Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species

Abstract

New species may arise via hybridization and without a change in ploidy. This process, termed homoploid hybrid speciation, is theoretically difficult because it requires the development of reproductive barriers in sympatry or parapatry. Theory suggests that isolation may arise through rapid karyotypic evolution and/or ecological divergence of hybrid neospecies. Here, we investigate the role of karyotypic change in homoploid hybrid speciation by generating detailed genetic linkage maps for three hybrid sunflower species, Helianthus anomalus, H. deserticola, and H. paradoxus, and comparing these maps to those previously generated for the parental species, H. annuus and H. petiolaris. We also conduct a quantitative trait locus (QTL) analysis of pollen fertility in a BC 2 population between the parental species and assess levels of pollen and seed fertility in all cross-combinations of the hybrid and parental species. The three hybrid species are massively divergent from their parental species in karyotype; gene order differences were observed for between 9 and 11 linkage groups (of 17 total), depending on the comparison. About one-third of the karyoypic differences arose through the sorting of chromosomal rearrangements that differentiate the parental species, but the remainder appear to have arisen de novo (six breakages/six fusions in H. anomalus, four breakages/three fusions in H. deserticola, and five breakages/five fusions in H. paradoxus). QTL analyses indicate that the karyotypic differences contribute to reproductive isolation. Nine of 11 pollen viability QTL occur on rearranged chromosomes and all but one map close to a rearrangement breakpoint. Finally, pollen and seed fertility estimates for F 1 's between the hybrid and parental species fall below 11%, which is sufficient for evolutionary independence of the hybrid neospecies.

Evolution of reproductive isolation in plants

“…First, several of the QTL conferring pollen sterility, an important intrinsic isolating barrier, map to collinear regions of the Helianthus genome, consistent with the action of genic isolation factors in addition to chromosomal ones (Rieseberg et al, 1999). Second, epistatic interactions among sterility QTL that do map to chromosomal rearrangements generally do not involve linkage groups that are part of the same multivalent configuration during meiosis (Lai et al, 2005). Both observations suggest that the effects of rearrangements on reproductive isolation are not due to their…”

Identification and mapping of SNPs from ESTs in sunflower

“…The RILs were developed by single-seed descent from the same two cultivars (RHA280 and RHA801) employed for the majority of EST sequencing. A dense map of anonymous markers already exists for this population Yu et al 2003); consequently, it has become the primary reference population for molecular breeding and comparative genomics research in sunflower (e.g., Burke et al 2004;Lai et al 2005). Ninety-four RILs from this cross were employed for population screening and map construction.…”

“…However, shortly thereafter several restriction fragment length polymorphism maps were published for the domesticated sunflower (Berry et al 1995;Gentzbittel et al 1995Gentzbittel et al , 1999Jan et al 1998), establishing a standard nomenclature for sunflower linkage groups and providing framework markers for comparisons among maps (Gedil et al 2001). More recently, high-resolution linkage maps based on more than 1,000 simple sequence repeat (SSR) and other sequence-tagged-site markers have been developed for the cultivated sunflower Yu et al 2003) and several wild species Burke et al 2004;Lai et al 2005).…”

Different scales of Ty1/copia-like retrotransposon proliferation in the genomes of three diploid hybrid sunflower species

“…These species, Helianthus anomalus, H. deserticola, and H. paradoxus, are independently derived via hybridization events between the same two parental taxa, H. annuus and H. petiolaris (Rieseberg, 1997;Lai et al, 2005). The three hybrid taxa occupy habitats considered abiotically extreme relative to either parental species (Rieseberg et al, 2003).…”