A first-generation microsatellite-based genetic linkage map of the Siberian jay (Perisoreus infaustus) : insights into avian genome evolution

BioMed Cen al Page 1 o 17 (page numbe no o ci a ion pu poses) BMC Genomics Open Access Resea ch a icle A i s -gene a ion mic osa elli e-based gene ic linkage map o he Sibe ian jay (Pe iso eus in aus us): insigh s in o a ian genome e olu ion Sonja Jaa i, Meng-Hua Li* and Juha Me ilä Add ess: Ecological Gene ics Resea ch Uni , Depa men o Biological and En i onmen al Sciences, PO Box 65, FIN-00014 Uni e si y o Helsinki, Finland Email: Sonja Jaa i - sonja.jaa i@helsinki. i; Meng-Hua Li* - menghua.li@helsinki. i; Juha Me ilä - juha.me il[email p o ec ed] * Co esponding au ho Abs ac Backg ound: Genomic esou ces o he majo i y o ee-li ing e eb a es o ecological and e olu iona y impo ance a e sca ce. The e o e, linkage maps wi h high-densi y genome co e age a e needed o p og ess in genomics o wild species. The Sibe ian jay (Pe iso eus in aus us; Co idae) is a passe ine bi d which has been subjec o lo s o esea ch in he a eas o ecology and e olu iona y biology. Knowledge o i s genome s uc u e and o ganiza ion is equi ed o ad ance ou unde s anding o he gene ic basis o ecologically impo an ai s in his species, as well as o p o ide insigh s in o a ian genome e olu ion. Resul s: We desc ibe he i s gene ic linkage map o Sibe ian jay cons uc ed using 117 mic osa elli es and a mapping pedig ee o 349 animals ep esen ing i e amilies om a na u al popula ion b eeding in wes e n Finland om he yea s 1975 o 2006. Ma ke s we e esol ed in o nine au osomal and a Z-ch omosome-speci ic linkage g oup, 10 ma ke s emaining unlinked. The bes -posi ion map wi h he mos likely posi ions o all signi ican ly linked loci had a o al sex-a e age size o 862.8 cM, wi h an a e age in e al dis ance o 9.69 cM. The emale map co e ed 988.4 cM, whe eas he male map co e ed only 774 cM. The Z-ch omosome linkage g oup comp ised six ma ke s, h ee pseudoau osomal and h ee sex-speci ic loci, and spanned 10.6 cM in emales and 48.9 cM in males. Eigh y-one o he mapped loci could be o de ed on a amewo k map wi h odds o >1000:1 co e ing a o al size o 809.6 cM in emales and 694.2 cM in males. Signi ican sex speci ic dis o ions owa ds educed male ecombina ion a es we e e ealed in he en i e bes -posi ion map as well as wi hin wo au osomal linkage g oups. Compa a i e mapping be ween Sibe ian jay and chicken ancho ed 22 homologous loci on 6 di e en linkage g oups co esponding o chicken ch omosomes Gga1, 2, 3, 4, 5, and Z. Qui e a ew cases o in a-ch omosomal ea angemen s wi hin he au osomes and h ee cases o in e -ch omosomal ea angemen be ween he Sibe ian jay au osomal linkage g oups (LG1, LG2 and LG3) and he chicken sex ch omosome GgaZ we e obse ed, sugges ing a conse ed syn eny, bu changes in ma ke o de , wi hin au osomes du ing abou 100 million yea s o a ian e olu ion. Conclusion: The cons uc ed linkage map ep esen s a aluable esou ce o in aspeci ic genomics o Sibe ian jay, as well as o a ian compa a i e genomic s udies. Apa om p o iding no el insigh s in o sex-speci ic ecombina ion a es and pa e ns, he desc ibed maps – om a p e iously genomically uncha ac e ized supe amily (Co idae) o passe ine bi ds – p o ide new insigh s in o a ian genome e olu ion. In combina ion wi h high- esolu ion da a on quan i a i e ai a iabili y om he s udy popula ion, hey also p o ide a ounda ion o QTL-mapping s udies. Published: 3 Janua y 2009 BMC Genomics 2009, 10:1 doi:10.1186/1471-2164-10-1 Recei ed: 16 July 2008 Accep ed: 3 Janua y 2009 This a icle is a ailable om: h p://www.biomedcen al.com/1471-2164/10/1 © 2009 Jaa i e al; licensee BioMed Cen al L d. This is an Open Access a icle dis ibu ed unde he e ms o he C ea i e Commons A ibu ion License (h p://c ea i ecommons.o g/licenses/by/2.0), which pe mi s un es ic ed use, dis ibu ion, and ep oduc ion in any medium, p o ided he o iginal wo k is p ope ly ci ed. BMC Genomics 2009, 10:1 h p://www.biomedcen al.com/1471-2164/10/1 Page 2 o 17 (page numbe no o ci a ion pu poses) Backg ound Unde a ious comple ed o ongoing p ojec s, apid p og ess has been a ained in he gene a ion o genomic esou ces o model o ganisms and domes ic animals o medical, economic, o ag icul u al impo ance (e.g. [1- 3]). Howe e , genomic esou ces o he majo i y o ee- li ing e eb a es o ecological and e olu iona y impo - ance a e s ill sca ce. Fo ins ance, in wild bi ds, de elop- men o genomic esou ces a e s ill in hei in ancy, and only ew ini ial e o s in linkage mapping [4-8], es ima- ion o he ex en o linkage disequilib ium [9,10], and syn enic compa ison be ween ela ed species [7,8,11-14] ] ha e been conduc ed. Hence, e y limi ed in o ma ion on he genome s uc u e o wild bi d species is a ailable o u he syn hesis, as well