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

Abstract

Pollinators are important in the evolution of flowering plants, but questions remain about how early stages of pollinator-mediated speciation arise. Studying intraspecific variation in floral traits can shed light on early stages of floral trait divergence and identify how traits evolve as signals to novel pollinators, either acting separately or in concert. Among two hummingbird- pollinated species of monkeyflowers (Mimulussection Erythranthe),M. cardinalisandM. verbenaceus, yellow floral morphs have arisen from more common, red-flowered morphs and have become well-established in several populations. To identify 1) whether these floral transitions involve additional floral traits beyond color and 2) if they represent incipient pollinator shifts, we characterized yellow-flowered morphs ofM. verbenaceusandM. cardinalisand their more common red-flowered forms across numerous floral traits (reflectance, pigmentation, volatile organic compounds, morphology, and nectar) and assessed pollinator perception and preference of floral signals by a novel bumblebee pollinator (Bombus terrestris ssp. audax). The two yellow morphs appeared to follow independent evolutionary paths, resulting in distinct hues of yellow that varied in reflectance, pigmentation, and perception by bees. For floral scent, both yellow forms differed from their red conspecific forms: in one case increasing total emissions of a similar scent profile (M. verbenaceus), and in the other, emitting a distinct scent profile at similarly low levels (M. cardinalis). In both species, yellow morphs had wider, less restrictive corolla openings and greater herkogamy than red flowers but produced similar nectar rewards. Collectively, these floral trait differences resulted in a clear preference for yellow floral morphs in both species, with naïve bumblebees choosing yellow flowers twice as often as red forms. Despite the increased attractiveness of yellow morphs, bumblebees had difficulty handling flowers to access rewards, suggesting they may be ineffective pollinators to current floral phenotypes. This study reveals that parallel transitions in floral color in two monkeyflower species involve a suite of changes to other floral traits which directly impacts interactions with potential pollinators. This work highlights the value of integrative studies of intraspecific floral phenotypes and behavioral responses of pollinators to understand incipient pollinator shifts and the potential for future pollinator-mediated floral evolution.

Adaptive generalization in pollination systems: Hawkmoths increase fitness to long‐tubed flowers, but secondary pollinators remain important

“…Diplacus (Short & Streisfeld, 2023 ), which could provide one hypothesis explaining how yellow flowers in C. sessiliflora may have arisen, especially in areas of range overlap with C. citrina . Alternatively, ancestral polymorphisms in floral color that precede speciation events (Sánchez‐Cabrera et al., 2023 ) or convergent shifts in floral color among related species (Stone & Wessinger, 2024 ; Thomson & Wilson, 2008 ; Wenzell et al., 2024 ) provide alternate explanations which require further study.…”

Adaptive generalization in pollinators: hawkmoths increase fitness to long-tubed flowers, but secondary pollinators remain important

“…Diplacus (Short and Streisfeld, 2023), which could provide one hypothesis explaining how yellow flowers in C. sessiliflora may have arisen, especially in areas of overlap with C. citrina. Alternatively, ancestral polymorphisms in floral color that precede speciation events (Sánchez-Cabrera et al, 2023) or convergent shifts in floral color among related species (Thomson and Wilson, 2008;Wenzell et al, 2023a;Stone and Wessinger, 2024) provide alternate explanations which require further study.…”