep-change ha has occu ed in molecula
b eed cha ac e iza ion since he ou ine implemen a ion o
li es ock Single Nucleo ide Polymo phism (SNP) a ays. To
ill his gap, a cen al ac i i y o he Final Con e ence o he
Eu opean Science Founda ion’s Genomic Resou ces p og am,
held a Ca di Uni e si y June 17 h–19 h 2014 was o pick ou a
se ies o p essing ques ions ha could o m pa o a esea ch and
policy agenda o FAnGR conse a ion o he nex decade. While
no ollowing he s anda d sys ema ic app oaches adop ed by
con en ional Ho izon Scanning exe cises, all 43 a endees o his
ocused mee ing ook pa in he exe cise, including scien is s and
policy-make s om Sou h and Eas Asia, No h Ame ica, Eu ope
F on ie s in Gene ics | www. on ie sin.o g 2Oc obe 2015 | Volume 6 | A icle 314
B u o d e al. Challenges in li es ock conse a ion
and A ica in ol ed in a ange o disciplines om genomics o
animal b eeding, gene ic esou ce managemen , economic and
social sciences and global ag icul u al policy de elopmen .
METHODS AND RESULTS
Du ing he cou se o he con e ence, a endees we e asked
o con ibu e up o i e ques ions o highes p io i y o
esea ch, in as uc u e and policy de elopmen du ing he
coming decade. Eigh y-six sugges ions we e ecei ed. The issue
iden i ied wi h highes equency (18 imes) was he need o
“nex gene a ion pheno yping” (i.e., high- h oughpu me hods o
collec and summa ize de ailed pheno ypic da a om domes ic
animals). A summa y o he op 20 ques ions is ound in
Table 1, a subse o which a e p esen ed below (some a e
amalgama ed). All esponses we e ca ego ized in o ou majo
g oups, “Me hodological Challenges,” “Analy ical Challenges,”
“Da a Managemen ,” and “Conse a ion Managemen and
P io i iza ion.” Fou wo king g oups we e con ened o co e
hese ca ego ies and hei indings a e p esen ed below.
Me hodological Challenges
Nex Gene a ion Pheno yping
The need o high- esolu ion pheno ypic da a o be collec ed o
in-dep h cha ac e iza ion o FAnGR was iden i ied, especially in
ligh o he apid ad ances ha ha e been made in molecula
b eed cha ac e iza ion. De eloping me hods o pheno ypic
cha ac e iza ion was also iden i ied by Ca dellino and Boyazoglu
(2009) ollowing om FAO ecommenda ions (FAO, 2007a) and
has clea ly emained an unde -explo ed esea ch a ea. Howe e ,
wi h he ichness o molecula da a inc easing d ama ically since
2009, he misma ch be ween molecula and pheno ypic da a
is widening o all excep highly comme cial ansbounda y
b eeds and lines wi h genomic b eeding alues. Inhe en in
high- esolu ion b eed cha ac e iza ion is a need o de ine
key pheno ypic ai s and cha ac e is ics (pa icula ly hose
po en ially in ol ed in local adap a ion) based on guidelines ha
can be used as common measu es o such s udies wi h s ingen
ield p o ocols o hei collec ion. FAO published guidelines
on pheno ypic cha ac e iza ion (FAO, 2012a). In his way mo e
compa able da a can be gene a ed, and b eed cha ac e iza ion
can ha e a mo e unc ional basis, especially wi h he u gen
need o unde s and b eed cha ac e is ics in he ace o clima e
change (Ho mann, 2010). Also an imp o ed desc ip ion o he
speci ic p oduc ion en i onmen and epidemiological his o y
in which popula ions o a b eed a e kep would allow be e
compa ison o pheno ypes and pe o mances (e.g., FAO, 2009).
Since b eed cha ac e iza ion can be a cos ly exe cise, especially
o emo e egions o he wo ld, as many pheno ypic ai s as
possible should be collec ed ollowing well documen ed and
ep oducible p ocedu es, a p ocess ha calls o he need o
s anda dized me hods o measu e/collec da a and ul ima ely o
aining o people on how o do i . Whe e possible, da a should
be made publicly a ailable h ough a eposi o y such as FAO’s
global Domes ic Animal Di e si y In o ma ion Sys em DAD-IS
(h p://dad. ao.o g) o compa a i e pu poses. The es ablishmen
o a wo king g oup o de ine guidelines, p o ocols and ools o
collec ing such da a unde he auspices o he FAO, In e na ional
Socie y o Animal Gene ics o he In e na ional Commi ee o
Animal Reco ding (www.ica .o g) would accele a e his p ocess.
