Ancestral polymorphisms shape the adaptive radiation of Metrosideros across the Hawaiian Islands

Jae Young Choi, Xiaoguang Dai, Ornob Alam, Julie Z. Peng, Priyesh Rughani, Scott Hickey, Eoghan Harrington, Sissel Juul, Julien F. Ayroles, Michael D. Purugganan, Elizabeth A. Stacy

Research output: Contribution to journalArticlepeer-review

Abstract

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 genomics 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 Metrosideros polymorpha var. incana and analyzed whole-genome sequences of 131 individuals from 11 taxa sampled across the islands. Demographic modeling and population genomics analyses suggested that Hawaiian Metrosideros originated from a single colonization event and subsequently spread across the archipelago following the formation of new islands. The evolutionary history of Hawaiian Metrosideros shows evidence of extensive reticulation associated with significant sharing of ancestral variation between taxa and secondarily with admixture. Taking advantage of the highly contiguous genome assembly, we investigated the genomic architecture underlying the adaptive radiation and discovered that divergent selection drove the formation of differentiation outliers in paired taxa representing early stages of speciation/divergence. Analysis of the evolutionary origins of the outlier single nucleotide polymorphisms (SNPs) showed enrichment for ancestral variations under divergent selection. Our findings suggest that Hawaiian Metrosideros possesses an unexpectedly rich pool of ancestral genetic variation, and the reassortment of these variations has fueled the island adaptive radiation.

Original languageEnglish (US)
Article numbere2023801118
JournalProceedings of the National Academy of Sciences of the United States of America
Volume118
Issue number37
DOIs
StatePublished - Sep 14 2021

All Science Journal Classification (ASJC) codes

  • General

Keywords

  • Adaptive radiation
  • Ecological speciation
  • Incipient speciation
  • Metrosideros
  • Speciation genomics

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