Differential strengths of selection on S-RNases from Physalis and Solanum (Solanaceae)

Abstract

Abstract

Background: The S-RNases of the Solanaceae are highly polymorphic self-incompatibility (S-) alleles subject to strong balancing selection. Relatively recent diversification of S-alleles has occurred in the genus Physalis following a historical restriction of S-allele diversity. In contrast, the genus Solanum did not undergo a restriction of S-locus diversity and its S-alleles are generally much older. Because recovery from reduced S-locus diversity should involve increased selection, we employ a statistical framework to ask whether S-locus selection intensities are higher in Physalis than Solanum . Because different S-RNase lineages diversify in Physalis and Solanum , we also ask whether different sites are under selection in different lineages.

Results: Maximum-likelihood and Bayesian coalescent methods found higher intensities of selection and more sites under significant positive selection in the 48 Physalis S-RNase alleles than the 49 from Solanum . Highest posterior densities of dN/dS (ω) estimates show that the strength of selection is greater for Physalis at 36 codons. A nested maximum likelihood method was more conservative, but still found 16 sites with greater selection in Physalis . Neither method found any codons under significantly greater selection in Solanum . A random effects likelihood method that examines data from both taxa jointly confirmed higher selection intensities in Physalis , but did not find different proportions of sites under selection in the two datasets. The greatest differences in strengths of selection were found in the most variable regions of the S-RNases, as expected if these regions encode self-recognition specificities. Clade-specific likelihood models indicated some codons were under greater selection in background Solanum lineages than in specific lineages of Physalis implying that selection on sites may differ among lineages.

Conclusions: Likelihood and Bayesian methods provide a statistical approach to testing differential selection across populations or species. These tests appear robust to the levels of polymorphism found in diverse S-allele collections subject to strong balancing selection. As predicted, the intensity of selection at the S-locus was higher in the taxon with more recent S-locus diversification. This is the first confirmation by statistical test of differing selection intensities among self-incompatibility alleles from different populations or species.