Laboratorio de Ecología y Comportamiento Animal, Depto. Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires e IEGEBA (UBA–CONICET). Piso 4, Pab. 2, Ciudad Universitaria, C1428EHA Buenos Aires, Argentina.
Next-generation sequencing techniques have changed the way of obtaining genetic data for studies in avian conservation, from the analysis of a few loci located in a small portion of the genome to obtaining information from hundreds to thousands of loci distributed all over the genome. A larger number of markers provides more information for phylogenetic, introgression and population structure studies, and allows a better estimation of demographic parameters. Measures such as heterozygosity, parentage, paternity and inbreeding can be estimated more accurately. In addition, one of the greatest contributions of genomic studies is the identification of both adaptive and neutral variation. In this paper I briefly explain the methodological basis of next-generation sequencing and show examples of the use of genomic data in conservation studies in birds.
ALLENDORF FW (2017) Genetics and the conservation of natural populations: allozymes to genomes. Molecular Ecology 26:420–430
ANDERSEN MJ, MANTHEY JD, NAIKATINI A Y MOYLE RG (2017) Conservation genomics of the silktail (Aves: Lamprolia victoriae) suggests the need for increased protection of native forest on the Natewa Peninsula, Fiji. Conservation Genetics 18:1277–1285
ANDREW SC, TAYLOR MP, LUNDREGAN S, LIEN S, JENSEN H Y GRIFFITH SC (en prensa) Signs of adaptation to trace metal contamination in a common urban bird. Science of the Total Environment
BAIRD NA, ETTER PD, ATWOOD TS, CURREY MC, SHIVER AL, LEWIS ZA, SELKER EU, CRESKO WA Y JOHNSON EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PloS One 3:e3376
BALL AD, STAPLEY J, DAWSON DA, BIRKHEAD TR, BURKE T Y SLATE J (2010) A comparison of SNPs and microsatellites as linkage mapping markers: lessons from the zebra finch (Taeniopygia guttata). BMC Genomics 11:art218
BATTEY CJ, LINCK EB, EPPERLY KL, FRENCH C, SLAGER DL, SYKES PW Y KLICKA J (2017) A migratory divide in the Painted Bunting (Passerina ciris). American Naturalist 191:259–268
BOUZAT JL (2010) Conservation genetics of population bottlenecks: the role of chance, selection and history. Conservation Genetics 11:463–478
BULGARELLA M, KOPUCHIAN C, DI GIACOMO AS, MATUS R, BLANK O, WILSON RE Y MCCRACKEN KG (2014) Molecular phylogeny of the South American sheldgeese with implications for conservation of Falkland Islands (Malvinas) and continental populations of the Ruddy-headed Goose Chloephaga rubidiceps and Upland Goose C. picta. Bird Conservation International 24:59–71
CAMPAGNA L, GRONAU I, SILVEIRA LF, SIEPEL A Y LOVETTE IJ (2015) Distinguishing noise from signal in patterns of genomic divergence in a highly polymorphic avian radiation. Molecular Ecology 24:4238–4251
CAMPAGNA L, REPENNING M, SILVEIRA LF, SUERTEGARAY FONTANA C, TUBARO PL & LOVETTE IJ (2017) Repeated divergent selection on pigmentation genes in a rapid finch radiation. Science Advances 3:art1602404
CHARLESWORTH B (2001) The effect of life-history and mode of inheritance on neutral genetic variability. Genetical Research 77:153–166
DAVEY JW, HOHENLOHE PA, ETTER PD, BOONE JQ, CATCHEN JM Y BLAXTER ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nature Reviews Genetics 12:499–510
DESAIX MG, BULLUCK LP, ECKERT AJ, VIVERETTE CB, BOVES TJ, REESE JA, TONRA CM Y DYER RJ (en prensa) Population assignment reveals low migratory connectivity in a weakly structured songbird. Molecular Ecology
