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Selection and Gene Flow Shape Genomic Islands that Control Floral Guides

ABSTRACT: Genomes of closely-related species or populations often display localized regions of enhanced relative sequence divergence, termed genomic islands. It has been proposed that these islands arise through selective sweeps and/or barriers to gene flow. Here, we genetically dissect a genomic island that controls flower color pattern differences between two subspecies of Antirrhinum, A.m.striatum and A.m.pseudomajus, and relate it to clinal variation across a natural hybrid zone. We show that selective sweeps likely raised relative divergence at two tightly-linked MYB-like transcription factors, leading to distinct flower patterns in the two subspecies. The two patterns provide alternate floral guides and create a strong barrier to gene flow where populations come into contact. This barrier affects the selected flower color genes and tightly linked loci, but does not extend outside of this domain, allowing gene flow to lower relative divergence for the rest of the chromosome. Thus, both selective sweeps and barriers to gene flow play a role in shaping genomic islands: sweeps cause elevation in relative divergence while heterogeneous gene flow flattens the surrounding “sea”, making the island of divergence stand out. By showing how selective sweeps establish alternative adaptive phenotypes that lead to barriers to gene flow, our study sheds light on possible mechanisms leading to reproductive isolation and speciation.

ORGANISM(S): Antirrhinum majus

PROVIDER: GSE118621 | GEO | 2018/08/18

REPOSITORIES: GEO

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Project description:Plumage color plays a prominent role in reproductive isolation and thus understanding the genetic basis of pigmentation patterns can provide critical insight into speciation. Subspecies of the dark-eyed junco (Junco hyemalis) show marked differences in melanic plumage coloration known to have evolved rapidly since the Last Glacial Maximum just 18,000 years ago. To understand this rapid radiation we studied the pigment composition and the genetic basis of coloration in two divergent subspecies, the slate-colored and Oregon juncos. We used HPLC and light microscopy to investigate pigment deposition patterns in feathers from four body areas. RNA-seq data generated under common garden experimental conditions were then used to compare the relative roles of differential gene expression in growing feathers and sequence divergence in loci expressed during feather development. Junco feathers were found to differ in eumelanin and pheomelanin content and distribution, producing a range of black, gray and brown colors. Transcriptomic data revealed marked regulatory differences among subspecies and among body-parts within subspecies in known melanin-pathway genes (including PMEL, TYR, TYRP1, OCA2, MLANA), but also in several novel or poorly known loci (EDAR, VPS33B, HPS1). Within subspecies, lighter feathers expressed less melanin synthesis genes, more ASIP, and showed differential expression of Wnt signaling genes. Feathers from different body regions also showed differential expression of Hox genes. The two subspecies differed in expression of ASIP and three other genes (MFSD12, KCNJ13, HAND2) previously associated with color development. Sequence variation in the expressed genes was not related to color differences between junco subspecies. Our findings suggest that differential expression of a few genes can account for marked differences in plumage color and pattern, a mechanism that can account for the rapid diversification of juncos. Several novel candidate pigmentation genes found in juncos may contribute to the expression of melanic coloration in other vertebrates.

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Selection and Gene Flow Shape Genomic Islands that Control Floral Guides

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