Omics Da a and Associa ion S udies
The d ama ic accele a ion in genome sequencing means ha
all domes ica ed species and hei ew emaining wild ela i es
will become genome-enabled in he coming decade (e.g., Qiu
e al., 2012; Wu e al., 2014). Re e ence genomes p o ide he
basis o de elopmen o genome-wide assays o a ia ion
in less commonly a med and/o mo e egionally dis ibu ed
li es ock species and popula ions using SNP a ays, as ha e
been de eloped and made a ailable o comme cial li es ock in
he pas 5 yea s (e.g., Ma ukumalli e al., 2009). The choice o
SNPs o inclusion in a ays o less comme cial popula ions
may be expec ed o ocus on a wide a ay o ai s han
o comme cial/ ansbounda y b eeds, such as hose ela ed o
local adap a ion, disease esis ance, d ough ole ance and niche
p oduc cha ac e s, bu in p ac ice his could be hampe ed by
a lack o eliable pheno ypic da a. To enable SNP a ays o be
de eloped in a apid, cos e ec i e and widely applicable manne ,
he iden i ica ion o common e e ence genomes and es panels
o indi iduals o a ay de elopmen and di e si y s udies is key.
Howe e , i is impo an o no e ha wi h he apidly alling cos
o whole genome esequencing (e.g., Lee e al., 2013; Zhang e al.,
2015) using nex gene a ion echnologies and he a ailabili y o
e en lowe cos geno yping by sequencing (GBS: De Dona o e al.,
2013) being a ailable, he p oblem o asce ainmen bias can be
mi iga ed agains since hey allow he iden i ica ion and di ec
es ima ion o SNP di e si y o FAnGR popula ions, b eeds o
species a easonable p ices. Indeed hese me hods a e su icien ly
cos -e ec i e now, ha hey can be in p inciple used as s anda d
assaying app oaches, wi h a cos in he low ens o dolla s o GBS
now easible o analysis o ens o housands o SNPs.
A majo issue iden i ied o genome-wide associa ion s udies
(GWAS) is expe imen al design including, bu no con ined
o, sample size conside a ions (Kada mideen, 2014) and he
a ailabili y o di e en SNP geno yping a ays o some
species and hei compa ibili y o lack he eo (Nicolazzi
e al., 2015). Cha ac e iza ion o en i onmen al pa ame e s
in ex ensi e p oduc ion sys ems is ano he key challenge
o GWAS bu may be assis ed by he applica ion o
E(en i onmen )WAS me hodologies as applied in humans (e.g.,
Pa el e al., 2010). Addi ionally, unde s anding he ole o he
epigenome and i s ole in en i onmen -dependen pheno ypic
di e si y and plas ici y is becoming an inc easing ocus in
li es ock gene ics (e.g., Jammes and Rena d, 2010; Magee
e al., 2011, 2014). Ul ima ely, he in eg a ion o genomic,
epigenomic, ansc ip omic, and en i onmen al da a will be
equi ed i meaning ul la ge-scale s udies a e o be success ul in
iden i ying selec ion and conse a ion a ge s in he e ogeneous
en i onmen s (Jones e al., 2013; Wu e al., 2014) and in
sc u inizing he biological basis o adap a ion, esilience, and
e en animal imp o emen .
Non-au osomal Inhe i ance
Non-au osomal inhe i ance (Y-ch omosomal, X-ch omosomal,
and mi ochond ial) is a compa a i ely neglec ed a ea o
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B u o d e al. Challenges in li es ock conse a ion
TABLE 1 | Summa y o he Top 20 ques ions in a m animal genomics esea ch iden i ied by he pa icipan s o he Ca di symposium.
Ques ion #
1. Nex gene a ion pheno yping The misma ch be ween molecula and pheno ypic da a has inc eased d ama ically. Which key pheno ypic ai s should be
used as common measu es o di e si y s udies o de ine b eed cha ac e is ics in he ace o clima e change?
2. Genome-wide SNP assays The iden i ica ion o common e e ence genomes and es panels o indi iduals o SNP a ay de elopmen in less
comme cial and/o local popula ions is key. Which s a egy shall be used o enable SNP a ays o be de eloped in a apid,
cos e ec i e and widely applicable manne ?
3. Re e ence genomes Which common e e ence genomes and es panels o indi iduals should be used o a ay de elopmen and di e si y
s udies?
4. E(en i onmen )WAS How o cha ac e ize en i onmen al pa ame e s in ex ensi e p oduc ion sys ems?
5. Epigene ics How can epigenomic in o ma ion be in eg a ed wi h pheno ypic and genomic da a o sc u inize he biological basis o
adap a ion and plas ici y/ esilience in li es ock popula ions?
6. Male-media ed gene ic di e si y Which me hodological app oach can be applied o p omo e eliable assembly o he Y-ch omosome, s ill lacking o many
li es ock species, as well as o de elop polymo phic Y-ch omosome ma ke s?
7. Ancien DNA and paleoen i onmen al
analyses
Which s a egies should be ollowed o collec zooa chaeological specimens om c i ical geog aphic si es and p omo e
he analysis o ancien genomes?
8. Conse a ion o genomic di e si y How o design a managemen p og am ha e alua es genomic egions o conse a ion?
9. Polygenic adap i e and economic ai s Haplo ypes s. SNPs: in which si ua ions do one o he o he p o ide a mo e e icien uni o di e si y in QTL egions?
10. Mic osa elli es (STRs) s. SNPs How o in eg a e da a om he STRs and SNPs, and how o manage he ansi ion om STR- o SNP-based
cha ac e iza ion o FAnGR?