as o s udy and cha ac e ize molecula unde pinnings o pheno ypic ai s. Since wild passe ine bi ds a e impo an 'model' o ganisms in ecol- ogy and e olu iona y biology, and in s udies o li e his o y e olu ion (e.g. [15]), beha iou (e.g. [16,17]) and e olu- iona y quan i a i e gene ics in pa icula (e.g. [18-20]), knowledge o hei genome s uc u e and o ganiza ion is i al o ad ance ou unde s anding o he gene ic basis o ecologically impo an ai s [21]. Gene ic maps cons i u e essen ial and powe ul o ganiza- ional ools o genomic esea ch [22]. Among he mos impo an applica ions o gene ic maps in genomic anal- yses is in ha hey p o ide a pla o m o suppo s udies u ilizing o aiming o apply candida e gene app oaches [21,23], QTL mapping [24], compa a i e genomics [25], and genome anno a ion [26]. Howe e , cons uc ion o gene ic linkage maps o non-model o ganisms is compli- ca ed by se e al ac o s [27,28]. One o he majo obs a- cles o he cons uc ion o linkage maps in passe ine bi ds (bu see [4]) is he sca ci y o in o ma i e gene ic ma ke s. Among a a ie y o molecula make s p e iously employed in linkage mapping in di e en o ganisms, mic osa elli e ma ke s ha e o en p o en mos use ul due o hei hype a iabili y, as e olu iona y a es, codomi- nance, wide dis ibu ion h oughou he genomes, and he ela i e ease wi h which hey can be de eloped and geno yped using he polyme ase chain eac ion (PCR; e.g. [29]). While gene ic maps exis in one o m o ano he o a ious species, i is wo h no icing ha he s udies a e so a gene ally limi ed o domes ic animals o na u al pop- ula ions o wild species ha can easily be b ed in cap i i y, o whe e su icien ly la ge li e sizes a e being p oduced in na u al se ings and a e accessible o sampling o allow he es ablishmen o he pedig ee necessa y o linkage analysis [9]. Un o una ely, he cha ac e is ics ha make popula ions p ac ical o linkage mapping [9] a e ound only among a small ac ion o species s udied by ecolo- gis and e olu iona y biologis s. Linkage maps ha e now been cons uc ed in ou popula ions o non-model ani- mals o which long- e m indi idual-based da ase s a e a ailable (see also: [8]), and whe e na u al long- e m ped- ig ees ( a he han expe imen al b eeding p og ammes) ha e been used o ollow he co-seg ega ion o ma ke alleles [28]. Two o hese mapping popula ions a e in ungula e species (soay sheep, O is a ies [24]; ed dee , Ce - us elaphus [27]) and wo a e in passe ine bi ds (g ea eed wa ble , Ac ocephalus a undinaceus [4,6,13]; colla ed ly- ca che , Ficedula albicollis [5,9,11]). The Sibe ian jay (Pe iso eus in aus us) is a passe ine bi d which has been subjec o conside able ecological and e olu iona y esea ch du ing he pas decades. S udies in i s b eeding biology [30-33], ma ing sys em [34,35], o - aging beha iou [36], ep oduc i e success [37], pa en al ca e and dispe sal pa e n [38,39], amily s uc u e [40], pheno ypic plas ici y [41] and le els o inb eeding [42] ha e been conduc ed. Thus, hese p e ious s udies o m an app op ia e se ing in an ini ia i e o explo e he in e- g a ion o genomics wi h he domain o ecology and e o- lu iona y biology [43], p o ided ha a leas some basic knowledge o he species' genome can be ob ained. Wi h an access o de ailed pedig ees o a Sibe ian jay popula- ion moni o ed o e 30 yea s [40,42], as well as access o a no el se o polymo phic mic osa elli es de eloped o his species [44], cons uc ion o a linkage map is now ealis ic. In an e olu iona y con ex , he chicken genome sequence [45] eleased ecen ly acili a es genomic s udies in o he bi d species by compa a i e genomic app oaches [13,25]. Mo eo e , gi en he ea ly di e gence o a ian lin- eages be ween passe i o ms and galli o ms (≈ 100 million yea s ago; [46]) and he high le el o phylogene ic di e - gence be ween jays belonging o he Co idae amily and he o he passe ines o which linkage maps ha e been published (e.g. [47,48]), a linkage map o he Sibe ian jay may p o ide new insigh s in o a ian genome e olu ion, and he eby also o he ex ensi e mo phological, li e his- o ical and beha iou al di e si ica ion wi hin he o de Passe i o mes (see [47]). The aim o his s udy was o de elop a i s -gene a ion gene ic linkage map o a wild popula ion o Sibe ian jays on he basis o 117 mic osa elli es, including a no el se o 108 ma ke s. To his end, a amewo k map was con- s uc ed o iden i y ma ke s whose local ela i e o de s we e s a is ically well suppo ed wi h an unambiguous loca ion in he map. Since he e ochiasmy has been obse ed in p e ious s udies o many species (e.g. zeb a ish [49]; and g ea eed wa ble [4]), sex-speci ic a ia ion in he ecombina ion a e and he gene ic map dis ance we e also in es iga ed. Fu he mo e, o p o ide a compa a i e pe spec i e o add ess he e olu ion o genome o ganisa ion he ex en o syn eny and locus