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

Abstract

Genetic correlations among different components of phenotypes, especially resulting from pleiotropy, can constrain or facilitate trait evolution. These factors could especially influence the evolution of traits that are functionally integrated, such as those comprising the flower. Indeed, pleiotropy is proposed as a main driver of repeated convergent trait transitions, including the evolution of phenotypically-similar pollinator syndromes. We assessed the role of pleiotropy in the differentiation of floral and other reproductive traits between two species —Jaltomata sinuosa and J. umbellata (Solanaceae)—that have divergent suites of floral traits consistent with bee- and hummingbird-pollination, respectively. To do so, we generated a hybrid population and examined the genetic architecture (trait segregation and QTL distribution) underlying 25 floral and fertility traits. We found that most floral traits had a relatively simple genetic basis (few, predominantly additive, QTL of moderate to large effect), as well as little evidence of antagonistic pleiotropy (few trait correlations and QTL co-localization, particularly between traits of different classes). However, we did detect a potential case of adaptive pleiotropy among floral size and nectar traits. These mechanisms may have facilitated the rapid floral trait evolution observed within Jaltomata, and may be a common component of rapid phenotypic change more broadly.