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Genomics of natural bird populations

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Molecular Ecology (2008) 17, 964–980 doi: 10.1111/j.1365-294X.2007.03551.x© 2007 The AuthorsJournal compilation © 2007 Blackwell Publishing LtdBlackwell Publishing LtdGenomics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genomeNICLAS BACKSTRÖM, SOFIE FAGERBERG and HANS ELLEGRENDepartment of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, SwedenAbstractAlthough there is growing interest to take genomics into the complex realms of naturalpopulations, there is a general shortage of genomic resources and tools available for wildspecies. This applies not at least to birds, for which genomic approaches should be helpfulto questions such as adaptation, speciation and population genetics. In this study, wedescribe a genome-wide reference set of conserved avian gene markers, broadly applicableacross birds. By aligning protein-coding sequences from the recently assembled chickengenome with orthologous sequences in zebra finch, we identified particularly conservedexonic regions flanking introns of suitable size for subsequent amplification and sequencing.Primers were designed for 242 gene markers evenly distributed across the chicken genome,with a mean inter-marker interval of 4.2 Mb. Between 78% and 93% of the markers amplifieda specific product in five species tested (chicken, peregrine falcon, collared flycatcher, greatreed warbler and blue tit). Two hundred markers were sequenced in collared flycatcher,yielding a total of 122.41 kb of genomic DNA sequence (12096 bp coding sequence and110 314 bp noncoding). Intron size of collared flycatcher and chicken was highly correlated,as was GC content. A polymorphism screening using these markers in a panel of 10 unrelatedcollared flycatchers identified 871 single nucleotide polymorphisms (π = 0.0029) and 33indels (mainly very short). Avian genome characteristics such as uniform genome size andlow rate of syntenic rearrangements suggest that this marker set will find broad utility as agenome-wide reference resource for molecular ecological and population genomic analysisof birds. We envision that it will be particularly useful for obtaining large-scale orthologoustargets in different species — important in, for instance, phylogenetics — and for large-scaleidentification of evenly distributed single nucleotide polymorphisms needed in linkagemapping or in studies of gene flow and hybridization.Keywords: chicken, collared flycatcher, comparative anchored tagged sequences, linkage mapping,QTL analysis, single nucleotide polymorphismReceived 22 May 2007; revision accepted 15 August 2007IntroductionThere is a growing interest in exploring the possibility tomerge knowledge, hypotheses and technologies from thefields of genomics and evolutionary biology (Feder &Mitchell-Olds 2003). Impetus for this would be, for instance,the long-term goals to understand and trace the geneticbackground to phenotypic traits under selection in naturalpopulations and, subsequently, to study adaptation usingthe combined information from genotypes and phenotypes.Other motivations could be to reveal the genetic basis ofreproductive isolation and to scale up analyses of popula-tion processes using population genomics approaches.However, although there is rapid progress in the generationand establishment of genomic resources in model species,we still lack resources and tools for the vast majority ofwild species, and this is so even for initial and small-scaleattempts to access the genome.Before the era of eukaryotic whole-genome sequences,O’Brien et al. (1993) and Lyons et al. (1997) introduced theconcept of ‘comparative anchor tagged sequences’ (CATS).CATS are anchored reference loci with known location in amodel genome that, based on evolutionary conservation,Correspondence: Hans Ellegren, Fax: +46-18-4716310; E-mail:[email protected] REFERENCE SET OF AVIAN GENE MARKERS 965© 2007 The AuthorsJournal compilation © 2007 Blackwell Publishing Ltdcan be analysed in other species and used for comparativemapping. By designing markers evenly spread in a model(human) genome, the idea was that the markers wouldsimplify the construction of genetic maps of other (mam-malian) species, to allow transfer of map informationbetween species and to make inference on chromosomeevolution. Specifically, the selection of an even distributionof CATS markers in the model was expected to reducethe number of markers needed to construct maps of otherspecies, given that related species tend to show conservedsynteny. Moreover, by focusing on markers evolving understrong functional constraint, like many protein-codinggenes, the possibility of cross-species analysis would befacilitated. The access to CATS played an important rolein the development of the first genetic maps of severalmammals (O’Brien et al. 1993; Lyons et al. 1999; Lahbib-Mansais et al. 2000).Although the suggested use for CATS was initially basedon probe hybridization of Southern blots (O’Brien et al.1993), the approach found more widespread use whenconverted to polymerase chain reaction (PCR)-baseddetection. The idea was to design primers in two adjacentand conserved exons flanking an intron of suitable size forPCR amplification. The rationale behind including exonicsequence was that it should not only increase amplifica-tion success, but also aid in the ability to confirm orthologybetween sequences from different species. In addition,amplification of introns would increase the likelihood offinding polymorphic sites. Although not presented in thecontext of deriving sets of reference markers evenly spreadacross the whole genome, other investigators independ-ently, or subsequently, used this approach on smaller scalesand termed it ‘traced orthologous amplified sequencetags’ (TOAST) (Jiang et al. 1998) or ‘exon-primed introncrossing’ (EPIC) PCR (Palumbi & Baker 1994). More recently,the concept of using conserved exonic, intron-spanningprimers has been frequently used in obtaining shortsequence tags (STS) of relatively uncharacterized genomes(Venta et al. 1996; Touriya et al. 2003; Aitken et al. 2004;Cogan et al. 2006).If we can start to unveil the links between genotypesand phenotypes in natural populations, this would clearlyadvance our knowledge on fundamental evolutionaryprocesses. Birds are important study organisms in thisrespect because there is ample background informationon many general


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