Reconstructing the History of Selection during Homoploid Hybrid Speciation

Abstract

This study aims to identify selection pressures during the historical process of homoploid hybrid speciation in three Helianthus (sunflower) hybrid species. If selection against intrinsic genetic incompatibilities (fertility selection) or for important morphological/ecological traits (phenotypic selection) were important in hybrid speciation, we would expect this selection to have influenced the parentage of molecular markers or chromosomal segments in the hybrid species' genomes. To infer past selection, we compared the parentage of molecular markers in high-density maps of the three hybrid species with predicted marker parentage from an analysis of fertility selection in artificial hybrids and from the directions of quantitative trait loci effects with respect to the phenotypes of the hybrid species. Multiple logistic regression models were consistent with both fertility and phenotypic selection in all three species. To further investigate traits under selection, we used a permutation test to determine whether marker parentage predicted from groups of functionally related traits differed from neutral expectations. Our results suggest that trait groups associated with ecological divergence were under selection during hybrid speciation. This study presents a new method to test for selection and supports earlier claims that fertility selection and phenotypic selection on ecologically relevant traits have operated simultaneously during sunflower hybrid speciation. Keywords ecological selection; fertility selection; homoploid hybrid speciation; Helianthus; permutation test; quantitative trait loci (QTLs)A major goal of evolutionary biology is to assess the relative importance of evolutionary factors responsible for present-day phenotypes and species differences. Studies of contemporary populations can identify traits currently under selection and connect the direction and intensity of selection to environmental variables (Lande and Arnold 1986). These kinds of studies are necessarily short-term, however, and their utility for reconstructing the history of selection is questionable because of temporal variation in the environment and in genotype-environment interactions (Agrawal et al. 2001;Hoekstra et al. 2001;Grant and Grant 2002). Comparative studies of phenotypic differences between species or higher taxa, on the other hand, typically fail to distinguish between phenotypic changes caused by selection and those resulting from neutral processes. Likewise, studies on the genetic footprints of selection can reveal genomic targets of recent selective sweeps but do not necessarily connect these targets to phenotypes or to the selective forces involved (reviewed in Nielsen 2005; but see Orr 1998). Homoploid hybrid species offer a unique opportunity for estimating the relative importance of drift and selection in evolution as well as for identifying traits or trait groups that are the direct targets of selection. During homoploid hybrid speciation, hybridization between chromosomally or genetically divergent spe...

A Natural Homoploid Hybrid between Centaurea horrida and Centaurea filiformis (Asteraceae) as Revealed by Morphological and Genetic Traits

“…Several cases of fertile homoploid natural hybrid populations were previously reported within Centaurea (Fernández Casas and Susanna 1986) and in other Asteraceae genera, such as Senecio L. (López et al 2008) and Helianthus L. (Gross et al 2003), as well as in other plant families (Howarth and Baum 2005;Pan et al 2007;Wang et al 2008). Even if homoploid hybrid speciation has traditionally been considered a rare event, recent studies suggest this phenomenon may be more frequent than previously considered (Chapman and Burke 2007;Karrenberg et al 2007;Rieseberg and Willis 2007;Buerkle and Rieseberg 2008;Seehausen et al 2008). …”

Genomic collinearity and the genetic architecture of floral differences between the homoploid hybrid species Iris nelsonii and one of its progenitors, Iris hexagona

“…A majority of homoploid hybrid species described to date have a mosaic genome (mosaic genome hybrid speciation; Jiggins et al, 2008), where genomic differences are sorted in the hybrid genome through both fertility and ecological selection (Karrenberg et al, 2007). In the most well studied of these systems, chromosomal rearrangements have a substantial role in strong postzygotic isolation between several independently derived homoploid hybrid sunflower species and their progenitors (Rieseberg et al, 1995;Rieseberg, 2000;Lai et al, 2005), as was predicted in earlier verbal models of homoploid hybrid speciation (Grant, 1971).…”

A genomic view of introgression and hybrid speciation

“…Analysis of genome structure in three synthetic and three natural hybrid species of sunflower revealed massive karyotypic change over a handful of hybrid generations [31,32]. While some of the karyotypic differences arose through the sorting of chromosomal rearrangements that distinguish the parental species, most arose de novo.…”

“…The most detailed analysis of the evolutionary forces responsible for fixing favored combinations of parental alleles or chromosomal segments in hybrids focused on recombination in the homoploid hybrid sunflowers [31]. Analysis revealed that selection on ecological traits had slightly higher power than selection for fertility when predicting hybrid genomic composition, although both forms of selection were significant.…”