Genomic Patterns of Adaptive Divergence between Chromosomally Differentiated Sunflower Species

Abstract

Understanding the genetic mechanisms of speciation and basis of species differences is among the most important challenges in evolutionary biology. Two questions of particular interest are what roles divergent selection and chromosomal differentiation play in these processes. A number of recently proposed theories argue that chromosomal rearrangements can facilitate the development and maintenance of reproductive isolation and species differences by suppressing recombination within rearranged regions. Reduced recombination permits the accumulation of alleles contributing to isolation and adaptive differentiation and protects existing differences from the homogenizing effects of introgression between incipient species. Here, we examine patterns of genetic diversity and divergence in rearranged versus collinear regions in two widespread, extensively hybridizing sunflower species, Helianthus annuus and Helianthus petiolaris, using sequence data from 77 loci distributed throughout the genomes of the two species. We find weak evidence for increased genetic divergence near chromosomal break points but not within rearranged regions overall. We find no evidence for increased rates of adaptive divergence on rearranged chromosomes; in fact, collinear chromosomes show a far greater excess of fixed amino acid differences between the two species. A comparison with a third sunflower species indicates that much of the nonsynonymous divergence between H. annuus and H. petiolaris probably occurred during or soon after their formation. Our results suggest a limited role for chromosomal rearrangements in genetic divergence, but they do document substantial adaptive divergence and provide further evidence of how species integrity and genetic identity can be maintained at many loci in the face of extensive hybridization and gene flow.

A recombination suppressor contributes to ecological speciation in OSTRINIA moths

“…Our results add to the limited number of studies that provide empirical support for this notion, including apple maggot flies (Feder et al, 2003;Michel et al, 2010;Powell et al, 2013), fruit flies (Noor et al, 2001;Kulathinal et al, 2009), stickleback fishes (Kitano et al, 2009), sunflowers (Rieseberg, 2001;Strasburg et al, 2009) and monkeyflowers (Lowry and Willis, 2010;Fishman et al, 2013). Our finding that structural mutations contribute to speciation may be the first of many for Lepidoptera.…”

“…An additional role of suppressed recombination for evolutionary divergence involves repeated bouts of gene exchange and disruptive selection. Specifically, barrier loci within inversions under the Navarro-Barton model (Navarro and Barton, 2003) might produce a molecular signal of differentiation that is spread across the inversion or at least near its breakpoints (Rieseberg, 2001;Noor et al, 2001;Strasburg et al, 2009;McGaugh and Noor, 2012) because of selective purging of maladapted (and nonrecombining) regions encompassed by inversions upon their introduction into sister taxa. Such a process might be analogous to 'differential introgression,' in which gene flow is restricted at individual barrier loci but is high elsewhere (Barton and Bengtsson, 1986;Wu, 2001;West and Via, 2008;Harrison, 2012).…”

Genomic impacts of chromosomal inversions in parapatricDrosophilaspecies

“…The D. pseudoobscura-D. persimilis system satisfies all requirements [6,15,16,47] [3,39]. Between D. pseudoobscura and D. persimilis for intergenic regions, breakpoints for the XL chromosome did not exhibit higher divergence relative to that observed inside the inversions.…”

“…Between some species, regions of high divergence appear to have been established and maintained purely by selection (reviewed in [1]). In others, establishment and maintenance of regions of high divergence appears facilitated by structural differences between species [2,3].…”

“…This suppressed effective recombination between heterokaryotypes of paracentric inversions may facilitate speciation by protecting locally adapted alleles inside the inversions from gene flow with other populations, allowing further divergence between two karyotypes (reviewed in earlier studies [9,10]). While theoretical [11 -14] and empirical [15 -21] support for this hypothesis exists, the maintenance of genomic divergence-within inversions over long time periods (many hundreds of thousands of generations), and the shape of elevated divergence-within inversions have been less explored empirically (but see [2][3][4][5]). …”