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The Aquilegia Genome: Adaptive Radiation and An bioRxiv preprint doi: https://doi.org/10.1101/264101; this version posted September 7, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available underManuscript aCC-BY 4.0 submittedInternational to license eLife. 1 The Aquilegia genome: adaptive 2 radiation and an extraordinarily 3 polymorphic chromosome with a 4 unique history 1 2 3 1,4 5 Danièle Filiault , Evangeline S. Ballerini , Terezie Mandáková , Gökçe Aköz , 2 5,6 5,6 5,6 6 Nathan Derieg , Jeremy Schmutz , Jerry Jenkins , Jane Grimwood , 5 5 5 5 5 7 Shengqiang Shu , Richard D. Hayes ,Uffe Hellsten , Kerrie Barry , Juying Yan , 5 7 1 8 Sirma Mihaltcheva , Miroslava Karafiátová , Viktoria Nizhynska , Martin A. 3 2,* 1,* 9 Lysak , Scott A. Hodges , Magnus Nordborg *For correspondence: [email protected] (SH); 1 10 Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, [email protected] 2 (MN) 11 Austria; Department of Ecology, Evolution, and Marine Biology, University of California 3 12 Santa Barbara, Santa Barbara, USA; Central-European Institute of Technology (CEITEC), 4 13 Masaryk University, Brno, Czech Republic; Vienna Graduate School of Population 5 14 Genetics, Vienna, Austria; Department of Energy Joint Genome Institute, Walnut Creek, 6 15 California, USA; HudsonAlpha Institute of Biotechnology, Huntsville, Alabama, USA; 7 16 Institute of Experimental Botany, Centre of the Region Haná for Biotechnological and 17 Agricultural Research, Olomouc, Czech Republic 18 19 Abstract The columbine genus Aquilegia is a classic example of an adaptive radiation, involving a 20 wide variety of pollinators and habitats. Here we present the genome assembly of A. coerulea 21 ’Goldsmith’, complemented by high-coverage sequencing data from 10 wild species covering the 22 world-wide distribution. Our analyses reveal extensive allele sharing among species and 23 demonstrate that introgression and selection played a role in the Aquilegia radiation. We also 24 present the remarkable discovery that the evolutionary history of an entire chromosome differs 25 from that of the rest of the genome – a phenomenon which we do not fully understand, but which 26 highlights the need to consider chromosomes in an evolutionary context. 27 28 Introduction 29 Understanding adaptive radiation is a longstanding goal of evolutionary biology (Schluter, 2000). As 30 a classic example of adaptive radiation, the Aquilegia genus has outstanding potential as a subject 31 of such evolutionary studies (Hodges et al., 2004; Hodges and Derieg, 2009; Kramer, 2009). The 32 genus is made up of about 70 species distributed across Asia, North America, and Europe (Munz, 33 1946)(Figure 1). Distributions of many Aquilegia species overlap or adjoin one another, sometimes 34 forming notable hybrid zones (Grant, 1952; Hodges and Arnold, 1994b; Li et al., 2014). Additionally, 35 species tend to be widely interfertile, especially within geographic regions (Taylor, 1967). 36 Phylogenetic studies have defined two concurrent, yet contrasting, adaptive radiations in Aquile- 37 gia (Bastida et al., 2010; Fior et al., 2013). From a common ancestor in Asia, one radiation occurred 38 in North America via Northeastern Asian precursors, while a separate Eurasian radiation took place 1 of 31 bioRxiv preprint doi: https://doi.org/10.1101/264101; this version posted September 7, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available underManuscript aCC-BY 4.0 submittedInternational to license eLife. A. vulgaris A. sibirica A. formosa A. pubescens A. barnebyi Semiaquilegia adoxoides A. aurea A. oxysepala A. japonica A. longissima A. chrysantha var. oxysepala Figure 1. Distribution of Aquilegia species. There are ~70 species in the genus Aquilegia, broadly distributed across temperate regions of the Northern Hemisphere (grey). The 10 Aquilegia species sequenced here were chosen as representatives spanning this geographic distribution as well as the diversity in ecological habitat and pollinator-influenced floral morphology of the genus. Semiaquilegia adoxoides, generally thought to be the sister taxon to Aquilegia (Fior et al., 2013), was also sequenced. A representative photo of each species is shown and is linked to its approximate distribution. 39 in central and western Asia and Europe. While adaptation to different habitats is thought to be 40 a common force driving both radiations, shifts in primary pollinators also play a substantial role 41 in North America (Whittall and Hodges, 2007; Bastida et al., 2010). Previous phylogenetic studies 42 have frequently revealed polytomies (Hodges and Arnold, 1994b; Ro and Mcpheron, 1997; Whittall 43 and Hodges, 2007; Bastida et al., 2010; Fior et al., 2013), suggesting that many Aquilegia species 44 are very closely related. 45 Genomic data are beginning to uncover the extent to which interspecific variant sharing reflects 46 a lack of strictly bifurcating species relationships, particularly in the case of adaptive radiation. 