Phylogeography and the Evolutionary History of Sunflower (Helianthus annuus L.): Wild Diversity and the Dynamics of Domestication

Abstract

Patterns of genetic variation in crops are the result of selection and demographic changes that occurred during their domestication and improvement. In many cases, we have an incomplete picture of the origin of crops in the context of their wild progenitors, particularly with regard to the processes producing observed levels of standing genetic variation. Here, we analyzed sequence diversity in cultivated sunflower (Helianthus annuus L.) and its wild progenitor (common sunflower, also H. annuus) to reconstruct phylogeographic relationships and population genetic/demographic patterns across sunflower. In common sunflower, south-north patterns in the distribution of nucleotide diversity and lineage splitting indicate a history of rapid postglacial range expansion from southern refugia. Cultivated sunflower accessions formed a clade, nested among wild populations from the Great Plains, confirming a single domestication event in central North America. Furthermore, cultivated accessions sorted by market type (i.e., oilseed vs. confectionery) rather than breeding pool, recapitulating the secondary development of oil-rich cultivars during its breeding history. Across sunflower, estimates of nucleotide diversity and effective population sizes suggest that cultivated sunflower underwent significant population bottlenecks following its establishment ~5000 years ago. The patterns inferred here corroborate those from previous studies of sunflower domestication, and provide a comprehensive overview of its evolutionary history.

The History of Lentil (Lens culinaris subsp. culinaris) Domestication and Spread as Revealed by Genotyping-by-Sequencing of Wild and Landrace Accessions

“…In the phylogenetic analyses, all culinaris are clustered together and nested within orientalis. In accord with the view that monophyly indicates a single domestication event, as opposed to multiple ones, our data support a single origin for lentil, similar to the proposed origins of einkorn, emmer wheat, barley, maize, pearl millet, soja, carrot, and sunflower (Luo et al, 2007;Ross-Ibarra and Gaut, 2008;Honne and Heun, 2009;Guo et al, 2010;Dussert et al, 2015;Arbizu et al, 2016;Park and Burke, 2020). Notwithstanding, this interpretation has been disputed on methodological and biological grounds for other SWA crops (Allaby et al, 2008;Brown et al, 2009;Fuller et al, 2011).…”

Transcriptomics of developing wild sunflower seeds from the extreme ends of a latitudinal gradient differing in seed oil composition

“…As these individuals were grown in a common garden, variation in gene expression is likely due to genetic differences between populations. The clear differences in gene expression between populations from Texas and Canada were expected based on evidence that wild sunflower exhibits north-south divergence in terms of both genetic and phenotypic variation (Blackman et al, 2011; McAssey et al, 2016; Park and Burke, 2020). These patterns likely result, at least in part, from selection for adaptation to the drastic environmental differences between Texas and Canada; such selection might also have contributed to variation in the expression of genes related to environmental adaptation (Akman et al, 2016; Lasky et al, 2014).…”

“…In addition to being a model for ecological studies, wild sunflower is the progenitor of cultivated sunflower (also H. annuus ), which is one of the world’s most important oilseed crops. Cultivated sunflower was initially domesticated over 4,000 years ago in what is now the east-central USA as a source of edible seeds and for cultural purposes (Heiser, 1978; Park and Burke, 2020; Rieseberg and Seiler, 1990), and was later subjected to intense selection for increased seed oil concentration, as well as a shift in FA composition (Fick and Miller, 1997). Sunflower oil is a naturally rich source of oleic and linoleic acids (18:1 and 18:2 respectively, where the numbers represent the length of the carbon chain and the number of double bonds present [i.e., the degree of FA unsaturation]).…”

Aberrant RNA splicing due to genetic incompatibilities in sunflower hybrids

“…The cultivated sunflowers' transition to domestication began approximately 5000 years ago (Baute et al, 2015;Badouin et al 2017). This evolutionary shift was accompanied by a reduction in genetic diversity and differentiation from wild H. annuus (Park and Burke 2020). Additionally, domestication was associated with changes in mRNA splicing patterns, particularly for genes involved in seed development (Smith et al 2018).…”

“…Here, we investigate splicing irregularities and genetic incompatibilities in the common sunflower, Helianthus annuus. Although wild and domesticated common sunflower are the same species, domesticated sunflower varieties are resolved as a distinct clade in phylogenetic analyses; F ST between domesticated and wild H. annuus genotypes ranges from 0.32 to 0.46 (Park and Burke 2020). Plant domestication frequently includes the evolution of partial reproductive isolation between the domesticate and its wild progenitor (Dempewolf et al 2012).…”