o de conse a ion be ween Sibe ian jay and chicken was e alua ed by a BLAST analysis agains he chicken genome sequence. BMC Genomics 2009, 10:1 h p://www.biomedcen al.com/1471-2164/10/1 Page 3 o 17 (page numbe no o ci a ion pu poses) Resul s Cha ac e is ics o polymo phic mic osa elli es O he 117 mic osa elli es sco ed, six loci (SJ009, SJ046, SJ048, SJ069, SJ083 and SJ108) we e assigned o he Z- ch omosome by obse a ion o comple e coseg ega ion wi h sex and he obse a ion o he e ozygosi y in some males bu none o he emales in he pedig ees. None o he ma ke s examined appea ed o be si ua ed in W-ch o- mosome since all he ma ke s had alleles in he males. The numbe o in o ma i e meioses a ied om 33 (SJ047) o 474 (CKL5) wi h an a e age o 284.63 in o ma i e mei- oses pe locus. Mo e de ails abou le els o gene ic a ia- bili y (HO, HE and PIC) a e shown in Addi ional File 1. Gene ic linkage maps An o e iew o he linkage da a is gi en in Figu es 1, 2 and Table 1 depic ing he bes -posi ion and amewo k link- age maps and hei cha ac e is ics. O he 117 mic osa el- li es, 107 loci (91%) we e assembled in o 9 au osomal linkage g oups (LG1 – LG9) and one Z-ch omosome link- age g oup (LGZ), and he o he 10 polymo phic mic osa - elli es (SJ002, SJ003, SJ005, SJ020, SJ030, SJ034, SJ118, MJG1, PER1 and LTML8) appea ed o be unlinked o any o he ma ke by wo-poin analysis wi h LOD sco es < 3.0. O he en unmapped ma ke s, six had less han 60 in o ma i e meioses while ou had mo e han 200 in o ma i e meioses. O he nine au osomal LGs, se en comp ised o six o mo e loci and he emaining h ee LGs each con ained wo o h ee loci, wi h an a e age o ca. 11 mic osa elli es pe LG. Fo he sex-a e age au osomal LGs in he bes -posi ion map (Figu e 1), he meio ic leng hs, e alua ed as he dis ance be ween he ou e mos ma ke s on each LG, anged om 10.6 cM (LG09) o 185.6 cM (LG01) spanning in o al 862.8 cM o he Sibe ian jay genome. The a e age ma ke in e al was 9.69 cM calcu- la ed as he a i hme ic mean o he map dis ances be ween adjacen ma ke s (Table 1). On he maps, 35.9% (33/92) o he in e als be ween ma ke s a ied om 0 o 5 cM, 31.5% (29/92) anged om 5 o 10 cM, and 20.7% (19/ 92) om 10 o 20 cM, and 12% (11/92) we e > 20 cM. Sex-speci ic au osomal maps we e also cons uc ed (Fig- u e 1). The sum o he leng h o all au osomal LGs was 774.0 cM in males and 988.4 cM in emales, wi h an a e - age in e ma ke spacing o 8.6 cM and 12.1 cM, espec- i ely. The male map comp ises LGs anging in leng h om 7.7 cM o 171.1 cM while he emale map con ains LGs wi h a leng h om 9.2 cM o 229.2 cM (Table 1). Ou o he nine pai s o male and emale LGs, se en we e la ge in he emale map and wo we e la ge in he male map. In o al, he au osomal LGs we e smalle in males as com- pa ed o emales wi h a emale- o-male map a io o 1.28. The sex-a e age map was in e media e in leng h be ween sex-speci ic maps, and 1.12 imes longe han he male map. F amewo k ma ke s, which could be o de ed wi h LOD sco e o 3.0 o g ea e (indica ing odds o 1000:1), a e indica ed in bold on s in he bes -posi ion map (Figu e 1). O he o al 107 mapped ma ke s, 81 loci we e signi - ican ly o de ed in he amewo k map and mos (16/24) o he emaining loci could be placed wi h signi ican sup- po in ei he o wo al e na i e in e als. When only he amewo k ma ke s we e conside ed, he o al size o au osomal linkage g oups was 692.1 cM in he sex-a e age map, 649.4 cM in he male map, and 799 cM in he emale Table 1: Cha ac e is ics o he bes -posi ion and amewo k maps o Sibe ian jay LG Bes -posi ion map (cM) F amewo k map (cM) No. o loci Sex a e age 씸씹A e age in e - ma ke dis ancea Ra io o 씸/ 씹 maps No. o loci Sex a e age 씸씹A e age in e - ma ke dis ancea Ra io o 씸/ 씹 maps LG1 29 185.6 213.6 168.3 6.87 1.27 20 167.0 182.8 156.7 8.35 1.17 LG2 27 181.5 229.2 141.3 6.72 1.62 21 141.3 212.1 116.8 6.73 1.82 LG3 13 182.6 197.9 171.1 16.6 1.16 10 170.2 175.5 171.3 17.02 1.02 LG4 11 98.2 110 86.7 9.82 1.27 9 76.0 88.3 63.8 8.44 1.38 LG5 8 85.2 92.9 82.1 12.17 1.13 7 83.9 93.4 78.4 11.99 1.19 LG6 6 78.2 98.9 65.4 15.64 1.51 3 14.4 15.5 13.2 4.80 1.17 LG7 3 26.4 24.3 32.3 13.2 0.75 2 14.2 9.8 22.4 7.10 0.44 LG8 2 14.5 9.2 19.1 15.5 0.48 2 14.5 9.2 19.1 7.25 0.48 LG9 2 10.6 12.4 7.7 10.6 1.61 2 10.6 12.4 7.7 5.30 1.61 LGAb101 862.8 988.4 774 9.69 1.28 76 692.1 799 649.4 9.11 1.23 LGZ 6 23.8 10.6 48.9 4.76 0.22 5 22.1 10.6 44.8 4.42 0.24 씸 Female-speci ic linkage g oups 씹 Male-speci ic linkage g oups a The a e age in e -ma ke dis ance is based on he sex-a e age map b o al au osomal linkage g oups BMC Genomics 2009, 10:1 h p://www.biomedcen al.com/1471-2164/10/1 Page 4 o 17 (page numbe no o ci a ion pu poses) The bes -posi ion linkage g oups (male-speci ic, M; sex-a e age, A; and emale-speci ic; F) in Kosambi cen imo gans o he Sibe ian jayFigu e 1 