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The genetic architecture of local adaptation I: the genomic landscape of foxtail pine (Pinus balfouriana Grev. & Balf.) as revealed from a high-density linkage map

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Abstract

Explaining the origin and evolutionary dynamics of the genetic architecture of adaptation is a major research goal of evolutionary genetics. Despite controversy surrounding success of the attempts to accomplish this goal, a full understanding of adaptive genetic variation necessitates knowledge about the genomic location and patterns of dispersion for the genetic components affecting fitness-related phenotypic traits. Even with advances in next-generation sequencing technologies, the production of full genome sequences for non-model species is often cost-prohibitive, especially for tree species such as pines where genome size often exceeds 20 to 30 Gbp. We address this need by constructing a dense linkage map for foxtail pine (Pinus balfouriana Grev. & Balf.), with the ultimate goal of uncovering and explaining the origin and evolutionary dynamics of adaptive genetic variation in natural populations of this forest tree species. We utilized megagametophyte arrays (n = 76–95 megagametophytes/tree) from four maternal trees in combination with double digest restriction-site associated DNA sequencing (ddRADseq) to produce a consensus linkage map covering 98.58 % of the foxtail pine genome, which was estimated to be 1276 cM in length (95 % CI, 1174 to 1378 cM). A novel bioinformatic approach using iterative rounds of marker ordering and imputation was employed to produce single-tree linkage maps (507–17,066 contigs/map; lengths, 1037.40–1572.80 cM). These linkage maps were collinear across maternal trees, with highly correlated marker orderings (Spearman’s ρ>0.95). A consensus linkage map derived from these single-tree linkage maps contained 12 linkage groups along which 20,655 contigs were non-randomly distributed across 901 unique positions (n=23 contigs/position), with an average spacing of 1.34 cM between adjacent positions. Of the 20,655 contigs positioned on the consensus linkage map, 5627 had enough sequence similarity to contigs contained within the most recent build of the loblolly pine (Pinus taeda L.) genome to identify them as putative homologues containing both genic and non-genic loci. Importantly, all 901 unique positions on the consensus linkage map had at least one contig with putative homology to loblolly pine. When combined with the other biological signals that predominate in our data (e.g., correlations of recombination fractions across single trees), we show that dense linkage maps for non-model forest tree species can be efficiently constructed using next-generation sequencing technologies. We subsequently discuss the usefulness of these maps as community-wide resources and as tools with which to test hypotheses about the genetic architecture of local adaptation.

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Acknowledgments

The authors would like to thank the staff at the USDA Institute of Forest Genetics, the VCU Nucleic Acids Research Facility, and the VCU Center for High Performance Computing. In addition, we would like to thank Tom Blush and Tom Burt for help in obtaining seeds. Funding for this project was made available to AJE via start-up funds from Virginia Commonwealth University. CJF was supported by the National Science Foundation (NSF) National Plant Genome Initiative (NPGI): Postdoctoral Research Fellowship in Biology (PRFB) FY 2013 Award no. NSF-NPGI-PRFB-1306622.

Data Archiving Statement

Raw short read data are located in the NCBI Short Read Archive (accession number: PRJNA266319). The linkage map summary files, assembly used for read mapping and SNP calling, and VCF files are given as supporting documents (Files S1 - S3). The consensus linkage map is also available in the Comparative Mapping Database located at the Dendrome website (accession number: TG151). Source code for this manuscript and data analyses are located at http://www.github.com/cfriedline/foxtail_linkage.

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Authors and Affiliations

  1. Department of Biology, Virginia Commonwealth University, Richmond, VA, 23284, USA

    Christopher J. Friedline, Erin M. Hobson, Douglas E. Harwood & Andrew J. Eckert

  2. Integrative Life Sciences Program, Virginia Commonwealth University, Richmond, VA, 23284, USA

    Brandon M. Lind

  3. Institute of Forest Genetics, USDA Pacific Southwest Research Station, Placerville, CA, 9566, USA

    Annette Delfino Mix

  4. Department of Plant Pathology, University of California, Davis, CA, 95616, USA

    Patricia E. Maloney

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  1. Christopher J. Friedline
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Communicated by S. N. Aitken

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Friedline, C.J., Lind, B.M., Hobson, E.M. et al. The genetic architecture of local adaptation I: the genomic landscape of foxtail pine (Pinus balfouriana Grev. & Balf.) as revealed from a high-density linkage map. Tree Genetics & Genomes 11, 49 (2015). https://doi.org/10.1007/s11295-015-0866-x

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