Pervasive ‘Less-Than-Additive’ Interactions Characterize Fitness Effects in Wide Solanum Crosses

Both heterosis and hybrid incompatibility share common features: both manifest in wide crosses, and both involve interactions between divergent alleles and/or loci that produce transgressive phenotypes. Focusing on the genetics of hybrid incompatibility, we systematically examined the prevalence of fertility-affecting interactions between pairs of short chromosomal regions from one species when co-introgressed into a heterospecific genetic background. We used a diallel crossing design to generate all pairwise combinations of 15 chromosomal segments from S. habrochaites in the background of S. lycopersicum (i.e., 95 double introgression lines). We compared the pollen and seed fertility expressed in each double introgression line to the expected additive effect of its two component single introgressions, and found that: epistasis was common among co-introgressed regions; epistastic effects were overwhelmingly antagonistic (i.e., double hybrids were less unfit than expected from additive single introgression effects); and, epistasis was substantially more prevalent in pollen fertility compared to seed fertility phenotypes. The first two patterns are similar to those observed for heterotic yield traits among Solanum species, and suggest that ‘less-than-additive’ high-order interactions frequently contribute to both heterosis and postzygotic sterility barriers in these species.