The bes -posi ion linkage g oups (male-speci ic, M; sex-a e age, A; and emale-speci ic; F) in Kosambi cen i- mo gans o he Sibe ian jay. The ma ke s in bold ace on a e amewo k loci wi h unambiguous ela i e posi ion be ween each o he . BMC Genomics 2009, 10:1 h p://www.biomedcen al.com/1471-2164/10/1 Page 5 o 17 (page numbe no o ci a ion pu poses) The amewo k linkage g oups (male-speci ic, M; sex-a e age, A; and emale-speci ic; F) in Kosambi cen imo gans o he Sibe- ian jayFigu e 2 The amewo k linkage g oups (male-speci ic, M; sex-a e age, A; and emale-speci ic; F) in Kosambi cen imo - gans o he Sibe ian jay. BMC Genomics 2009, 10:1 h p://www.biomedcen al.com/1471-2164/10/1 Page 6 o 17 (page numbe no o ci a ion pu poses) map (Figu e 2 and Table 1). We compa ed ecombina ion dis ances be ween adjacen amewo k ma ke s ha we e mapped on bo h he bes -posi ion map and he ame- wo k map and o e all he emale- o-male a io o he amewo k map was 1.23, sligh ly lowe han he a io o 1.28 obse ed abo e in he bes -posi ion map. Among he Z-linked mic osa elli es, all six ma ke s showed highly signi ican linkage be ween each o he wi h LODs > 37.0. This linkage g oup spanned 23.8 cM in he sex-a e age map, 48.9 cM in he male map and 10.6 cM in emale map, which co esponds o a emale- o-male a io o 0.22. The emale linkage map indica es he posi- ion and app oxima e ex en o a pseudoau osomal egion (PAR) om SJ069 o beyond SJ048. In emales, no ecom- bina ion was obse ed be ween SJ083 and SJ046 and no he e ozygosi y was obse ed o hese ma ke s; he e o e hey mus lie ou side he pseudoau osomal egion, sug- ges ing ha he pseudoau osomal bounda y lies be ween SJ048 and SJ046. As expec ed, he e is conside able di e - ence in male and emale ecombina ion a es o he pseu- doau osomal egion o he Z-ch omosome, wi h he male dis ance be ween SJ108 and SJ069 being 41.7 cM as com- pa ed o he emale dis ance o 5.1 cM. This inc eased sex- speci ic ecombina ion a e be ween he h ee pseudoau- osomal loci was simila o he obse a ions in he pseu- doau osomal egions o he mammalian sex ch omosomes, o example in humans [50], o ines [51] and bo ines [52]. In he sex-a e age map, he map densi y was 4.0 cM/ma ke among all Z-linked ma ke s and 3.3 cM/ma ke among he i e amewo k loci. Di e ences in ecombina ion a e be ween sexes In addi ion o a much sho e o al leng h o au osomal linkage maps in males han in emales, he maps allowed compa ison o meio ic ecombina ion a e be ween sexes. The sexes show signi ican di e ences in ecombina ion a es, bo h in gene al and o speci ic pai s o linked ma k- e s (Wilcoxon's signed- ank es , P = 0.037; Figu e 3 and Table 2). In he bes -posi ion map (Figu e 1), he p opo - ion o in e als in he au osomal linkage g oups ha demons a ed a highe ecombina ion ac ion in emales was 54.3%. Among all adjacen au osomal ma ke s he ecombina ion ac ion was 1.28 imes highe in emales han in he males. Howe e , he e we e excep ions o his in some LGs, and in some speci ic in e als wi hin LGs. Fo ins ance, LG7 and LG8 exhibi ed highe ecombina- ion ac ions in males han in emales (Table 2). The numbe o in e als ha show highe ecombina ion ac- ions in he male map ela i e o he emale map was less, bu no negligible (Figu e 3). When in es iga ing he dis- o ions o e he au osomal linkage g oups, wo o he nine linkage g oups showed signi ican (P < 0.05) di e - ence in ecombina ion a e be ween he sex-speci ic maps (Table 2). This was also obse ed when he o e all map leng h was in es iga ed o sex-speci ic di e ence. All in all, hese esul s sugges ha o e all ecombina ion is sig- ni ican ly supp essed in male meiosis as compa ed o emale meiosis. Compa a i e mapping The BLAST sea ches unde bo h se ings gene a ed he same se o signi ican hi s a 1e-10. We ound 25 homolo- gous (21.4%, 25/117) zeb a inch sequences using a c oss-species MEGABLAST sea ch in NCBI's zeb a inch genome da abase (Table 3). By BLAST sea ching using wo me hods, in o al 22 mapped (20.5%, 22/107) and h ee unlinked loci o which a homologous sequence could be iden i ied in chicken we e assigned o a ch omosomal loca ion in he chicken genome (Table 3). The 10 Sibe ian jay LGs co esponded o i e di e en au osomal and one Z ch omosome in chicken. Loci om he same Sibe ian jay LG ma ched sequences on a single chicken ch omo- some in he BLAST analysis (Figu e 4 and Table 3), wi h he excep ion o loci SJ039, SJ101 and SJ076 on he au o- somal LGs (LG1, LG2, and LG3, espec i ely) ha mapped o chicken ch omosome Z (GgaZ), whe eas he o he loci on hese LGs mapped o he chicken au osomes. Table 2: The Wilcoxon's signed- ank es esul s o ecombina ion ac ion ( θ ) be ween sexes wi h linkage g oups Linkage g oups NaA e age θ FbA e age θ Mc θ F/ θ MWilcoxon's signed- ank es (P)d LG1 28 0.071 0.055 1.29 0.174 LG2 26 0.085 0.054 