11. GW di e si y s a is ics Which combina ion o pa ame e s will be equi ed o adequa ely summa ize genome di e si y?
12. Da a managemen How can links be ween majo FAnGR da abases be p omo ed o be able o ede a e esou ces and ac as an educa ional
cen al poin ?
13. Da a a ailabili y Which o ma should be used o make NGS, pheno yping and GIS da a publicly a ailable, and how can indus y
con ibu e owa d popula ion and main enance o such da abase?
14. Pa icipa o y p ojec s How can pa icipa o y p ojec s, including ci izen science, o example, he use o sma -phone echnologies be
encou aged o enable da a collec ion on FAnGR a a la ge scale?
15. P io i iza ion o conse a ion Why a e p io i iza ion me hods no being applied by policy make s and manage s and is he e a lack o dissemina ion o
pene ance?
16. Genomic p io i iza ion How o implemen genomic app oaches sys ema ically in conse a ion p io i iza ion o include genes impo an in
unc ionally aluable ai s?
17. U iliza ion in p ac ice How o econcile he cos o genomic analysis s. he economic e u ns on geno yped s ock o allow o a wide use o
genomic da a o assis conse a ion, p oduc ion and managemen o FAnGR? Wha is he demand and willingness o pay
wi hin he sec o ?
18. Sys ema ic collec ion How o ensu e ha gene ic and genomic da a a e collec ed su icien ly sys ema ically o be applied o new indica o s?
19. De ining goals Which indica o s can be applied o mos e icien ly moni o gene ic ends in domes ic popula ions?
20. S a egic app oach How will he la es ad ances in ‘omics echnology con ibu e o achie e he ul ima e goal o hal ing he loss o biodi e si y
o FAnGR?
F equencies a e no included o each ques ion and he ques ions a e no lis ed in ank o de .
esea ch in li es ock conse a ion. While s udies o non-
au osomal gene ic ma ke s ha e been ex ensi ely used in
s udies o e olu iona y his o y, bo h singly and combined
(e.g., Gö he s öm e al., 2005; Meadows and Kijas, 2008;
S ensson and Gö he s öm, 2008; Pe ei a e al., 2009; Ramí ez
e al., 2009; Ginja e al., 2010; G oene eld e al., 2010),
hei exploi a ion in genomic s udies has been somewha
o e looked in compa ison o au osomal ma ke s in many
li es ock species. This o e sigh is su p ising gi en he well-
documen ed links be ween mi ochond ial sequence a ia ion
and i ness in human popula ions (e.g., Wallace, 2005) and he
inc easingly ecognized ole ha Y-ch omosomal a ia ion plays
in male e ili y in li es ock (e.g., Chang e al., 2013; Yue e al.,
2014). Technical challenges ha e long been acknowledged wi h
inding polymo phic ma ke s on he Y-ch omosome in mammals
and W-ch omosome in bi ds, howe e such ma ke s, al hough
elusi e, ha e been shown o p o ide no el insigh s in o li es ock
di e si y when a ailable (e.g., Edwa ds e al., 2011; Wallne e al.,
2013), and should be used as a ma e o cou se o p o ide a
male/ emale pe spec i e on li es ock genomic di e si y.
Ancien DNA S udies
Al hough i mly es ablished as a majo ou e in o a deepe
unde s anding o li es ock e olu ion and di e si y (e.g., La son
e al., 2010), ancien DNA (aDNA) s udies ha e been hampe ed
by a numbe o cons ain s. These include limi ed access o
samples om geog aphic a eas whe e (local) domes ica ion may
ha e aken place (e.g., A ica, Nea Eas , Asia, Sou h Ame ica),
limi ed da a sha ing among hose g oups wo king on samples
om c i ical si es (bu see A buckle e al., 2014) and limi ed
success a es, especially o genome-wide s udies. None heless,
ecen ly de eloped me hodological and bioin o ma ics ools
allowed o inc eased accu acy in he analysis o high- h oughpu
ancien DNA da a and e en he cha ac e iza ion o comple e
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B u o d e al. Challenges in li es ock conse a ion
genomes o Pleis ocene ho ses (O lando e al., 2013). Also,
al e na i e sou ces o ma e ial such as pa chmen a e, howe e ,
p o iding p omising ou comes (Teasdale e al., 2015). Exci ing
oppo uni ies ha e ecen ly been opened up by he disco e y
o li es ock DNA in lake sedimen samples in Lake An e ne,
Swi ze land (Gigue -Co ex e al., 2014), which enabled a di ec
compa ison o be made o he paleoen i onmen wi h changes
in his en i onmen due o he a i al o a ming and domes ic
li es ock, and could be applied o desc ibe his o ic luc ua ions in
ag icul u al in ensi y and p ac ice and, exci ingly, may e en allow
he possibili y o p edic i e modeling o he p esence/absence o
sui able ag i-habi a unde u u e clima e change scena ios.