47 Discordance between gene and species trees has been widely observed (Novikova et al., 2016) (and 48 references 15,34-44 therein) (Svardal et al., 2017; Malinsky et al., 2017), and while disagreement at 49 the level of individual genes is expected under standard population genetics coalescent models 50 (Takahata, 1989) (also known as “incomplete lineage sorting” (Avise and Robinson, 2008)), there 51 is increased evidence for systematic discrepancies that can only be explained by some form of 52 gene flow (Green et al., 2010; Novikova et al., 2016; Svardal et al., 2017; Malinsky et al., 2017). 53 The importance of admixture as a source of adaptive genetic variation has also become more 54 evident (Lamichhaney et al., 2015; Mallet et al., 2016; Pease et al., 2016). Hence, rather than 55 being a problem to overcome in phylogenetic analysis, non-bifurcating species relationships could 56 actually describe evolutionary processes that are fundamental to understanding speciation itself. 57 Here we generate an Aquilegia reference genome based on the horticultural cultivar Aquilegia 58 coerulea ‘Goldsmith’ and perform resequencing and population genetic analysis of 10 additional 2 of 31 bioRxiv preprint doi: https://doi.org/10.1101/264101; this version posted September 7, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available underManuscript aCC-BY 4.0 submittedInternational to license eLife. 59 individuals representing North American, Asian, and European species, focusing in particular on 60 the relationship between species. 61 Results 62 Genome assembly and annotation 63 We sequenced an inbred horticultural cultivar (A. coerulea ‘Goldsmith’) using a whole genome 64 shotgun sequencing strategy. A total of 171,589 Sanger sequencing reads from seven genomic 65 libraries (Supplementary File 1) were assembled to generate 2,529 scaffolds with an N50 of 3.1Mb 66 (Supplementary File 2). With the aid of two genetic maps, we assembled these initial scaffolds 67 into a 291.7 Mbp reference genome consisting of 7 chromosomes (282.6 Mbp) and an additional 68 1,027 unplaced scaffolds (9.13 Mbp) (Supplementary File 3). The completeness of the assembly 69 was validated using 81,617 full length cDNAs from a variety of tissues and developmental stages 70 (Kramer and Hodges, 2010), of which 98.69% mapped to the assembly. We also assessed assembly 71 accuracy using Sanger sequencing of 23 full-length BAC clones. Of more than 3 million base pairs 72 sequenced, only 1,831 were found to be discrepant between BAC clones and the assembled refer- 73 ence (Supplementary File 4). To annotate genes in the assembly, we used RNAseq data generated 74 from a variety of tissues and Aquilegia species (Supplementary File 5), EST data sets (Kramer and 75 Hodges, 2010), and protein homology support, yielding 30,023 loci and 13,527 alternate transcripts. 76 The A. coerulea v3.1 genome release is available on Phytozome (https://phytozome.jgi.doe.gov/). 77 For a detailed description of assembly and annotation, see Materials and Methods. 78 Polymorphism and divergence 79 We deeply resequenced one individual from each of ten Aquilegia species (Figure 1 and Figure 80 1—figure supplement 1). Sequences were aligned to the A. coerulea v3.1 reference using bwa-mem 81 (Li and Durbin, 2009; Li, 2013) and variants were called using GATK Haplotype Caller (McKenna et al., 82 2010). Genomic positions were conservatively filtered to identify the portion of the genome in which 83 variants could be reliably called across all ten species (see Materials and Methods for alignment, 84 SNP calling, and genome filtration details). The resulting callable portion of the genome was heavily 85 biased towards genes and included 57% of annotated coding regions (48% of gene models), but 86 only 21% of the reference genome as a whole. 87 Using these callable sites, we calculated nucleotide diversity as the percentage of pairwise 88 sequence differences in each individual. Assuming random mating, this metric reflects both 89 individual sample heterozygosity and nucleotide diversity in the species as a whole. Of the ten 90 individuals, most had a nucleotide diversity of 0.2-0.35% (Figure 2a), similar to previous estimates 91 of nucleotide diversity in Aquilegia (Cooper et al., 2010), yet lower than that of a typical outcrossing 92 species (Leffler et al., 2012). While likely partially attributable to enrichment for highly conserved 93 genomic regions with our stringent filtration, this atypically low nucleotide diversity could also 94 reflect inbreeding. Additionally, four individuals in our panel had extended stretches of near- 95 homozygosity (defined as nucleotide diversity < 0.1%) consistent with recent inbreeding (Figure2- 96 figure supplemental 1). Aquilegia has no known self-incompatibility mechanism, and selfing does 97 appear to be common.
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