DOMÍNGUEZ M, PIZZARELLO G, ATENCIO M, SCARDAMAGLIA R Y MAHLER B (en prensa) Genetic assignment and monitoring of yellow cardinals. Journal of Wildlife Management
DOYLE JM, BELL DA, BLOOM PH, EMMONS G, FESNOCK A, KATZNER TE, LAPRÉ L, LEONARD K, SAN MIGUEL P, WESTERMAN R Y DEWOODY JA (2018) New insights into the phylogenetics and population structure of the prairie falcon (Falco mexicanus). BMC Genomics 19:art233
ELGVIN TO, TRIER CN, TØRRESEN OK, HAGEN IJ, LIEN S, NEDERBRAGT AJ, RAVINET M, JENSEN H Y SÆTRE GP (2017) The genomic mosaicism of hybrid speciation. Science Advances 3:art1602996
ELLEGREN H (2010) Evolutionary stasis: the stable chromosomes of birds. Trends in Ecology and Evolution 25:283–291
ELLEGREN H (2013) The evolutionary genomics of birds. Annual Review of Ecology, Evolution and Systematics 44:239–259
ELLEGREN H (2014) Genome sequencing and population genomics in non-model organisms. Trends in Ecology and Evolution 29:51–63
ELSHIRE RJ, GLAUBITZ JC, SUN Q, POLAND JA, KAWAMOTO K, BUCKLER ES Y MITCHELL SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379
EÖRY L, GILBERT MT, LI C, LI B, ARCHIBALD A, AKEN BL, ZHANG G, JARVIS E, FLICEK P Y BURT DW (2015) Avianbase: a community resource for bird genomics. Genome Biology 16:art21
FEDER JL, EGAN SP Y NOSIL P (2012) The genomics of speciation-with-gene-flow. Trends in Genetics 28:342–350
FERNANDES G Y CAPARROZ R (2013) DNA sequence analysis to guide the release of blue and yellow macaws (Ara ararauna, Psittaciformes, Aves) from the illegal trade back to the wild. Molecular Biology Reports 40:2757–2762
FRANKHAM R (1995) Conservation genetics. Annual Review of Genetics 29:305–327
FRANKHAM R (2005) Stress and adaptation in conservation genetics. Journal of Evolutionary Biology 18:750–755
FRANKHAM R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biological Conservation 143:1919–1927
FRANKHAM R, BALLOU JD, ELDRIDGE MDB, LACY RC, RALLS K, DUDASH MR Y FENSTER CB (2011) Predicting the probability of outbreeding depression. Conservation Biology 25:465–475
FRASER DJ Y BERNATCHEZ L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology 10:2741–2752
FUENTES-PARDO AP Y RUZZANTE DE (2017) Whole-genome sequencing approaches for conservation biology: advantages, limitations and practical recommendations. Molecular Ecology 26:5369–5406
FUNK WC, MCKAY JK, HOHENLOHE PA Y ALLENDORF FW (2012) Harnessing genomics for delineating conservation units. Trends in Ecology and Evolution 27:489–496
GALLA SJ, FORSDICK NJ, BROWN L, HOEPPNER MP, KNAPP M, MALONEY RF, MORAGA R, SANTURE AW Y STEEVES TE (en prensa) Reference genomes from distantly related species can be used for discovery of single nucleotide polymorphisms to inform conservation management. Genes
GILLIGAN DM, BRISCOE DA Y FRANKHAM R (2005) Comparative losses of quantitative and molecular genetic variation in finite populations of Drosophila melanogaster. Genetical Research 85:47–55
GOMULKIEWICZ R Y HOLT RD (2006) When does evolution by natural selection prevent extinction? Evolution 49:201–207
GOODWIN S, MCPHERSON JD Y MCCOMBIE WR (2016) Coming of age: ten years of next-generation sequencing technologies. Nature Reviews Genetics 17:333–351
GREGORY TR (2005) Synergy between sequence and size in large-scale genomics. Nature Reviews Genetics 6:699–708