Analy ical Challenges
Conse a ion o Genomic Di e si y
The concep o genome conse a ion has been discussed
ex ensi ely in he li e a u e bu ad ances in genome da a
and echnologies only now allow he de elopmen o b eed
managemen p og ams able o achie e his aim. Fo example,
He e o-Med ano e al. (2014), using genome esequencing
and SNP a ays disco e ed almos 100 non-synonymous
polymo phic nucleo ides nea ly ixed in comme cial pig b eeds
bu wi h an al e na i e allele in non-comme cial popula ions,
a ec ing 65 genes in o al. Such genomic polymo phisms could
all in o a ca ego y o hose ha “canno a o d o be los ” om
less comme cial local b eeds, gi en hei dis inc i eness and
he alue hey po en ially ep esen as a gene ic esou ce o
al e na i e selec ion should he p oduc ion en i onmen change
(K is ensen e al., 2015). Howe e , o design a managemen
p og am ha e alua es genomic egions o conse a ion, no
only do polymo phisms need o be iden i ied, he unc ional
a chi ec u e o hose genomic egions and he genes hey con ain
needs o be assessed and he in e ac ion among hose genes
needs o be conside ed. Recen ly, a s udy o chicken b eeds
examined unc ional a ia ion in copy numbe a ian s (CNV) a
o e 200 genes o e lapping 1000 quan i a i e ai loci, including
some pu a i ely in ol ed in ai s such as skin colo and skele al
cha ac e is ics (Han e al., 2014).
Haplo ype Blocks s. Indi idual SNPs
Ob aining an accu a e desc ip ion o he gene ic polymo phisms
explaining a ai o e olu iona y, adap i e and/o economic
impo ance is no a i ial ask, as ai s subs an ially a y in
he numbe o polymo phisms in ol ed in hei pheno ype and
whe e hese occu ac oss he genome (Godda d and Hayes,
2009; Olson-Manning e al., 2012). Fo example, many o such
ai s a e polygenic and dis ibu ed a ound he genome, making
whole-genome esequencing, and medium and high-densi y SNP
a ays a powe ul app oach o loca ing hem and elucida ing hei
a ia ion (e.g., Huang e al., 2010). Howe e , o ce ain linked
ai s, haplo ypes may p o ide a mo e e icien uni o assessing
di e si y in QTL egions han indi idual SNPs (e.g., Kijas e al.,
2013; Bosse e al., 2014a,b; Mok y e al., 2014), e lec ing local
genomic a chi ec u e in a mo e accu a e ashion. Consequen ly,
a he ini ial s ages o s udies aiming o iden i y he gene ic
basis o pheno ypic a ia ion, gene al genome-wide SNP analyses
may be mo e sui able. I is wo h no ing, howe e , ha phasing
haplo ypes in di e gen popula ions lacking complemen a y
pedig ee da a p esen s a non- i ial challenge. Haplo ype analysis
can p o ide an especially powe ul ool o in es iga e he
hyb id o igin o domes ica ed popula ions. Fo ins ance, mode n
Wes e n comme cial pig genomes a e a mosaic o Eas e n and
Wes e n Eu asian biogeog aphic o igin. Admix u e mapping
allows he “so ing” o haplo ype segmen s o hei pu a i e
o igin. In addi ion, his s a egy has been shown o be powe ul
o in e selec ion on speci ic haplo ypes pos -hyb idiza ion (Bosse
e al., 2014a,b).
Managing he T ansi ion om Mic osa elli e o SNP
Da a
The ansi ion om mic osa elli e ma ke s o SNPs has happened
apidly in FAnGR o comme cial/ ansbounda y b eeds due o
he a ailabili y o ela i ely inexpensi e 50K SNP geno yping
a ays o mos common li es ock species (Ma ukumalli e al.,
2009). Howe e , SNP a ays a e no ye a o dable ools o
much o he wo ld’s FAnGR and a e no ye a ailable o
all species (see abo e). This he e o e aises he immedia e
p oblem o how o in eg a e da a om he wo ma ke ypes
and how o manage he ansi ion om mic osa elli e-based
FAnGR cha ac e iza ion (much o which has been ca ied ou
using ma ke s ecommended by ISAG, FAO, 2011) o SNP-
based cha ac e iza ion. One op ion is o e-geno ype many o
he b eeds ha al eady ha e mic osa elli e geno ypes wi h SNPs
(Ajmone-Ma san e al., 2014), bu his would be expensi e and
i implemen ed would aise he ques ion as o whe he he new
da a would again be eplaced by a newe echnology (e.g., whole-
genome esequencing). P agma ically, i seems ha mic osa elli e
da a a e pe ec ly adequa e o es ima ing gene ic di e si y and
desc ibing demog aphic ela ionships (e.g., Fe ando e al., 2014).
Howe e , o cos easons he ull se o mic osa elli e ma ke s
was equen ly no applied, especially in de eloping coun ies.
Also, mic osa elli e da a will no be as e icien o enabling
he iden i ica ion and a ge ed conse a ion o genomic egions
unde selec ion since da a a e usually p oduced wi h a ew ens o
quasi-neu al ma ke s (e.g., He e o-Med ano e al., 2013).