1.57 0.046 * LG3 12 0.152 0.133 1.14 0.323 LG4 10 0.101 0.077 1.31 0.038 * LG5 7 0.127 0.110 1.15 0.687 LG6 5 0.178 0.126 1.41 0.192 LG7 2 0.115 0.145 0.79 0.5 LG8 1 0.09 0.18 0.5 - LG9 1 0.12 0.08 1.5 - To al au osomal 92 0.101 0.079 1.28 0.037 * LGZ 5 0.02 0.094 0.21 0.025* a numbe o in e als; b a e age ecombina ion ac ion in emales; c a e age ecombina ion ac ions in males; d *, signi ican , P < 0.05. BMC Genomics 2009, 10:1 h p://www.biomedcen al.com/1471-2164/10/1 Page 7 o 17 (page numbe no o ci a ion pu poses) Likewise, mos loci on he same chicken ch omosome ma ched sequences on a single Sibe ian jay LG, wi h he excep ions o h ee unlinked loci (SJ005, SJ020 and SJ034) and loci SJ009, SJ039, SJ101 and SJ076 on GgaZ ha mapped o ou di e en LGs, LGZ and LG1, LG2, and LG3, espec i ely. The ela i e o de o he ma ke s mapped o he Sibe ian jay LGs was compa ed wi h he same loci on chicken ch o- mosomes in Figu e 4. The chicken-Sibe ian jay compa i- son indica ed ha he o de o loci was s ikingly di e en be ween he chicken mac och omosomes Gga1, Gga2 and Sibe ian jay LG1, LG2 in he bes -posi ion map, espec- i ely. Al hough some loci sha ed he same ela i e o de in he wo species, la ge ea angemen s o he ch omo- some would ha e been necessa y o gi e ise o he di e - en o de s ound he e. The cases o in e - and in a- ch omosomal ea angemen s we e in ol ed mos ly in he amewo k loci and ep esen ed a la ge p opo ion o Gga-LG1 ha spanned a ound a 120-cM Sibe ian jay/20- Mb chicken in e al. The h ee unlinked loci, SJ005, SJ020, and SJ034, we e loca ed a he dis al ends o wo chicken mac och omosomes, Gga1 and Gga2. Discussion This s udy cons i u es he i s mapping e o o he Sibe- ian jay genome, and is among he i s ones o p esen a p elimina y linkage map o any en i ely na u al e e- b a e species om he wild ( e iewed in [28]). The linkage map was composed using 107 polymo phic mic osa elli e loci yped on ca. 350 animals, making i one o he mos de ailed linkage maps a ailable o na u al animal popu- Female s. male ecombina ion ac ion o 97 pai s o adjacen ma ke s om he 10 linkage g oups in he Sibe ian jayFigu e 3 Female s. male ecombina ion ac ion o 97 pai s o adjacen ma ke s om he 10 linkage g oups in he Sibe ian jay. BMC Genomics 2009, 10:1 h p://www.biomedcen al.com/1471-2164/10/1 Page 8 o 17 (page numbe no o ci a ion pu poses) la ions [28]. In ac , i is one o only a ew gene ic linkage maps o wild bi d species o da e. Apa om he e ealing e idence o sex di e ences in ecombina ion a es, he cons uc ed maps ep esen an excellen esou ce om which he ma ke s may be selec ed o u u e mapping p ojec s in his and ela ed species, as well as o compa - a i e genomic s udies o genome o ganisa ion. In wha ollows, we will discuss he salien ea u es o he con- s uc ed linkage maps in compa ison o simila maps and esul s om ea lie s udies. In pa icula , we will pay a en ion o sex-speci ic di e ences in ecombina ion a es, map co e age and some o he issues dese ing u u e a en ion. Geno yping in he mapping popula ion The cons uc ed map con ains 107 mic osa elli es, o which 101 a e au osomal, h ee Z-ch omosome-speci ic and h ee pseudoau osomal loci (see below). The ideal se o molecula ma ke da a o linkage mapping has no missing alues, no geno yping e o s and he ma ke s seg- ega e in he expec ed a io o he speci ic ype o popula- ion [53]. In p ac ice, howe e , mapping da a is comp omised in all o hese espec s. Howe e , as simu- la ed and concluded in p e ious esea ch [53], he e ec o missing geno ypes depends g ea ly on he sample size: he smalle he sample, he mo e se e e he e ec s a e likely o be. In compa ison o published simula ions, in Table 3: The homologous loci o mic osa elli es mapped in Sibe ian jay on he chicken and zeb a inch genome assigned using BLAST analyses o he clone sequences o he mic osa elli es and he homologous zeb a inch WGS sequences. Locus Linkage g oup Zeb a inch Ensemble ID Chicken Ensemble ID Gga aChicken genome s a posi ion (bp) SJ010 LG1 gb|AC188472.1 NW_001471554.1 Gga1_WGA51_2b1 9,129,918 SJ016 LG1 - NW_001471545.1 Gga1_WGA43_2b1 9,256,107 SJ022 LG1 - NW_001471526.1 Gga1_WGA26_2b1 2,462,620 SJ025 LG1 gb|AC188472.1 NW_001471534.1 Gga1_WGA33_2b1 20,407,077 SJ057 LG1 - NW_001471554.1 Gga1_WGA51_2b1 7,801,901 SJ094 LG1 - NW_001471554.1 Gga1_WGA51_2b1 22,042,793 SJ113 LG1 - NW_001471545.1 Gga1_WGA43_2b1 8,757,200 SJ020 unlinked - NW_001471529.1 Gga1_WGA29_2b1 1,098,266 SJ005 unlinked gb|AC188184.3 NW_001471513.1 Gga1_WGA14_2c1 2,080,202 SJ036 LG2 - NW_001471639.1 Gga2_WGA66_2b2 20,469,429 SJ072 LG2 - NW_001471633.1 Gga2_WGA60_2b2 32,273,874 CK.1B5D LG2 gb|AC225878.2 NW_001471639.1 Gga2_WGA66_2b2 23,539,833 SJ026 LG2 gb|AC206427.2 NW_001471639.1 Gga2_WGA66_2c2 21,465,630 SJ054 LG2 gb|AC188186.2 NW_001471633.1 Gga2_WGA60_2c2 