GROHME MA, FRIAS SOLER R, WINK M Y FROHME M (2013) Microsatellite marker discovery using single molecule real-time circular consensus sequencing on the Pacific Biosciences RS. BioTechniques 55:253–256
HARTMANN SA, SCHAEFER HM Y SEGELBACHER G (2014) Development of 12 microsatellite loci for the endangered Pale-headed Brushfinch (Atlapetes pallidiceps) and their cross-amplification in two co-occurring brushfinches. Journal of Ornithology 155:835–839
HARVEY MG, SMITH BT, GLENN TC, FAIRCLOTH BC Y BRUMFIELD RT (2016) Sequence capture versus restriction site associated DNA sequencing for shallow systematics. Systematic Biology 65:910–924
HEDRICK PW (2001) Conservation genetics: where are we now? Trends in Ecology and Evolution 16:629–636
HOBAN S, KELLEY JL, LOTTERHOS KE, ANTOLIN MF, BRADBURD G, LOWRY DB, POSS ML, REED LK, STORFER A Y WHITLOCK MC (2016) Finding the genomic basis of local adaptation: pitfalls, practical solutions and future directions. American Naturalist 188:379–397
IUCN SPECIES SURVIVAL COMMISSION (2013) Guidelines for reintroductions and other conservation translocations. Version 1.0. IUCN, Gland
KAISER SA, TAYLOR SA, CHEN N, SILLETT TS, BONDRA ER Y WEBSTER MS (2017) A comparative assessment of SNP and microsatellite markers for assigning parentage in a socially monogamous bird. Molecular Ecology Resources 17:183–193
KAWECKI TJ Y EBERT D (2004) Conceptual issues in local adaptation. Ecology Letters 7:1225–1241
KIIALAINEN A, KARLBERG O, AHLFORD A, SIGURDSSON S, LINDBLAD-TOH K Y SYVÄNEN AC (2011) Performance of microarray and liquid based capture methods for target enrichment for massively parallel sequencing and SNP discovery. PLoS One 6:e16486
KLICKA LB, KUS BE, TITLE PO Y BURNS KJ (2016) Conservation genomics reveals multiple evolutionary units within Bell’s Vireo (Vireo bellii). Conservation Genetics 17:455–471
KOHN MH, MURPHY WJ, OSTRANDER EA Y WAYNE RK (2006) Genomics and conservation genetics. Trends in Ecology and Evolution 21:629–637
KOPUCHIAN C, CAMPAGNA L, DI GIACOMO AS, WILSON RE, BULGARELLA M, PETRACCI P, MAZAR BARNETT J, MATUS R, BLANK O Y MCCRACKEN KG (2016) Demographic history inferred from genome-wide data reveals two lineages of sheldgeese endemic to a glacial refugium in the southern Atlantic. Journal of Biogeography 43:1979–1989
LABUSCHAGNE C, NUPEN L, KOTZÉ A, GROBLER PJ Y DALTON DL (2015) Assessment of microsatellite and SNP markers for parentage assignment in ex situ African Penguin (Spheniscus demersus) populations. Ecology and Evolution 5:4389–4399
LACY RC (1994) Managing genetic diversity in captive populations of animals. Pp. 63–89 en: BOWLES ML Y WHELAN CJ (eds) Restoration and recovery of endangered plants and animals. Cambridge University Press, Cambridge
LANGIN KM, ALDRIDGE CL, FIKE JA, CORNMAN RS, MARTIN K, WANN GT, SEGLUND AE, SCHROEDER MA, BRAUN CE, BENSON DP, FEDY BC, YOUNG JR, WILSON S, WOLFE DH Y OYLER-MCCANCE SJ (2018) Characterizing range-wide divergence in an alpine-endemic bird: a comparison of genetic and genomic approaches. Conservation Genetics 19:1471–1485
LEE L, TIRRELL N, BURRELL C, CHAMBERS S, VOGEL S Y DOMYAN ET (2018) Genetic tests reveal extra-pair paternity among Gentoo penguins (Pygoscelis papua ellsworthii) at Loveland Living Planet Aquarium: implications for ex situ colony management. Zoo Biology 37:236–244
MACE GM (2004) The role of taxonomy in species conservation. Philosophical Transactions of the Royal Society of London B 359:711–719
MARRA PP, COHEN EB, LOSS SR, RUTTER JE Y TONRA CM (2015) A call for full annual cycle research in animal ecology. Biology Letters 11:art20150552
