Maintenance of Species Differences in Closely Related Tetraploid Parasitic Euphrasia (Orobanchaceae) on an Isolated Island

Hannes Becher,Max R Brown,Gavin Powell,Chris Metherell,Nick J Riddiford,Alex D Twyford

doi:10.1016/j.xplc.2020.100105

Abstract

Polyploidy is pervasive in angiosperm evolution and plays important roles in adaptation and speciation. However, polyploid groups are understudied due to complex sequence homology, challenging genome assembly, and taxonomic complexity. Here, we study adaptive divergence in taxonomically complex eyebrights (Euphrasia), where recent divergence, phenotypic plasticity, and hybridization blur species boundaries. We focus on three closely related tetraploid species with contrasting ecological preferences that are sympatric on Fair Isle, a small isolated island in the British Isles. Using a common garden experiment, we show a genetic component to the morphological differences present between these species. Using whole-genome sequencing and a novel k-mer approach we call “Tetmer”, we demonstrate that the species are of allopolyploid origin, with a sub-genome divergence of approximately 5%. Using ∼2 million SNPs, we show sub-genome homology across species, with a very low sequence divergence characteristic of recent speciation. This genetic variation is broadly structured by species, with clear divergence of Fair Isle heathland Euphrasia micrantha, while grassland Euphrasia arctica and coastal Euphrasia foulaensis are more closely related. Overall, we show that tetraploid Euphrasia is a system of allopolyploids of postglacial species divergence, where adaptation to novel environments may be conferred by old variants rearranged into new genetic lineages.

Highlights

Plant populations that grow in contrasting ecological conditions experience different selection pressures for adaptive traits that underlie survival and reproduction (Clausen et al, 1940, 1948; Clausen and Hiesey, 1958; Nun ̃ ez-Farfan and Schlichting, 2001)
Individuals partly clustered by species in a principal component analysis (PCA, Figure 2B), while linear discriminant analysis (LDA) trained on 80% of the data classified all remaining individuals correctly
Using LDA trained on 80% of the data (439 of 549 individuals without any missing data), it was possible to accurately classify 75% of the individuals in the test set (i.e., 82 of 110 individuals were assigned the species from which their seeds had been collected, Figure 2D)

Summary

Introduction

Plant populations that grow in contrasting ecological conditions experience different selection pressures for adaptive traits that underlie survival and reproduction (Clausen et al, 1940, 1948; Clausen and Hiesey, 1958; Nun ̃ ez-Farfan and Schlichting, 2001). The trajectory of divergence in the early stages of speciation is complex, with recent studies showing that populations may diverge in the face of ongoing gene flow that was previously thought sufficient to homogenize population differences and oppose divergence (Danley et al, 2000; Papadopulos et al, 2011; Nadeau et al, 2013; Richards et al, 2016) Such insights have been made in different plant species, they are mostly ecological and evolutionary model systems amenable to genomic analysis (Bernasconi et al, 2009; Twyford et al, 2015).

Methods

Results

Conclusion