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

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.

Performance of generalist hemiparasiticEuphrasiaacross a phylogenetically diverse host spectrum

“…Overall, the hosts that emerged as most consistently advantageous across all four Euphrasia species were Lolium perenne and L. corniculatus , which fulfil many of the above criteria (Beddows, 1967; Jones & Turkington, 1986). These conserved parasite responses are notable as we used highly divergent diploid and tetraploid Euphrasia species (~5% nucleotide divergence, corresponding to ~8 million years divergence (Wang et al , 2018; Becher et al , 2020)). In contrast, host conservation in many highly specialised holoparasitic taxa, like Orobanche , is uncommon, with host specific ecotypes found even within the same parasite species (Thorogood et al , 2009).…”

“…Host species are spatially heterogenous in their distribution and vary in abundance by habitat and geographic area, creating conditions that may allow local host adaptation. The low migration rate between Euphrasia populations, particularly in small flowered selfing taxa (French et al , 2005; Becher et al , 2020), may cause differentiation and promote local adaptation. While the drivers and tempo of local host adaptation are not understood, further investigations with many hemiparasite species combined with extensive host combinations will shed light on the nature of these interactions.…”

“…Experimental 1 aimed to understand the performance of Euphrasia across a phylogenetic diverse spread of plant species with a range of relevant attributes such as annual and perennial life history strategies. For this experiment, we focused on a single species, Euphrasia arctica , due to its widespread distribution in Britain, where it mainly occupies mixed grassland habitats (Metherell & Rumsey, 2018; Becher et al , 2020). We used forty-five diverse vascular plant species, including known hosts and suspected non-hosts (SI Appendix Table Sl).…”

The nature of intraspecific genome size variation in taxonomically complex eyebrights

“…Here we explore GS variation in British eyebrights ( Euphrasia L., Orobanchaceae), a recently radiating group of facultative hemiparasites. They comprise five diploid (2n = 2x = 22) and 15 tetraploid species (2n = 4x = 44) (Metherell & Rumsey, 2018), with genomic sequencing showing that British tetraploids are closely related allotetraploids, with one sub-genome derived from, or closely related to, British diploids (Becher et al ., 2020). The genus is an ideal model group for investigating GS variation within and between closely related species because species diversification is frequently postglacial (Gussarova et al ., 2008; Wang et al ., 2018a), with many taxa being narrow endemics or recent hybrid species.…”

Plant Evolutionary Adaptation

“…The second study of polyploidy takes a closer look at the origin and evolution of three tetraploid species of eyebrights ( Euphrasia ), which are semi-parasites of grass species ( Becher et al., 2020 ). The authors employ a common garden study to show that the phenotypic differences defining the tetraploid species are genetically controlled.…”