MARTIN-WINTLE MS, WINTLE NJP, DÍEZ-LEÓN M, SWAISGOOD RR Y ASA CS (en prensa) Improving the sustainability of ex situ populations with mate choice. Zoo Biology
MCMAHON BJ, TEELING EC Y HÖGLUND J (2014) How and why should we implement genomics into conservation? Evolutionary Applications 7:999–1007
MEIRMANS PG (2015) Seven common mistakes in population genetics and how to avoid them. Molecular Ecology 24:3223–3231
NARUM SR, BUERKLE CA, DAVEY JW, MILLER MR Y HOHENLOHE PA (2013) Genotyping-by-sequencing in ecological and conservation genomics. Molecular Ecology 22:2841–2847
NG EYX, GARG KM, LOW GW, CHATTOPADHYAY B, OHR RY, LEE JGH Y RHEINDT FE (2017) Conservation genomics identifies impact of trade in a threatened songbird. Biological Conservation 214:101–108
NOOR MAF Y BENNETT SM (2009) Islands of speciation or mirages in the desert: examining the role of restricted recombination in maintaining species. Heredity 103:439–444
OUBORG NJ, PERTOLDI C, LOESCHCKE V, BIJLSMA RK Y HEDRICK PW (2010) Conservation genetics in transition to conservation genomics. Trends in Genetics 26:177–187
OYLER-MCCANCE SJ, OH KP, LANGIN KM Y ALDRIDGE CL (2016) A field ornithologist’s guide to genomics: practical considerations for ecology and conservation. Auk 133:626–648
OZSOLAK F Y MILOS PM (2011) RNA sequencing: advances, challenges and opportunities. Nature Reviews Genetics 12:87–98
PARIS JR, STEVENS JR Y CATCHEN JM (2017) Lost in parameter space: a road map for STACKS. Methods in Ecology and Evolution 8:1360–1373
PERTOLDI C, BIJLSMA R Y LOESCHCKE V (2007) Conservation genetics in a globally changing environment: present problems, paradoxes and future challenges. Biodiversity and Conservation 16:4147–4163
PETERS JL, LAVRETSKY P, DACOSTA JM, BIELEFELD RR, FEDDERSEN JC Y SORENSON MD (2016) Population genomic data delineate conservation units in mottled ducks (Anas fulvigula). Biological Conservation 203:272–281
PETERSON BK, WEBER JN, KAY EH, FISHER HS Y HOEKSTRA HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7:e37135
POELSTRA JW, VIJAY N, BOSSU CM, LANTZ H, RYLL B, MULLER I, BAGLIONE V, UNNEBERG P, WIKELSKI M, GRABHERR MG, UNNEBERG P & WOLF JBW (2014) The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science 344:1410–1414
PRATT D Y MITTERMEIER JC (2016) Notes on the natural history, taxonomy and conservation of the endemic avifauna of the Samoan Archipelago. Wilson Journal of Ornithology 128:217–241
PRIMMER CR, PAINTER JN, KOSKINEN MT, PALO JU Y MERILÄ J (2005) Factors affecting avian cross-species microsatellite amplification. Journal of Avian Biology 36:348–360
RUEGG KC, ANDERSON EC, PAXTON KL, APKENAS V, LAO S, SIEGEL RB, DESANTE DF, MOORE F Y SMITH TB (2014) Mapping migration in a songbird using high-resolution genetic markers. Molecular Ecology 23:5726–5739
RUEGG KC, BAY RA, ANDERSON EC, SARACCO JF, HARRIGAN RJ, WHITFIELD M, PAXTON EH Y SMITH TB (2018) Ecological genomics predicts climate vulnerability in an endangered southwestern songbird. Ecology Letters 21:1085–1096
RUNGE CA, MARTIN TG, POSSINGHAM HP, WILLIS SG Y FULLER RA (2014) Conserving mobile species. Frontiers in Ecology and the Environment 12:395–402
SANGER F, NICKLEN S Y COULSON AR (1977) DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences 74:5463–5467
SAVOLAINEN O, LASCOUX M Y MERILÄ J (2013) Ecological genomics of local adaptation. Nature Reviews Genetics 14:807–820
