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

Abstract

Summary Genetic correlations among different components of phenotypes, especially those 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 quantitative trait locus (QTL) distribution) underlying 25 floral and fertility traits. We found that most floral traits had a relatively simple genetic basis (few, predominantly additive, QTLs of moderate to large effect), as well as little evidence of antagonistic pleiotropy (few trait correlations and QTL colocalization, 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.

Comparative analysis of corolla tube development across three closely related Mimulus species with different pollination syndromes

“…Because of its obvious importance in flower‐pollinator interactions, corolla tube length variation has been subjected to quantitative trait locus (QTL) mapping analyses in several plant lineages, including Mimulus (Bradshaw et al, 1998; Fishman et al, 2015), Petunia (Stuurman et al, 2004), Leptosiphon (Goodwillie et al, 2006), Ipomopsis (Nakazato et al, 2013), Penstemon (Wessinger et al, 2014), and Jaltomata (Kostyun et al, 2019). These studies show that tube length is clearly a polygenic trait.…”

Pollination syndromes in the 21st century: where do we stand and where may we go?

“…reward and corolla shape in Penstemon , Wessinger et al ., 2014; flower size and nectar in Jaltomata , Kostyun et al ., 2019) or to linked, but independent, gene clusters (e.g. colour, scent and reproductive organ length in Petunia, Hermann et al ., 2013; Kostyun et al ., 2019). Both processes allow the rapid adaptation of multiple traits to changing pollinator selection regimes.…”

“…Molecular developmental studies, experimental manipulations, selection studies and QTL screening have the capacity to get to the core of these questions (Bolstad et al ., 2014; Wessinger et al ., 2014). In recent years, particular focus has been placed on studying the advertisement traits colour and scent (each trait included in 33% of studies in the literature review, but also see Kostyun et al ., 2019). In several pollination‐syndrome model systems (e.g.…”

Modularity and selection of nectar traits in the evolution of the selfing syndrome in Ipomoea lacunosa (Convolvulaceae)

“…QTL studies often infer properties of the genetic architecture of divergence from patterns of QTL overlap (e.g. Slotte et al, 2012;Wessinger et al, 2014;Kostyun et al, 2019). Seldom are these inferences evaluated by comparing the patterns of QTL overlap and the actual genetic correlations among traits.…”

“…Numerous studies have identified QTLs for floral traits that differ between two species, and many have made inferences about the genetic architecture of divergence based on QTL overlaps (Slotte et al, 2012;Wessinger et al, 2014;Kostyun et al, 2019). However, studies rarely evaluate the validity of these inferences.…”