Demography and selection analysis of the incipient adaptive radiation of a Hawaiian woody species

Ayako Izuno,Keito Kobayashi,Kentaro K Shimizu,Yusuke Onoda,Mana Mukai,Yuji Isagi,Gaku Amada,Juliette De Meaux

doi:10.1371/journal.pgen.1009987

Abstract

Ecological divergence in a species provides a valuable opportunity to study the early stages of speciation. We focused on Metrosideros polymorpha, a unique example of the incipient radiation of woody species, to examine how an ecological divergence continues in the face of gene flow. We analyzed the whole genomes of 70 plants collected throughout the island of Hawaii, which is the youngest island with the highest altitude in the archipelago and encompasses a wide range of environments. The continuous M. polymorpha forest stands on the island of Hawaii were differentiated into three genetic clusters, each of which grows in a distinctive environment and includes substantial genetic and phenotypic diversity. The three genetic clusters showed signatures of selection in genomic regions encompassing genes relevant to environmental adaptations, including genes associated with light utilization, oxidative stress, and leaf senescence, which are likely associated with the ecological differentiation of the species. Our demographic modeling suggested that the glaberrima cluster in wet environments maintained a relatively large population size and two clusters split: polymorpha in the subalpine zone and incana in dry and hot conditions. This ecological divergence possibly began before the species colonized the island of Hawaii. Interestingly, the three clusters recovered genetic connectivity coincidentally with a recent population bottleneck, in line with the weak reproductive isolation observed in the species. This study highlights that the degree of genetic differentiation between ecologically-diverged populations can vary depending on the strength of natural selection in the very early phases of speciation.

Highlights

Adaptation to distinct resources or environments often causes genetic differentiation in a species [1]
M. polymorpha plants growing in different environments have substantially different genomes, especially at the genomic regions with genes putatively controlling physiology to fit in distinct environment
It is suggested that genetic barriers can strengthen or weaken depending on environments splitting the ecology of a species before reproductive isolation becomes complete

Summary

Introduction

Adaptation to distinct resources or environments often causes genetic differentiation in a species [1]. The genetic differentiation can increase and result in speciation, when an ecological divergence is allopatric [2] and/or adaptive traits are associated with non-random mating [3]. After colonizing the Hawaiian Islands 3.1–3.9 million years ago [5,6], the species has adapted to a wide range of environments: it grows from sea level to the alpine tree line and from dry substrates in early successional stages to wet and mature forest soils [7,8]. Morphological variation in a common garden suggests that most of the phenotypic differences are genetically determined [10,12,13]. Home site advantage shown in reciprocal transplantation experiments indicates that phenotypic differentiation is associated with fitness [14]. Despite efforts in recent genomic studies [15,16], the genetic regions and selective forces associated with phenotypic differences are still unclear

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