6,229,425 SJ116 LG2 gb|AC148379.2 NW_001471633.1 Gga2_WGA60_2c2 22,279,892 SJ034 unlinked - NW_001471654.1 Gga2_WGA81_2b2 2,075,856 SJ015 LG3 gb|AC188188.2 NW_001471673.1 Gga3_WGA106_2c3 3,458,567 SJ032 LG7 - NW_001471681.1 Gga4_WGA107_2b4 8,679,773 SJ087 LG7 gb|AC155211.2 NW_001471681.1 Gga4_WGA107_2c4 4,015,500 SJ117 LG7 - NW_001471681.1 Gga4_WGA107_2b4 8,679,607 SJ049 LG4 - NW_001471710.1 Gga5_WGA136_2b5 9,314,084 SJ009 LGZ - NW_001488876.1 GgaZ_WGA457_2bZ 1,412,682 SJ101 LG2 gb|AC213969.2 NW_001488849.1 GgaZ_WGA430_2bZ 1,097,987 SJ039 LG1 gb|AC231254.2 NW_001488882.1 GgaZ_WGA463_2cZ 1,315,022 SJ076 LG3 gb|AC188376.1 NW_001488862.1 GgaZ_WGA443_2cZ825,441 SJ050 LG1 gb|AC189030.1 - - - SJ051 LG1 gb|AC189030.1 - - - SJ055 LG1 gb|AC189030.1 - - - SJ064 LG1 gb|AC206426.2 - - - SJ112 LG1 gb|AC192320.2 - - - CK.2A5A LG1 gb|AC188469.1 - - - SJ029 LG4 gb|AC188184.3 - - - SJ033 LG4 gb|AC188469.1 - - - SJ106 LG4 gb|AC188184.3 - - - SJ017 LG5 gb|AC192320.2 - - - SJ041 LG9 gb|AC210531.1 - - - SJ069 LGZ gb|AC188466.2 - - - SJ083 LGZ gb|AC229626.2 - - - a Chicken ch omosome numbe ; b Via he clone sequences o he Sibe ian jay mic osa elli es; c Via he homologous zeb a inch WGS sequences BMC Genomics 2009, 10:1 h p://www.biomedcen al.com/1471-2164/10/1 Page 9 o 17 (page numbe no o ci a ion pu poses) Compa ison o he whole o all sex-a e age linkage g oups in he Sibe ian jay and he whole o chicken ch omosomesFigu e 4 Compa ison o he whole o all sex-a e age linkage g oups in he Sibe ian jay and he whole o chicken ch o- mosomes. The homologous loci on linkage g oups and ch omosomes a e p esen ed wi h hei gene ic posi ions (cM) on he bes -posi ion map o hei genomic loca ions (Mb) in he chicken genome. Sibe ian Jay ma ke names in bold on indica e amewo k loci. BMC Genomics 2009, 10:1 h p://www.biomedcen al.com/1471-2164/10/1 Page 16 o 17 (page numbe no o ci a ion pu poses) 37. Ekman J, Bylin A, Teges öm H: Inc eased li e ime ep oduc i e success o Sibe ian jay (Pe iso eus in aus us) males wi h delayed dispe sal. P oceedings o he Royal Socie y B: Biological Sci- ences 1999, 266:911-915. 38. Ekman J, Baglione V, Egge s S, G iesse M: Delayed dispe sal: li ing unde he egion o nepo is ic pa en s. Auk 2001, 118:1-10. 39. G iesse M, Ekman J: Nepo is ic ala m calling in Sibe ian jay, Pe iso eus in aus us. Animal Beha iou 2004, 67:933-939. 40. Lilland BG, Bensch S, on Schan z T: Family s uc u e in he Sibe ian jay as e ealed by mic osa elli e analyses. Condo 2003, 105:505-514. 41. Egge s S, G iesse M, Ekman J: P eda o -induced plas ici y in nes isi a ion a es in he Sibe ian jay (Pe iso eus in aus us). Beha io al Biology 2004, 16:309-315. 42. Alho JS, Lilland BG, Jaa i S, Me ilä J: Mul ilocus he e ozygosi y and inb eeding in he Sibe ian jay. Conse a ion Gene ics 2009. 43. Fede M, Mi chell-Olds T: E olu iona y and ecological unc- ional genomics. Na u e Re iews Gene ics 2003, 4:651-657. 44. Jaa i S, Välimäki K, Me ilä J: Isola ion and cha ac e iza ion o 100 mic osa elli e p ime s o he Sibe ian jay (Pe iso eus in aus- us). Molecula Ecology Resou ces 2008, 8:1469-1474. 45. In e na ional Chicken Genome Sequencing Conso ium: Sequenc- ing and compa a i e analysis o he chicken genome p o ide unique pe spec i es on e eb a e e olu ion. Na u e 2004, 432:695-716. 46. an Tuinen M, Sibley CG, Hedges SB: The ea ly his o y o mode n bi ds in e ed om DNA sequences o nuclea and mi o- chond ial ibosomal genes. Molecula Biology and E olu ion 2000, 17:451-457. 47. Ba ke FK, Ba owclough GF, G o h JG: A phylogene ic hypo he- sis o passe ine bi ds: axonomic and biogeog aphic impli- ca ions o an analysis o nuclea DNA sequence da a. P oceedings o he Royal Socie y B: Biological Sciences 2002, 269:295-308. 48. T eplin S: In e ence o phylogene ic ela ionships in passe ine bi ds (A es: Passe i o mes) using new molecula ma ke s. In PhD hesis The Uni e si y o Po sdam; 2006. 49. Singe A, Pe lman H, Yan Y, Walke C, Co ley-Smi h G, B andho s B, Pos le hwai J: Sex-speci ic ecombina ion a es in zeb a ish (Danio e io). Gene ics 2002, 160:649-657. 50. Schmi K, Lazze oni LC, Foo e S, Voll a h D, Fishe EM, Go adia TM, Lange K, Page DC, A nheim N: Mul ipoin linkage map o he human pseudoau osomal egion based on single-spe m yp- ing: do double c osso e s occu du ing male meiosis? Ame i- can Jou nal o Human Gene ics 1994, 55:423-430. 51. Galloway SM, Han ahan V, Dodds KG, Po s MD, C aw o d AM, Hill DF: A linkage map o he o ine X ch omosome. Genome Resea ch 1996, 6:667-677. 52. Sons ega d TS, Lopez-Co ales NL, Kappes SM, S one RT, Ambady S, Ponce de León FA, Bea ie CW: An in eg a ed gene ic and phys- ical map o he bo ine X ch omosome. Mammalian Genome 1997, 8:16-20. 53. Hacke CA, B oad oo LB: E ec s o geno yping e o s, missing alues and seg ega ion dis o ion in molecula ma ke da a on he cons uc ion o linkage maps. He edi y 2003, 90:33-38. 