Multiple strong postmating and intrinsic postzygotic reproductive barriers isolate florally diverse species of Jaltomata (Solanaceae)

Abstract

Divergence in phenotypic traits often contributes to premating isolation between lineages, but could also promote isolation at postmating stages. Phenotypic differences could directly result in mechanical isolation or hybrids with maladapted traits; alternatively, when alleles controlling these trait differences pleiotropically affect other components of development, differentiation could indirectly produce genetic incompatibilities in hybrids. Here, we determined the strength of 9 postmating and intrinsic postzygotic reproductive barriers among 10 species of Jaltomata (Solanaceae), including species with highly divergent floral traits. To evaluate the relative importance of floral trait diversification on the strength of these postmating barriers, we assessed their relationship to floral divergence, genetic distance, geographical context, and ecological differences, using conventional tests and a new linear mixed modeling approach. Despite close evolutionary relationships, all species pairs showed moderate to strong isolation. Nonetheless, floral trait divergence was not a consistent predictor of the strength of isolation; instead this was best explained by genetic distance, although we found evidence for mechanical isolation in one species, and an overall positive relationship between floral trait divergence and fruit set isolation across species pairs. Overall, our data indicate that intrinsic postzygotic isolation is more strongly associated with genome-wide genetic differentiation, rather than floral divergence.

A simple genetic architecture and low constraint allow rapid floral evolution in a diverse and recently radiating plant genus

“…BC 1 individuals tended to have lower seed set and poorer quality seeds (decreased viability and response to germination‐inducing stimuli), and the recombinant BC population contained a subset of highly sterile individuals. The segregation of recombinant individuals with reduced viability and fertility often occurs in hybrids (Baack et al ., ), including in hybrids from additional Jaltomata species pairs (Kostyun & Moyle, ). Such patterns are typically a result of deleterious epistatic interactions between loci that have diverged between the two parental lineages, as has been shown in close relatives, including tomatoes (Moyle & Nakazato, ; Sherman et al ., ).…”

“…; Supporting Information Table S1). J. sinuosa has large rotate flowers with purple petals and a small amount of concentrated nectar (consistent with bee pollination; Fenster et al ., ; Mione et al ., ), whereas J. umbellata has small short‐tubular flowers with yellowish‐white petals and a large amount of dilute, but dark red, nectar that is visible through the corolla tube (Kostyun & Moyle, ). The tubular corollas, large volume of nectar, exerted reproductive organs, and red coloration observed in this species are consistent with hummingbird pollination (Fenster et al ., ).…”

“…Interestingly, this trait combination (large flowers with copious dark nectar) is actually not exhibited by either parental species used in this experiment (Fig. ; Table ); however, it is found in numerous other Jaltomata species and is consistent with suspected pollination syndromes within the genus (see later; Miller et al ., ; Kostyun & Moyle, ). Correlated changes in corolla size and nectar volume have also been observed in several other systems, including those with documented or hypothesized pollinator shifts (e.g.…”

“…Viable F 1 individuals in both directions of the cross produce flowers that are phenotypically intermediate between the parental genotypes (Fig. ) and retain reduced but sufficient fertility when backcrossed to parents (Kostyun & Moyle, ). Because we were especially interested in the genetic basis of red nectar and a fused corolla tube (exhibited by J. umbellata , present but less pronounced in F 1 individuals, but absent in J. sinuosa ; Figs , S1), we generated the mapping population by backcrossing a single J. sinuosa × J. umbellata F 1 (as the ovule parent) to the original parental J. sinuosa individual (as the pollen parent).…”

“…J. sinuosa is distributed along the Andes in South America from Venezuela to Bolivia, whereas J. umbellata is restricted to lomas formations along the Peruvian coast. Both species are self‐compatible (Kostyun & Moyle, ) and shrubby, but differ in leaf traits such as overall size and shape, and type of trichomes. This species pair also has several incomplete, intrinsic postzygotic reproductive barriers, including quantitatively reduced fruit set and hybrid seed viability (Kostyun & Moyle, ).…”