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 BC2 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 F1's between the hybrid and parental species fall below 11%, which is sufficient for evolutionary independence of the hybrid neospecies.

Figure 1.

Present-day distributions of the two parental species, H. annuus and H. petiolaris, and their three hybrid-derivative species, H. anomalus, H. deserticola, and H. paradoxus (based on Rogers et al. 1982).

Figure 2.

Gene order relationships for a representative linkage group (LG2) between two parental sunflower species, H. annuus and H. petiolaris, and their three diploid hybrid derivatives, H. anomalus, H. deserticola, and H. paradoxus. Note the fission of LG2 in H. paradoxus and the fusion of linkages 2 and 8 in H. anomalus and H. petiolaris. Markers beginning with ORS are simple sequence repeats (SSRs), those beginning with AFP are AFLPs, and those beginning with RPD are RAPDs. Markers followed by species names in parentheses (ann, annuus; ano, anomalus; par, paradoxus; and pet, petiolaris) are informative and map to the same linkage group in the listed species. Informative loci on adjacent linkage groups are also connected by lines. Numbers to the left of each linkage group refer to genetic distance (centimorgans). Single arrows indicate the location of inferred chromosomal breakages/fusions that are necessary to account for the differences between this map and that of H. annuus (Figure S4 at http://www.genetics.org/supplemental/). Letters (A and B) following some linkage group designations indicate fragmented linkage groups, with fragments homologous to the top of the H. annuus linkage group designated A, the next highest fragment labeled B, and so forth.

Figure 3.

Inferred chromosomal structural relationships between the parental species, H. annuus and H. petiolaris, and their three diploid hybrid derivatives, H. anomalus, H. deserticola, and H. paradoxus. Segments containing inversions are indicated by hatched lines. Note that there was insufficient marker density in H. deserticola and H. paradoxus to evaluate the presence or absence of inversions. Asterisks indicate the approximate position of pollen viability QTL (cf. Table 3).

Figure 3.

Inferred chromosomal structural relationships between the parental species, H. annuus and H. petiolaris, and their three diploid hybrid derivatives, H. anomalus, H. deserticola, and H. paradoxus. Segments containing inversions are indicated by hatched lines. Note that there was insufficient marker density in H. deserticola and H. paradoxus to evaluate the presence or absence of inversions. Asterisks indicate the approximate position of pollen viability QTL (cf. Table 3).

Figure 4.

Percentage seed set of first-generation hybrids between the parental species, H. annuus and H. petiolaris, and their three diploid hybrid derivatives, H. anomalus, H. deserticola, and H. paradoxus. Values are presented as mean (standard error). Line thickness is proportional to cross-compatibility. Dashed lines indicate that some individuals were completely sterile for that cross. Values for crosses among H. annuus, H. petiolaris, and H. anomalus derive from Rieseberg (2000).