Within-species floral evolution reveals convergence in adaptive walks during incipient pollinator shift

Abstract

Understanding how evolution proceeds from molecules to organisms to interactions is critical for evolutionary biology and requires integrative studies that span biological levels. By linking phenotypic changes with associated genes and fitness implications, we gain insight on the repeatability of evolution and how adaptive walks move organisms between fitness peaks, which remains poorly understood at intermediate stages, e.g. potential fitness valleys. Floral trait evolution can proceed rapidly, confer reproductive isolation, and provides numerous examples of convergent evolution associated with pollinator guilds. Within the monkeyflowers (Mimulus sect. Erythranthe), intraspecific shifts to yellow flowers within red hummingbird-pollinated species have arisen at least twice and may represent incipient shifts between optima of pollinator adaptation. Here, we compare two natural yellow-flowered forms of M. cardinalis and M. verbenaceus to their red conspecifics in floral phenotypes, biochemistry, transcriptomic and genomic variation, and interactions with pollinators. We find convergent evolution in the adaptive walks of yellow morphs in both species, with consistent changes in traits of large effect (floral pigments and associated gene expression), which result in strong preference for yellow flowers by bumblebees. Shifts in additional traits (scent emissions and floral opening size) are also consistent with bee pollination, which may represent smaller-effect steps in an ongoing walk from hummingbird to bee pollination. By examining intraspecific variation representing incipient pollinator shifts in two related species, this work elucidates how adaptive walks proceed at early stages by highlighting how convergent large effect mutations (floral color) may drive pollinator attraction, preceding smaller effect changes controlling pollinator fit and reward access. This work integrates phenotypic, biochemical, genomic, and behavioral evidence to shed light on how repeated steps in adaptive walks to new fitness optima may impact reproductive isolation and incipient speciation via convergent evolution.