54. G oenen MA, Cheng HH, Bums ead N, Benkel BF, B iles WE, Bu ke T, Bu DW, C i enden LB, Dodgson J, Hillel J, Lamon S, de Leon AP, Solle M, Takahashi H, Vignal A: A consensus linkage map o he chicken genome. Genome Resea ch 2000, 10:137-147. 55. P imme CR, Raudsepp T, Chowdha y BP, Mølle AP, Elleg en H: Low equency o mic osa elli es in he a ian genome. Genome Resea ch 1997, 7:471-482. 56. G oenen MA, C ooijmans RP, Veenendaal A, Cheng HH, Siwek M, Poel JJ an de : A comp ehensi e mic osa elli e linkage map o he chicken genome. Genomics 1998, 49:265-274. 57. Ne MW, B oman KW, Melle sh CS, Ray K, Acland GM, Agui e GD, Ziegle JS, Os ande EA, Rine J: A second-gene a ion gene ic linkage map o he domes ic dog, Canis amilia is. Gene ics 1999, 151:803-820. 58. Kayang BB, Vignal A, Inoue-Mu ayama M, Miwa M, Mon oisin JL, I o S, Min ielle F: A i s -gene a ion mic osa elli e linkage map o he Japanese quail. Animal Gene ics 2004, 35:195-200. 59. May B, Johnson KR: Composi ion linkage map o salmonid ishes (Sal elinus, Salmo and Onco hynchus). In Gene ic Maps: Locus Maps o Complex Genomes Edi ed by: O'B ien SJ. New Yo k: Cold Sp ing Ha bo ; 1990:151-159. 60. Young WP, Wheele PA, Co yell VH, Keim P, Tho gaa d GH: A de ailed linkage map o ainbow ou p oduced using dou- ble haploids. Gene ics 1998, 148:839-850. 61. Sons ega d TS, Ba endse W, Benne GL, B ockmann GA, Da is S, D oegemulle C, Kalm E, Kappes SM, Kühn C, Li Y, Schwe in M, Tay- lo J, Thomsen H, an Tassell CP, Yeh CC: Consensus and com- p ehensi e linkage maps o he bo ine sex ch omosomes. Animal Gene ics 2001, 32:105-121. 62. Maddox JF, Da ies KP, C aw o d AM, Hulme DJ, Vaiman D, C ibiu EP, F eking BA, Beh KJ, Cocke NE, Kang N, Ri kin CD, D inkwa e R, Moo e SS, Dodds KG, Lumsden JM, an S ijn TC, Phua SH, Adelson DL, Bu kin HR, B oom JE, Bui kamp J, Camb idge L, Cushwa WT, Ge a d E, Galloway SM, Ha ison B, Hawken RJ, Hiendlede S, Hen y HM, Med ano JF, Pa e son KA, Schible L, S one RT, an Hes B: An enhanced linkage map o he sheep genome comp ising mo e han 1000 loci. Genome Resea ch 2001, 11:1275-1289. 63. Hube S, Hedgecock D: Linkage Maps o Mic osa elli e DNA Ma ke s o he Paci ic Oys e C assos ea gigas. Gene ics 2004, 168:351-362. 64. Ma ise TC, Chen F, Chen W, De La Vega FM, Hansen M, He C, Hyland FC, Kennedy GC, Kong X, Mu ay SS, Ziegle JS, S ewa WC, Buyske S: A second-gene a ion combined linkage physical map o he human genome. Genome Resea ch 2007, 17:1783-1786. 65. Handley LJ, Cepli is H, Elleg en H: E olu iona y s a a on he chicken Z ch omosome: implica ion o sex ch omosome e olu ion. Gene ics 2004, 167:367-376. 66. Sunds öm H, Webs e MT, Elleg en H: Reduced a ia ion on he chicken Z ch omosome. Gene ics 2004, 167:377-385. 67. Elleg en H, Hul in-Rosenbe g L, B uns öm B, Dencke L, Kul ima K, Scholz B: Faced wi h inequali y: chicken do no ha e a gene al dosage compensa ion o sex-linked genes. BMC Biology 2007, 5:40. 68. S o cho á R, Di ina P: Non- andom ep esen a ion o sex- biased genes on chicken Z ch omosome. Jou nal o Molecula E olu ion 2006, 63:676-681. 69. B oman KW, Rowe LB, Chu chill GA, Paigen K: C osso e in e - e ence in he mouse. Gene ics 2002, 160:1123-1131. 70. Mon ell H, F idol sson AK, Elleg en H: Con as ing le els o nucleo ide di e si y on he a ian Z and W sex ch omo- somes. Molecula Biology and E olu ion 2001, 18:2010-2016. 71. Lynn A, Kashuk C, Pe e sen MB, Bailey JA, Cox DR, An ona akis SE, Chak a a i A: Pa e ns o meio ic ecombina ion on he long a m o human ch omosome 21. Genome Resea ch 2000, 10:1319-1332. 72. Solignac M, Mougel F, Vau in D, Monne o M, Co nue JM: A hi d- gene a ion mic osa elli e-based linkage map o he honey bee, Apis melli e a, and i s compa ison wi h he sequence- based physical map. Genome Biology 2007, 8:R66. 73. Zenge KR, McKenzie LM, Coope DW: The i s comp ehensi e gene ic map o a ma supial: he amma wallaby (Mac opus eugenii). Gene ics 2002, 162:321-330. 74. Samollow PB, Kamme e CM, Mahaney SM, Schneide JL, Wes en- be ge SJ, VandeBe g JL, Robinson ES: Fi s -gene a ion linkage map o he g ay, sho - ailed opossum, Monodelphis domes- ica, e eals genome-wide educ ion in emale ecombina- ion a es. Gene ics 2004, 166:307-329. 75. Kai W, Kikuchi K, Fuji a M, Sue ake H, Fujiwa a A, Yoshiu a Y, O o- ake M, Venka esh B, Miyaki K, Suzuki Y: A gene ic map o he ige pu e ish, Taki ugu ub ipes. Gene ics 2005, 171:227-238. 76. Bouza C, He mida M, Pa do BG, Fe nández C, Fo es GG, Cas o J, Sánchez L, P esa P, Pé ez M, Sanjuán A, de Ca los A, Al a ez-Dios JA, Ezcu a S, Cal RM, Pi e e F, Ma ínez P: A mic osa elli e gene ic map o he u bo (Scoph halmus maximus). Gene ics 2007, 177:2457-2467. 77. Sekino M, Ha a M: Linkage maps o he Paci ic Abalone (Genus halio is) based on mic osa elli e DNA ma ke s. Gene ics 2007, 175:945-958. 