Multiple chromosomal inversions contribute to adaptive divergence of a dune sunflower ecotype

Abstract

<jats:p>Both models and case studies suggest that chromosomal inversions can facilitate adaptation and speciation in the presence of gene flow by suppressing recombination between locally adapted alleles. Until recently, however, it has been laborious and time-consuming to identify and genotype inversions in natural populations. Here we apply RAD sequencing data and newly developed population genomic approaches to identify putative inversions that differentiate a sand dune ecotype of the prairie sunflower (<jats:italic>Helianthus petiolaris</jats:italic>) from populations found on the adjacent sand sheet. We detected seven large genomic regions that exhibit a different population structure than the rest of the genome and that vary in frequency between dune and non-dune populations. These regions also show high linkage disequilibrium and high heterozygosity between, but not within haplotypes, consistent with the behavior of large inversions, an inference subsequently validated in part by comparative genetic mapping. Genome-environment association analyses show that key environmental variables, including vegetation cover and soil nitrogen, are significantly associated with inversions. The inversions co-locate with previously described "islands of differentiation", and appear to play an important role in adaptive divergence and incipient speciation within <jats:italic>H. petiolaris</jats:italic>.</jats:p>

Frequency, Origins, and Evolutionary Role of Chromosomal Inversions in Plants

“…(B) Inversions become established through a process similar to (A) but by carrying a combination of alleles at two loci that are adapted to different aspects of the local environment (triangles and squares in different colors). For example, in a dune ecotype of the prairie sunflower (Helianthus petiolaris), larger seed size and tolerance to low nutrient soils were found to map to the same inversions (Huang et al, 2019;Todesco et al, 2019). (C) Mixed geographic model proposed by Feder et al (2011).…”

“…Surprisingly, inversions segregating within species often have no visible effect on fertility, such as reported for Brassica oleracea (Kianian and Quiros, 1992) and maize (Fang et al, 2012). In Mimulus and Helianthus, crosses between ecotypes that are separated only by inversions do not show reduced pollen viability (Lowry and Willis, 2010;Ostevik et al, 2016;Huang et al, 2019), although meiotic abnormalities diagnostic for inversions have been reported for interspecific crosses (Chandler et al, 1986). This suggests that the reduction in recombination associated with inversions within plant species is typically achieved by disrupting pairing and crossing over between inverted regions (Searle, 1993) rather than selection against inviable recombinant gametes.…”

“…Up to 74 inversions and 15 translocations were found across the five taxa. Lastly, Huang et al (2019) developed genetic maps for dune and non-dune ecotypes of H. petiolaris and successfully identified multiple inversions, but no translocations.…”

“…As with the LD method, analyses of genotypic relationships within the predicted inversion can offer further support for the putative inversion. The local population structure approach has been used to detect polymorphic inversions from RAD sequencing data or whole-genome shotgun data within the wild sunflower species, Helianthus annuus, H. argophyllus, and H. petiolaris (Huang et al, 2019;Todesco et al, 2019). While many of the inversions predicted by this method in sunflower have been subsequently confirmed via comparisons of reference sequences, comparative mapping, or Hi-C sequencing, two were not, indicating that these population genomic approaches can offer suggestive evidence of inversions, but are less diagnostic.…”

“…However, new data from Helianthus sunflowers implies that secondary contact and hybridization may contribute importantly to the establishment of large inversions. We used a combination of population genomic, comparative mapping, and HiC sequencing to detect numerous polymorphic inversions within Helianthus annuus, H. argophyllus and H. petiolaris (Huang et al, 2019;Todesco et al, 2019), which are sympatric and known to hybridize with multiple other species. However, when we applied a similar population genomic approach to the analyses of two Helianthus species that are largely (H. bolanderi; data from Owens et al, 2016) or completely (H. niveus; data from Zhang et al, 2019) allopatric, we failed to find clear signals of inversions (Figure 3).…”