SHAFER ABA, WOLF JBW, ALVES PC, BERGSTRÖM L, BRUFORD MW, BRÄNNSTRÖM I, COLLING G, DALÉN L, DE MEESTER L, EKBLOM R, FAWCETT KD, FIOR S, HAJIBABAEI M, HILL JA, HOEZEL AR, HÖGLUND J, JENSEN EL, KRAUSE J, KRISTENSEN TN, KRÜTZEN M, MCKAY JK, NORMAN AJ, OGDEN R, ÖSTERLING EM, OUBORG NJ, PICCOLO J, POPOVIC D, PRIMMER CR, REED FA, ROUMET M, SALMONA J, SCHENEKAR T, SCHWARTZ MK, SEGELBACHER G, SENN H, THAULOW J, VALTONEN M, VEALE A, VERGEER P, VIJAY N, VILÀ C, WEISSENSTEINER M, WENNERSTRÖM L, WHEAT CW Y ZIELINSKI P (2015) Genomics and the challenging translation into conservation practice. Trends in Ecology and Evolution 30:78–87
STAPLEY J, REGER J, FEULNER PGD, SMADJA C, GALINDO J, EKBLOM R, BENNISON C, BALL AD, BECKERMAN AP Y SLATE J (2010) Adaptation genomics: the next generation. Trends in Ecology and Evolution 25:705–712
VAN STRAALEN NM Y ROELOFS D (2006) An introduction to ecological genomics. Oxford University Press, Oxford
TEER JK, BONNYCASTLE LL, CHINES PS, HANSEN NF, AOYAMA N, SWIFT AJ, ABAAN HO, ALBERT TJ, MARGULIES EH, GREEN ED, COLLINS FS, MULLIKIN JC Y BIESECKER LG (2010) Systematic comparison of three genomic enrichment methods for massively parallel DNA sequencing. Genome Research 20:1420–1431
THRASHER DJ, BUTCHER BG, CAMPAGNA L, WEBSTER MS Y LOVETTE IJ (2018) Double-digest RAD sequencing outperforms microsatellite loci at assigning paternity and estimating relatedness: a proof of concept in a highly promiscuous bird. Molecular Ecology Resources 18:953–965
TOEWS DPL, CAMPAGNA L, TAYLOR SA, BALAKRISHNAN CN, BALDASSARRE DT, DEANE-COE PE, HARVEY MG, HOOPER DM, IRWIN DE, JUDY CD, MASON NA, MCCORMACK JE, MCCRACKEN KG, OLIVEROS CH, SAFRAN RJ, SCORDATO ESC, STRYJEWSKI KF, TIGANO A, UY JAK Y WINGER BM (2015) Genomic approaches to understanding population divergence and speciation in birds. Auk 133:13–30
WEINMAN LR, SOLOMON JW Y RUBENSTEIN DR (2015) A comparison of single nucleotide polymorphism and microsatellite markers for analysis of parentage and kinship in a cooperatively breeding bird. Molecular Ecology Resources 15:502–511
WU CI (2001) The genic view of the process of speciation. Journal of Evolutionary Biology 14:851–865
ZHANG G, LI B, LI C, GILBERT MTP, JARVIS ED Y WANG J (2014a) Comparative genomic data of the Avian Phylogenomics Project. GigaScience 3:art26
ZHANG G, LI C, LI Q, LI B, LARKIN DM, LEE C, STORZ JF, ANTUNES A, GREENWOLD MJ, MEREDITH RW, ÖDEEN A, CUI J, ZHOU Q, XU L, PAN H, WANG Z, JIN L, ZHANG P, HU H, YANG W, HU J, XIAO J, YANG Z, LIU Y, XIE Q, YU H, LIAN J, WEN P, ZHANG F, LI H, ZENG Y, XIONG Z, LIU S, ZHOU L, HUANG Z, AN N, WANG J, ZHENG Q, XIONG Y, WANG G, WANG B, WANG J, FAN Y, DA FONSECA RR, ALFARO-NÚÑEZ A, SCHUBERT M, ORLANDO L, MOURIER T, HOWARD JT, GANAPATHY G, PFENNING A, WHITNEY O, RIVAS MV, HARA E, SMITH J, FARRÉ M, NARAYAN J, SLAVOV G, ROMANOV MN, BORGES R, MACHADO JP, KHAN I, SPRINGER MS, GATESY J, HOFFMANN FG, OPAZO JC, HÅSTAD O, SAWYER RH, KIM H, KIM KW, KIM HJ, CHO S, LI N, HUANG Y, BRUFORD MW, ZHAN X, DIXON A, BERTELSEN MF, DERRYBERRY E, WARREN W, WILSON RK, LI S, RAY DA, GREEN RE, O’BRIEN SJ, GRIFFIN D, JOHNSON WE, HAUSSLER D, RYDER OA, WILLERSLEV E, GRAVES GR, ALSTRÖM P, FJELDSÅ J, MINDELL DP, EDWARDS SV, BRAUN EL, RAHBEK C, BURT DW, HOUDE P, ZHANG Y, YANG H, WANG J, AVIAN GENOME CONSORTIUM, JARVIS ED, GILBERT MTP Y WANG J (2014b) Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346:1311–1320
ZINK RM (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proceedings of the Royal Society B, Biological Sciences 271:561–564