Ne e heless, i is becoming clea ha da a p oduced
using SNP a ays a e mo e epea able and do no su e
om sco ing di e ences ha ha e made he combina ion o
mic osa elli e da ase s some imes p oblema ic and equi ing
s a is ical e alua ion (Lens a e al., 2012). Pa adoxically, whole
genome esequencing may become he mos eliable and cos
e ec i e way o analyse genomic di e si y in he u u e, e en o
non-comme cial b eeds, i he cos comes down by ano he o de
o magni ude (as may happen wi h po able sequence s such as
Ox o d Nanopo e’s MiniION sys em), p o iding he ad an age o
no longe needing o use a se o SNP ma ke s asce ained om
comme cial popula ions.
Genome-wide Di e si y S a is ics
The eme gence o whole genome sequencing and medium-high
densi y SNP a ays means ha summa izing gene ic di e si y can
now be a mo e nuanced and genomic egion-speci ic exe cise. I
is well known ha asce ainmen bias o SNP a ays can s ongly
unde es ima e he di e si y o he (usually au och honous and
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B u o d e al. Challenges in li es ock conse a ion
less comme cial) b eeds no used o design he a ays (Po o
Ne o and Ba endse, 2010). This phenomenon does no impac on
whole-genome esequencing as all polymo phisms a e cap u ed
p o ided su icien sequence dep h is achie ed. A combina ion
o pa ame e s will be equi ed o adequa ely summa ize genome
di e si y (e.g., he e ozygosi y and e ec i e popula ion size and
inb eeding), as no single all-encompassing s a is ic o summa ize
all o a popula ion’s genomic di e si y and his o y exis s, despi e
o how emp ing i may be o de ine such s a is ic (e.g., o
policy make s). E ec i e popula ion size (Ne) es ima es can
be ob ained wi h as li le as a single genome using me hods
such as he Pai wise Sequen ial Ma ko ian Coalescen , al hough
hese analyses can p o e inconclusi e i genome co e age is
insu icien o i admix u e pe ains (Li and Du bin, 2011;
O ozco- e Wengel and B u o d, 2014; Schi els and Du bin,
2014; F an z e al., 2015). Fo ecen ly e ol ed popula ions,
such as many domes ic species, linkage disequilib ium-based
(LD) es ima es may be mo e accu a e and me hods a e now
eme ging o ca y ou hese analysis (e.g., Ba ba o e al.,
2015). Runs o homozygosi y (ROH; e.g., Bosse e al., 2012;
Sc aggs e al., 2014) unc ions desc ibing he dis ibu ion o
homozygosi y h oughou he genome may also se e as a obus
genome-scale Ne es ima o in he u u e, al hough in e p e a ion
and scaling depends on he local ecombina ion. ROH a e
al eady used as a genomic p oxy o inb eeding (e.g., Pu ield
e al., 2012; Cu ik e al., 2014), including o speci ic genome-
loca ed ai s (P yce e al., 2014). This app oach p omises
o be an e icien way o a oid he p oduc ion o o sp ing
homozygous o dele e ious alleles a speci ic genomic egions
ha a e associa ed wi h inb eeding dep ession (P yce e al.,
2014).
Da a Managemen
Da a Accessibili y
As also iden i ied by Ca dellino and Boyazoglu (2009) he e
emains a majo need o p o ide much be e links be ween
he majo FAnGR da abases, which ha e la gely been se up
independen ly and a e b eed- ocused (G oene eld e al., 2010).
The li es ock genomics communi y needs ei he o build on an
exis ing pla o m (such as he ARKDB, h p://www. hea kdb.
o g/a kdb/ and he Eu opean Nucleo ide A chi e, h p://www.
ebi.ac.uk/ena), ha ha e some le el o connec i i y, e.g., wi h
Ensembl (h p://www.ensembl.o g/index.h ml) o o es ablish an
independen communi y-based ini ia i e(s) unde he o m o a
use - iendly global web po al and would include web se ices
able o ede a e esou ces and ac as an educa ional cen al
poin . Such esou ces a e al eady being de eloped, including
he Adap map p ojec o goa s (h p://www.goa adap map.
o g/). In o ma ion on li es ock ela ed da a should be made
a ailable and use ul ecommenda ions a e equi ed o in o m
s akeholde s on how o eco d da a, and whe e o s o e wha
ype o in o ma ion. In pa icula , i is impo an o p omo e
wi hin he communi y o use s ha aw and me a-da a a e
key componen s and ha hey should be made a ailable in
public da ase s oge he wi h elabo a ed da ase s. When he e
a e exis ing public esou ces o a gi en da a ype such as
hose lis ed abo e, hey should be used o hei abili y o
se s anda ds and cen alize da a access. Fo o he da a ypes,
open digi al eposi o ies such as D yad (h p://da ad yad.o g/),
Zenodo (h ps://zenodo.o g/), o igsha e (h p:// igsha e.com/)
comp ise in aluable ools ac ing as incen i es o people o
main ain and upg ade hei da ase s as da a can be submi ed
and au ho s a e p o ided wi h a e e ence which can be ci ed.
