Microsatellite signature of ecological selection for salt tolerance in a wild sunflower hybrid species, Helianthus paradoxus

Abstract

The hybrid sunflower species Helianthus paradoxus inhabits sporadic salt marshes in New Mexico and southwest Texas, USA, whereas its parental species, Helianthus annuus and Helianthus petiolaris, are salt sensitive. Previous studies identified three genomic regions - survivorship quantitative trait loci (QTLs) - that were under strong selection in experimental hybrids transplanted into the natural habitat of H. paradoxus. Here we ask whether these same genomic regions experienced significant selection during the origin and evolution of the natural hybrid, H. paradoxus. This was accomplished by comparing the variability of microsatellites linked to the three survivorship QTLs with those from genomic regions that were neutral in the experimental hybrids. As predicted if one or more selective sweeps had occurred in these regions, microsatellites linked to the survivorship QTLs exhibited a significant reduction in diversity in populations of the natural hybrid species. In contrast, no difference in diversity levels was observed between the two microsatellite classes in parental populations.

Fig. 1

Principal components analysis of allele size variation across the 12 microsatellite loci in Helianthus annuus (crosses), Helianthus paradoxus (closed circles), and Helianthus petiolaris (squares). The contribution of each microsatellite to each component is computed to maximize the difference between individuals. Vectors represented by black lines indicate the contribution of PSR microsatellites, whereas red line vectors show the contribution of PUR markers. The first two components explain 59% of the total variation for allele sizes.

Fig. 2

Comparison of variability levels (means and standard errors) between microsatellites in PSRs (grey) and in PURs (white). (a) gene diversity, He; (b) allelic richness, Rs; (c), lnRH of Helianthus paradoxus over Helianthus annuus and over Helianthus petiolaris, respectively; (d) lnRV of H. paradoxus over each one of its parents. Note that standard errors do not take into account population effects and therefore cannot be used to test for differences between microsatellite classes in H. paradoxus.

Fig. 3

Results of a blind-test performed on the genetic diversity estimator (He) in Helianthus paradoxus. For each microsatellite, the frequency of the marker in the class with the lower diversity is in white. The difference between classes for the level of genetic diversity was assessed by the summary statistic S, and S_0.05 was computed as the threshold value for rejecting the null hypothesis of no diversity differences between classes at the probability level α = 0.05. The frequency at which S exceeds S_0.05 is in grey, stars indicate when S exceeds S_0.001.