Stacy, E. | bioRxiv Science

bioRxiv2020

Selection on ancient variations drives the adaptive radiation of Metrosideros across the Hawaiian archipelago

Some of the most spectacular adaptive radiations begin with founder populations on remote islands. How genetically limited founder populations give rise to the striking phenotypic and ecological diversity characteristic of adaptive radiations is a paradox of evolutionary biology. We conducted an evolutionary genomic analysis of genus Metrosideros, a landscape-dominant, incipient adaptive radiation of woody plants that spans a striking range of phenotypes and environments across the Hawaiian Islands. Using nanopore-sequencing, we created a chromosome-level genome assembly for M. polymorpha var. incana and analyzed wholegenome sequences of 131 individuals from 11 taxa sampled across the islands. We found evidence of population structure that grouped taxa by island. Demographic modeling showed concordance between the divergence times of island-specific lineages and the geological formation of individual islands. Gene flow was also detected within and between island taxa, suggesting a complex reticulated evolutionary history. We investigated genomic regions with increased differentiation as these regions may harbor variants involved in local adaptation or reproductive isolation, thus forming the genomic basis of adaptive radiation. We discovered differentiation outliers have arisen from balancing selection on ancient divergent haplotypes that formed before the initial colonization of the archipelago. These regions experienced recurrent divergent selection as lineages colonized and diversified on new islands, and hybridization likely facilitated the transfer of these ancient variants between taxa. Balancing selection on multiple ancient haplotypes-or time-tested variants-may help to explain how lineages with limited gene pools can rapidly diversify to fill myriad ecological niches on remote islands. Significance statementSome of the most spectacular adaptive radiations of plants and animals occur on remote oceanic islands, yet such radiations are preceded by founding events that severely limit genetic variation. How genetically depauperate founder populations give rise to the spectacular phenotypic and ecological diversity characteristic of island adaptive radiations is not known. We generated novel genomic resources for Hawaiian Metrosideros--a hyper-variable incipient adaptive radiation of woody taxa--for insights into the paradox of remote island radiations. We found that Metrosideros colonized each island shortly after formation and diversified within islands through recurrent selection on ancient variations that predate the radiation. Recurring use of ancient variants may explain how genetically depauperate lineages can diversify to fill countless niches on remote islands.

evolutionary biology↗

bioRxiv2019

Divergent selection and primary gene flow shape incipient speciation of a riparian tree on Hawaii Island

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 hyper-variable 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 newelliis 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 million years. 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.\n\nAuthor summaryA long-standing question in evolution is whether or not new species can arise in the presence of gene flow, which is expected to inhibit the formation of reproductive isolating barriers. We investigated the genomics underlying the origin of a Hawaii Island-endemic riparian tree and purported case of incipient sympatric speciation due to disruptive selection across a sharp forest-riparian ecotone. We find extensive evidence of ongoing gene flow between the riparian tree and its closest relative along with local genomic regions resistant to admixture that likely formed through selection on genes for ecological adaptation and/or reproductive isolation. These results strongly suggest that where disruptive selection is strong, incipient speciation with gene flow is possible even in long-lived, highly dispersible trees.

evolutionary biology↗