This da a ecosys em becomes especially impo an wi h he
my iad o SNP a ay da ase s ha a e now a ailable and he
incompa ibili y among di e en e sions o hese a ays wi hin
he same species (Nicolazzi e al., 2015). Mo eo e , o add alue
o gene ic esou ces, ede a ing gene bank esou ces is one s ep
ha needs o be comple ed by explici connec ion— h ough
geog aphical coo dina es—wi h pheno ypic da a, bu also wi h
socio-economic, socio-demog aphic, clima ic, en i onmen al,
and policy in o ma ion. This equi es links o exis ing online
digi al esou ces (Joos e al., 2010) ha a e cu en ly a ely used
by he FAnGR communi y and need o be lis ed on such a global
po al.
Da a A ailabili y
While many geno yping p ojec s on comme cial li es ock b eeds
a e unded by indus y, ende ing all excep summa y da a
una ailable in many cases, in p inciple aw da a om publicly
unded p ojec s should be made publicly a ailable. Indeed,
when da a a e open, i i s makes he in o ma ion mo e
c edible, makes da a e-usable, and also enables ep oducibili y
an impo an scien i ic p inciple (E z e al., 2014). Inc easingly,
in e na ional conso ia, such as FAANG on animal unc ional
genomics ollow he To on o p o ocol and immedia ely place
da a in he public domain (h p://www. aang.o g; The To on o
In e na ional Da a Release Wo kshop Au ho s, 2009; Ande sson
e al., 2015). A nex gene a ion pheno yping da abase should also
be es ablished, including GIS and anonymized a m le el da a,
animal pho og aphs and me a-da a— his could pa ly ollow
he o ma o he EU FP5 p ojec Econogene (h p://www.
econogene.eu) and would be mos e icien ly linked wi h FAO’s
DAD-IS and EFABIS (h p://e abis. z . al.de). The owne ship
and hos ing o such a esou ce would be logis ically and
inancially challenging, and could p o ide an oppo uni y o he
ag i-indus y o con ibu e owa d conse a ion o he gene ic
esou ces i has u ilized in he pas and may need again in
he u u e. This could also be pa o he communi y-based
ac ion men ioned abo e, wi h many ad an ages (logis ic and
unding), bu equi ing a s ong leade ship. An app oach o
da a esou cing such has been exempli ied wi h human da a by
he 1000 Genomes p ojec (h p://www.1000genomes.o g) and
he 1001 A abidopsis genomes esou ce (h p://1001genomes.
o g wi h da a being publicly a ailable ei he immedia ely o
a e an ag eed emba go pe iod, could be e y applicable o
li es ock s udies. Fo example, he esequencing da a om he
EU F amewo k 7 Nex gen p ojec was made a ailable sho ly
a e he p ojec ’s comple ion a he Eu opean Bioin o ma ics
Ins i u e’s FTP si e ( p:// p.ebi.ac.uk/pub/da abases/nex gen/).
Pa icipa o y P ojec s
Many indi iduals who a e in e es ed in FAnGR a e in ol ed
in ag icul u e as smallholde s, a me s, b eede s, and p oduce s
F on ie s in Gene ics | www. on ie sin.o g 6Oc obe 2015 | Volume 6 | A icle 314
B u o d e al. Challenges in li es ock conse a ion
and many o hese a e no o mally in ol ed in b eeding
p og ams and li es ock conse a ion, ye main ain an in e es
h ough ag icul u al shows and a me s’ ma ke s (e.g., Zimme e ,
2010; Johns e al., 2013). A he same ime, he ole o
pa icipa o y app oaches and mobile echnology po en ially
enables obus da a collec ion on a p e iously unimaginable
scale (Lisson e al., 2010; Teache e al., 2013; Sambo e al.,
2015). Use o c owdsou cing should he e o e be encou aged in
FAnGR as should use o sma -phone apps and echnologies o
pho og aphy, da a s o age and sampling (e.g., “do- o ms” h p://
www.do o ms.com). A logical combina ion o hese ini ia i es
lies in he possibili y o a li es ock communi y independen
ini ia i e, including web se ices o ede a e hese da a sou ces,
o ca y ou quali y con ol and p o iding a cen al access poin
o da a bu also in o ma ion o educa e people on how o eco d
FAnGR da a. Such app oaches could also help in secu ing unds
o p ojec s in FAnGR popula ions and b eeds, which o en
ace he p oblem o secu ing unds o ca y ou his necessa y
esea ch.
Conse a ion, Managemen , and
P io i iza ion
Is P io i iza ion a P io i y?
