The nature of intraspecific and interspecific genome size variation in taxonomically complex eyebrights.

Hannes Becher,Jaume Pellicer,Max R Brown,Alex D Twyford,Chris Metherell,Robyn F Powell,Ilia J Leitch

doi:10.1093/aob/mcab102

Abstract

Background and aimsGenome size varies considerably across the diversity of plant life. Although genome size is, by definition, affected by genetic presence/absence variants, which are ubiquitous in population sequencing studies, genome size is often treated as an intrinsic property of a species. Here, we studied intra- and interspecific genome size variation in taxonomically complex British eyebrights (Euphrasia, Orobanchaceae). Our aim is to document genome size diversity and investigate underlying evolutionary processes shaping variation between individuals, populations and species.MethodsWe generated genome size data for 192 individuals of diploid and tetraploid Euphrasia and analysed genome size variation in relation to ploidy, taxonomy, population affiliation and geography. We further compared the genomic repeat content of 30 samples.Key resultsWe found considerable intraspecific genome size variation, and observed isolation-by-distance for genome size in outcrossing diploids. Tetraploid Euphrasia showed contrasting patterns, with genome size increasing with latitude in outcrossing Euphrasia arctica, but with little genome size variation in the highly selfing Euphrasia micrantha. Interspecific differences in genome size and the genomic proportions of repeat sequences were small.ConclusionsWe show the utility of treating genome size as the outcome of polygenic variation. Like other types of genetic variation, such as single nucleotide polymorphisms, genome size variation may be affected by ongoing hybridization and the extent of population subdivision. In addition to selection on associated traits, genome size is predicted to be affected indirectly by selection due to pleiotropy of the underlying presence/absence variants.

Highlights

Genome size, defined as the amount of DNA in an individual’s unreplicated gametophytic nucleus (Greilhuber et al, 2005), is associated with an organism’s life history, development, physiology, ecology, genome dynamics and evolution (Van’t Hof and Sparrow, 1963; Beaulieu et al, 2008; Šímová and Herben, 2012; Greilhuber and Leitch, 2013; Bilinski et al, 2018; Simonin and Roddy, 2018; Novák et al, 2020; Roddy et al, 2020)
Our study aims to answer the following questions: (1) How variable is genome size within species, between species and between ploidy levels? (2) What is the contribution of genomic repeats to genome size variation in British Euphrasia, and how does repeat content differ between the ploidy levels? (3) Does genome size variation correspond with known patterns of genetic structure and/or environmental variables in British Euphrasia? We discuss our results in the light of polygenic variation, and we argue for a closer integration of population genomics with research on genome size variation
We investigated the nature of genome size variation across taxonomically complex diploid and tetraploid British Euphrasia

Summary

Introduction

Genome size, defined as the amount of DNA in an individual’s unreplicated gametophytic nucleus (Greilhuber et al, 2005), is associated with an organism’s life history, development, physiology, ecology, genome dynamics and evolution (Van’t Hof and Sparrow, 1963; Beaulieu et al, 2008; Šímová and Herben, 2012; Greilhuber and Leitch, 2013; Bilinski et al, 2018; Simonin and Roddy, 2018; Novák et al, 2020; Roddy et al, 2020). Studies of diverse species differing in ploidy have shown that while whole genome duplication events initially lead to an increase in genome size, their subsequent evolution is often accompanied by genome downsizing over time (Leitch et al, 2008; Leitch and Leitch, 2008; Pellicer et al, 2010; Wong and Murray, 2012; Wendel, 2015; Zenil-Ferguson et al, 2016; Wang et al, 2021). While representative genome size estimates have been obtained for approximately two-thirds of flowering plant families (Pellicer and Leitch, 2020), variation between individuals and populations has typically received less attention, despite the increasing realization that such variation within species may be common (e.g. Šmarda et al, 2010; Kolář et al, 2017). Intraspecific differences in DNA content have been reported or are predicted between by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited

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