TY - JOUR
T1 - Divergent Selection and Primary Gene Flow Shape Incipient Speciation of a Riparian Tree on Hawaii Island
AU - Choi, Jae Young
AU - Purugganan, Michael
AU - Stacy, Elizabeth A.
N1 - Funding Information:
We thank the Hawaii Department of Forestry and Wildlife for permission to collect leaf samples from state forests and J. Johansen for assistance with sample collection. We are grateful also to T. Sakishima, A. Veillet, and the Core Genetics Facility at the University of Hawaii Hilo for assistance with DNA isolation. We are also grateful to S. Ferrand at New York University Abu Dhabi (NYUAD) for assistance with the library preparation, and M. Gros-Balthazard at NYUAD for support with the genomic data. We thank A. Nguyen for assistance with maps, and we thank E. Richards at University of North Carolina Chapel Hill for help with the analysis. We also thank the NYUAD Center for Genomics and Systems Biology for sequencing support and the New York University IT High Performance Computing for supplying the computational resources, services, and staff expertise. This work was supported by grants from the National Science Foundation Plant Genome Research Program (IOS-1546218), the Zegar Family Foundation (A16-0051), and the NYUAD Research Institute (G1205) to M.P., and from the National Science Foundation Faculty Early Career Development Program (DEB 0954274) (PI) and Centers of Research Excellence in Science and Technology Program (HRD-0833211) (co-PI) to E.A.S.
Publisher Copyright:
© 2019 The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
PY - 2020/3/1
Y1 - 2020/3/1
N2 - A long-standing goal of evolutionary biology is to understand the mechanisms underlying the formation of species. Of particular interest is whether or not speciation can occur in the presence of gene flow and without a period of physical isolation. Here, we investigated this process within Hawaiian Metrosideros, a hypervariable and highly dispersible woody species complex that dominates the Hawaiian Islands in continuous stands. Specifically, we investigated the origin of Metrosideros polymorpha var. newellii (newellii), a riparian ecotype endemic to Hawaii Island that is purportedly derived from the archipelago-wide M. polymorpha var. glaberrima (glaberrima). Disruptive selection across a sharp forest-riparian ecotone contributes to the isolation of these varieties and is a likely driver of newellii's origin. We examined genome-wide variation of 42 trees from Hawaii Island and older islands. Results revealed a split between glaberrima and newellii within the past 0.3-1.2 My. Admixture was extensive between lineages within Hawaii Island and between islands, but introgression from populations on older islands (i.e., secondary gene flow) did not appear to contribute to the emergence of newellii. In contrast, recurrent gene flow (i.e., primary gene flow) between glaberrima and newellii contributed to the formation of genomic islands of elevated absolute and relative divergence. These regions were enriched for genes with regulatory functions as well as for signals of positive selection, especially in newellii, consistent with divergent selection underlying their formation. In sum, our results support riparian newellii as a rare case of incipient ecological speciation with primary gene flow in trees.
AB - A long-standing goal of evolutionary biology is to understand the mechanisms underlying the formation of species. Of particular interest is whether or not speciation can occur in the presence of gene flow and without a period of physical isolation. Here, we investigated this process within Hawaiian Metrosideros, a hypervariable and highly dispersible woody species complex that dominates the Hawaiian Islands in continuous stands. Specifically, we investigated the origin of Metrosideros polymorpha var. newellii (newellii), a riparian ecotype endemic to Hawaii Island that is purportedly derived from the archipelago-wide M. polymorpha var. glaberrima (glaberrima). Disruptive selection across a sharp forest-riparian ecotone contributes to the isolation of these varieties and is a likely driver of newellii's origin. We examined genome-wide variation of 42 trees from Hawaii Island and older islands. Results revealed a split between glaberrima and newellii within the past 0.3-1.2 My. Admixture was extensive between lineages within Hawaii Island and between islands, but introgression from populations on older islands (i.e., secondary gene flow) did not appear to contribute to the emergence of newellii. In contrast, recurrent gene flow (i.e., primary gene flow) between glaberrima and newellii contributed to the formation of genomic islands of elevated absolute and relative divergence. These regions were enriched for genes with regulatory functions as well as for signals of positive selection, especially in newellii, consistent with divergent selection underlying their formation. In sum, our results support riparian newellii as a rare case of incipient ecological speciation with primary gene flow in trees.
KW - Metrosideros
KW - ecological speciation
KW - gene flow
KW - genomic islands of divergence
KW - incipient speciation
KW - sympatric speciation
UR - http://www.scopus.com/inward/record.url?scp=85081104136&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85081104136&partnerID=8YFLogxK
U2 - 10.1093/molbev/msz259
DO - 10.1093/molbev/msz259
M3 - Article
C2 - 31693149
AN - SCOPUS:85081104136
VL - 37
SP - 695
EP - 710
JO - Molecular Biology and Evolution
JF - Molecular Biology and Evolution
SN - 0737-4038
IS - 3
ER -