78. A chibald AL, Haley CS, B own JF, Coupe whi e S, McQueen HA, Nicholson D, Coppie e s W, Weghe A Van de, S a il A, Win e ø AK, e al.: The PiGMap conso ium linkage map o he pig (Sus sc o a). Mammalian Genome 1995, 6:157-175. 79. Kappes SM, Keele JW, S one RT, McG aw RA, Sons ega d TS, Smi h TP, Lopez-Co ales NL, Bea ie CW: A second-gene a ion link- age map o he bo ine genome. Genome Resea ch 1997, 7:235-249. Publish wi h BioMed Cen al and e e y scien is can ead you wo k ee o cha ge "BioMed Cen al will be he mos signi ican de elopmen o dissemina ing he esul s o biomedical esea ch in ou li e ime." Si Paul Nu se, Cance Resea ch UK You esea ch pape s will be: a ailable ee o cha ge o he en i e biomedical communi y pee e iewed and published immedia ely upon accep ance ci ed in PubMed and a chi ed on PubMed Cen al you s — you keep he copy igh Submi you manusc ip he e: h p://www.biomedcen al.com/in o/publishing_ad .asp BioMedcen al BMC Genomics 2009, 10:1 h p://www.biomedcen al.com/1471-2164/10/1 Page 17 o 17 (page numbe no o ci a ion pu poses) 80. D acopoli NC, O'Connell P, Elsne TI, Lalouel JM, Whi e RL, Bue ow KH, Nishimu a DY, Mu ay JC, Helms C, Mish a SK, e al.: The CEPH conso ium linkage map o human ch omosome 1. Genomics 1991, 9:686-700. 81. S auss M, Tomiuk J, Segelbache G, D iesel S, Fie z J, Bachmann L, Kömp J: Sex-speci ic ecombina ion a es in Pa us majo and P. cae uleus, an excep ion o Huxley's ule. He edi as 2003, 139:199-205. 82. Haldane JBS: Sex a io and unisexual s e ili y in hyb id ani- mals. Jou nal o Gene ics 1922, 12:101-109. 83. T i e s R: Sex di e ences in a es o ecombina ion and sex- ual selec ion. In The E olu ion o Sex Edi ed by: Michob R, Le in B. Sunde land: Sinaue Associa es; 1988:270-286. 84. Sheldon BC, Me ilä J, Q a ns öm A, Elleg en H: Female gene ic bene i om ex a-pai copula ion p edic ed by ela i e size o male seconda y sexual cha ac e . P oceedings o he Royal Soci- e y B: Biological Sciences 1997, 264:297-302. 85. Hou man AM: Female zeb a inches choose ex a-pai copula- ions wi h gene ically a ac i e males. P oceedings o he Royal Socie y B: Biological Sciences 1992, 249:3-6. 86. Leno mand T, Du heil J: Recombina ion di e ence be ween sexes: a ole o haploid selec ion. PLoS Biology 2005, 3:e63. 87. Glazie AM, Nadeau JH, Ai man TJ: Finding genes ha unde line complex ai s. Science 2002, 298:2345-2349. 88. I oh Y, A nold AP: Ch omosomal polymo phism and compa - a i e pain ing analysis in he zeb a inch. Ch omosome Resea ch 2005, 13:47-53. 89. C amp S, Pe ins CM: The Bi ds o he Wes e n Palea c ic Volume VIII. Ox o d: Ox o d Uni e si y P ess; 1994. 90. Helle P, Lilland BG: Sibe ian jay. In The Eu opean bi d census council a las o Eu opean b eeding bi ds: hei dis ibu ion and abundance Edi ed by: Hagemeije WJM, Blai MJ. London: T & AD Poyse ; 1997:669. 91. Uimaniemi L, O ell M, Mönkkönen M, Huh a E, Jokimäki J, Lumme J: Gene ic di e si y in he Sibe ian jay Pe iso eus in aus us in agmen ed old-g ow h o es s o Fennoscandia. Ecog aphy 2000, 23:669-677. 92. Ekman J, Egge s S, G iesse M: Figh ing o s ay: he ole o sibling i al y o delayed dispe sal. Animal Beha iou 2002, 64:453-459. 93. Lilland BG, Bensch S, on Schan z T: Pa en age de e mina ion in kin-s uc u ed popula ions: mic osa elli e analyses in he Sibe ian jay Pe iso eus in aus us du ing a 25-yea popula ion s udy. A ian Science 2001, 1:3-14. 94. De jushe a S, Ku gano a A, Habe mann F, Gaginskaya E: High ch o- mosome conse a ion de ec ed by compa a i e ch omo- some pain ing in chicken, pigeon and passe ine bi ds. Ch omosome Resea ch 2004, 12:715-723. 95. Pigozzi MI, Sola i AJ: Ge m cell es ic ion and egula ans- mission o an accesso y ch omosome ha mimics a sex body in he zeb a inch, Taeniopygia gu a a. Ch omosome Resea ch 1998, 6:105-113. 96. Sunds öm H, Webs e MT, Elleg en H: Is he a e o inse ion and dele ion mu a ion male biased?: Molecula e olu iona y analysis o a ian and p ima e sex ch omosome sequences. Gene ics 2003, 164:259-268. 97. Lilland BG: La sk ikans (Pe iso eus in aus us) popula ion- su eckling inom e sammanhängande skogsom åde i Sydös e bo en 1974–1992. MSc Thesis, Uni e si y o Helsinki 1993. 98. G iesse M: Nepo is ic igilance beha iou o Sibe ian jay pa - en s. Beha io al Ecology 2003, 14:246-250. 99. G een P, Falls K, C ooks S: Documen a ion o CRI-MAP e sion 2.4 S . Louis: Washing on Uni e si y School o Medicine; 1990. 100. Nei M: Molecula E olu iona y Gene ics New Yo k: Columbia Uni e si y P ess; 1987. 101. Pa k SDE: T ypano ole ance in Wes A ican Ca le and he Popula ion Gene ic E ec s o Selec ion. In PhD hesis Uni e si y o Dublin; 2001. 102. Voo ips RE: MapCha : so wa e o he g aphical p esen a- ion o linkage maps and QTLs. Jou nal o He edi y 2002, 93:77-78.