A pa adigm wi hin FAnGR o he pas 15 yea s conce ns he use
o gene ic da a, alongside o he in o ma ion in p io i iza ion o
li es ock popula ions and b eeds o conse a ion (Wei zman,
1992; Simiane e al., 2003; Boe che e al., 2010; Ginja e al.,
2013). Howe e , he e is limi ed e idence ha his app oach
is being applied sys ema ically ac oss coun ies epo ing o
he FAO, al hough he second epo on he S a e o he
Wo ld’s Animal Gene ic Resou ces has documen ed ac i i ies
o some ex en (FAO, 2015b,c). I , howe e , p io i iza ion
me hods a e no being applied by manage s and policy-
make s, he ques ion needs o be asked as o why? A
numbe o explana ions may pe ain: i s , he me hod(s)
may ha e no gained enough ac ion wi h policy make s
o ensu e i s/ hei implemen a ion, which may indeed be
because genomic me hods, which ha e ye o be sys ema ically
implemen ed, will la gely supe sede he mic osa elli e-based
app oaches implemen ed hus a and enable conse a ion
p io i iza ion o include genes impo an in unc ionally aluable
ai s (e.g., To o e al., 2014). Fu he mo e, p io i iza ion on he
basis o gene ic dis ances (Wei zman, 1992) is con ounded by
gene ic isola ion o b eeds (Eu opean Ca le Gene ic Di e si y
Conso ium, 2006). Second, p io i iza ion may no ac ually
be needed, a leas in ce ain egions, whe e b eed socie ies
a e ac i e and all o mos o he b eeds can be main ained.
Howe e , ecen animal heal h eme gencies (e.g., ou b eaks
o ansmissible spongi o m encephalopa hies, TSEs) ha e cas
doub on his simplis ic scena io and equi ed he applica ion
o ca e ul gene ic managemen du ing and a e he ou b eak.
While p io i iza ion may be less o a p io i y in he wo ld’s
iches egions, i is no expec ed o be he case in de eloping
coun ies, whe e ex inc ion may ake a numbe o o ms,
including gene ic e osion (e.g., Be houly-Salaza e al., 2012;
FAO, 2015a,b). Finally, he me hods de eloped may no
ha e been applied because policy make s and manage s a e
unawa e o hei a ailabili y, which could be due o a lack
o dissemina ion o pene ance o educa ional ma e ial o he
decision make s.
U iliza ion in P ac ice
While esea ch and applica ion o genomic ools in li es ock
is occu ing in many comme cial/ ansbounda y b eeds (e.g.,
P yce e al., 2014; Sc aggs e al., 2014), i s applica ion in less
comme cial popula ions is spo adic and he scien i ic basis o
decisions on managemen o indigenous li es ock, o example
in which ge mplasm o s o e, assessing he e ec s o upg ading
o e alua ing ongoing gene ic managemen is he e o e highly
a iable (e.g., B own e al., 2014; FAO, 2015b). This poin s o
he eali y ha gene ically-based p io i iza ion is unlikely o be
ope a ional in he absence o o he conside a ions, including
comme cial eali y and he ecosys em/p oduc ion en i onmen
(e.g., Sande son e al., 2013). The use o genomic da a o manage
FAnGR wi hin b eeds is howe e , con inuing apace (see abo e)
and can be demons a ed o be assis ing conse a ion, p oduc ion
and managemen in many cases (e.g., He e o-Med ano e al.,
2014; Sc aggs e al., 2014). Howe e , o many b eeds he cos o
gene ic/genomic analysis s. he po en ial economic e u ns on
geno yped s ock (wi h a ew excep ions such as TSE esis ance)
makes i s applica ion uneconomic, and he e o e i is o en
no applied. I is unlikely ha geno yping cos s will each he
le el o economic iabili y o many FAnGR, howe e his
assump ion should be es ed by some a ge ed esea ch ac oss he
sec o .
De ining Goals
The Con en ion on Biological Di e si y’s Aichi Ta ge 13,
which ecommends ha : “s a egies ha e been de eloped and
implemen ed o minimizing gene ic e osion and sa egua ding
gene ic di e si y” is e lec ed in he Ta ge o S a egic
P io i y A ea 4 o he Global Plan o Ac ion o Animal
Gene ic Resou ces (FAO, 2007b). These esou ce indica o s
con ibu e o he measu emen o p og ess owa d Aichi
Ta ge 13 (FAO, 2012b) and a e calcula ed a na ional,
egional and global le els, based on da a en e ed by Na ional
Coo dina o s o he Managemen o Animal Gene ic Resou ces1
(172 coun ies had nomina ed a Na ional Coo dina o as o
July, 2014) in o he Domes ic Animal Di e si y In o ma ion
Sys em (DAD-IS). The ollowing indica o s ha e been ag eed
by he Commission on Gene ic Resou ces o Food and
Ag icul u e:
• he numbe o locally adap ed b eeds;
• he p opo ion o he o al popula ion accoun ed o by locally
adap ed and exo ic b eeds; and
• he numbe o b eeds classi ied as a isk, no a isk and
unknown.
The Global Da abank o Animal Gene ic Resou ces, he
backbone o DAD-IS, enables Na ional Coo dina o s o en e
b eed-speci ic da a, including da a on he size and s uc u e o
b eed popula ions, equi ed o calcula e hei isk s a us. FAO
1The lis o Na ional Coo dina o s o he Managemen o Animal Gene ic
Resou ces is ound a dad. ao.o g/cgi-bin/E abisWeb.cgi?sid=-1,con ac s.
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B u o d e al. Challenges in li es ock conse a ion
p oduces biannual S a us and T ends Repo s (FAO, 2015a). Fo
he i s epo on The S a e o he Wo lds Animal Gene ic
Resou ces, a isk s a us classi ica ion based on popula ion size
da a was used. The (lack o ) a ailabili y o global da a cu en ly
makes a mo e elabo a e sys em in ol ing, o example, molecula
di e si y indices, popula ion s uc u e/ agmen a ion, pedig ee
da a, numbe and size o he ds, and geog aphic dis ibu ion
inope able. While genomic me hods migh help o o e come
hese da a de iciencies, i hey a e o be applied o li es ock
conse a ion, i is impo an o de ine he goals o such
app oaches and how he da a could be used o imp o e o
augmen he cu en se o indica o s using da a ha could
be collec ed on ends in e ec i e popula ion size, admix u e,
inb eeding and genome-wide di e si y. The wide applica ion
o such da a hinges on hei applicabili y o au och onous, less-
comme cial b eeds. Un o una ely, he da a cu en ly p o ided o
FAO does no e en allow he eliable calcula ion o basic ends
cu en ly measu ed ia he abo e indica o s (Ti enso e al.,
2014; FAO, 2015a), ye he li es ock gene ics and conse a ion
communi y possess many o he ools needed o di ec ly e alua e
whe he signa o ies o he CBD a e “.. .minimizing gene ic
e osion” and “sa egua ding gene ic di e si y” (CBD Ta ge 13).
Two key de elopmen s a e equi ed o enable he cu en
app oach o mo e di ec ly use gene ic o genomic da a in he
u u e: i s , he li es ock conse a ion gene ics communi y mus
he e o e insis ha da a a e collec ed and analyzed in such a
way ha esul s a e di ec ly compa able and second, o help
de elop be e indica o s applied o moni o ing gene ic ends in
domes ic popula ions.
CONCLUSION
Any exe cise designed o assess he s a e-o - he-a in a scien i ic
ield only manages o cap u e a b ie momen in ime, which is
why he Ho izon scanning exe cises ca ied ou in biodi e si y
conse a ion a e epea ed e e y yea (see Su he land e al.,
2015). He e, we a emp ed o ake a longe - e m (decadal) iew
o genomic esou ces conse a ion, and du ing his pe iod,
some majo miles ones will be passed. Chie among hese is
he imminen elease o he Second Repo on he S a e o
he Wo ld’s Animal Gene ic Resou ces (FAO, 2015b,d) and he
Con en ion on Biological Di e si y’s 2020 deadline hal ing he
loss o biodi e si y Aichi a ge s. In he con ex o he d ama ic
ad ances in ‘omics echnology ha a e expec ed du ing he
nex decade, he ield is expec ed o mo e as . Bu s uc u al
changes in he li es ock sec o ha will b ing u he e osion
du ing his pe iod a e likely o be equally apid. Howe e , his
makes i c i ically impo an ha a s a egic app oach is aken
o inco po a ing hese echnological ad ances in o eal wo ld
FAnGR conse a ion. Such an app oach has been aken in he
pas (e.g., wi h he implemen a ion o app o ed mic osa elli e
ma ke se s) and, we would a gue, is needed now o ensu e ha
p ac ical conse a ion o a m animal ag icul u al biodi e si y is
no le behind. The FAnGR communi y he e o e needs o make
bes use o new genomic ools, and a he same ime con inue
and augmen i s classical pheno yping e o s. Bo h, genomic
and pheno ypic ools need o be applied mo e consis en ly, a
a much wide scale and o mo e b eeds, o desc ibe, u ilize
and conse e he wo ld’s genomic/b eed di e si y o u u e
gene a ions.
ACKNOWLEDGMENTS
The Eu opean Science Founda ion (ESF) GENOMIC—
RESOURCES Resea ch Ne wo king P og amme (RNP) was
suppo ed by: Fonds zu Fö de ung de wissenscha lichen
Fo schung (FWF), FWF Aus ian Science Fund, Aus ia—Fonds
Na ional de la Reche che Scien i ique (FNRS), Belgium—Fonds
oo We enschappelijk Onde zoek—Vlaande en (FWO),
The Resea ch Founda ion—Flande s, Belgium—Nacionalna
zaklada za znanos , isoko škols o i ehnologijski az oj
Republike H a ske, C oa ian Science Founda ion, Republic
o C oa ia—Suomen Aka emia, Bio ie eiden ja ympä is ön
u kimuksen oimikun a, Academy o Finland, Resea ch
Council o Biosciences and En i onmen , Finland—Deu sche
Fo schungsgemeinscha (DFG), Ge man Resea ch Founda ion,
Ge many—Nede landse O ganisa ie oo We enschappelijk
Onde zoek (NWO), The Ne he lands O ganisa ion o Scien i ic
Resea ch, The Ne he lands—No ges Fo sknings åd, The
Resea ch Council o No way, No way—Fo sknings åde ö
miljö, a eella nä inga och samhällsbyggande, Swedish Council
o En i onmen , Ag icul u al Sciences and Spa ial Planning
(FORMAS), Sweden—Schweize ische Na ional onds (SNF),
Swiss Na ional Science Founda ion, Swi ze land—Bio echnology
and Biological Sciences Resea ch Council (BBSRC), Uni ed
Kingdom.
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