Evolution of floral scent in relation to self-incompatibility and capacity for autonomous self-pollination in the perennial herbArabis alpina

Abstract

Background and Aims The transition from outcrossing to selfing is a frequent evolutionary shift in flowering plants and is predicted to result in reduced allocation to pollinator attraction if plants can self-pollinate autonomously. The evolution of selfing is associated with reduced visual floral signalling in many systems, but effects on floral scent have received less attention. We compared multiple populations of the arctic–alpine herb Arabis alpina (Brassicaceae), and asked whether the transition from self-incompatibility to self-compatibility has been associated with reduced visual and chemical floral signalling. We further examined whether floral signalling differ between self-compatible populations with low and high capacity for autonomous self-pollination, as would be expected if benefits of signalling decrease with reduced dependence on pollinators for pollen transfer. Methods In a common garden we documented flower size and floral scent emission rate and composition in eight self-compatible and nine self-incompatible A. alpina populations. These included self-compatible Scandinavian populations with high capacity for autonomous self-pollination, self-compatible populations with low capacity for autonomous self-pollination from France and Spain, and self-incompatible populations from Italy and Greece. Key Results The self-compatible populations produced smaller and less scented flowers than the self-incompatible populations. However, flower size and scent emission rate did not differ between self-compatible populations with high and low capacity for autonomous self-pollination. Floral scent composition differed between self-compatible and self-incompatible populations, but also varied substantially among populations within the two categories. Conclusions Our study demonstrates extensive variation in floral scent among populations of a geographically widespread species. Contrary to expectation, floral signalling did not differ between self-compatible populations with high and low capacity for autonomous self-pollination, indicating that dependence on pollinator attraction can only partly explain variation in floral signalling. Additional variation may reflect adaptation to other aspects of local environments, genetic drift, or a combination of these processes.

Phenotypic plasticity in floral scent in response to nutrient, but not water, availability in the perennial plant Arabis alpina

“…Plants in each treatment received the following volumes and concentrations of fertilizer: (a) 60 ml water, 0.3 g/L fertilizer; (b) 30 ml water, 0.6 g/L fertilizer; (c) 60 ml water, 0.03 g/L fertilizer or (d) 30 ml water, 0.06 g/L fertilizer. Fertilizer concentrations were chosen such that the high‐nutrient treatment consisted of the amount of fertilizer used to maintain A. alpina in the greenhouse in a previous study (Petrén et al., 2021), and the plants of the low‐nutrient treatment received 1/10 of this amount. The resulting sizes of plants growing in both nutrient treatments corresponded well to the size variation detected within natural populations (personal observation) (see Section 3).…”

“…We also excluded peaks corresponding to green leaf volatiles as determined by the leaf samples. Compound identities were determined using a combination of retention time and mass spectrum data from the NIST library (NIST98 Mass Spectral Library with Windows Search Program Version 2.0, Standard Reference Database 1A), and cross‐referenced with compounds we detected in a previous study of A. alpina (Petrén et al., 2021). These were identified by a combination of Kovats retention index analysis and co‐chromatography of synthetic compounds (Table S2).…”

“…Additionally, the mating system variation provides the opportunity to compare the sensitivity of fragrance to environmental conditions between plants that putatively rely heavily on floral attractive traits for reproduction (self‐incompatible plants) and plants for which volatile production may be less important for fitness (self‐compatible plants; cf. Petrén et al., 2021). One might predict higher relative plasticity in floral attractive traits such as fragrance in self‐compatible plants than in self‐incompatible plants, since self‐compatible plants generally tend to show lower pollen limitation than self‐incompatible plants (Larson & Barrett, 2000) and so may experience relaxed selection for pollinator attraction.…”

“…The majority of angiosperm plant species rely on animal pollinators for reproduction (Ollerton et al., 2011), and pollinator‐mediated selection is thought to have contributed to the incredible diversity of floral morphological and chemical traits observed among flowering plant species (Bradshaw & Schemske, 2003; Campbell et al., 1997; Darwin, 1862; Schemske & Bradshaw, 1999; Waelti et al., 2008). In addition to variation among species, floral traits can vary dramatically among populations of the same species (Delph et al., 2002; Schlumpberger et al., 2009), and floral scent is no exception (Delle‐Vedove et al., 2017; Dötterl et al., 2005; Friberg et al., 2019; Petrén et al., 2021). Floral volatiles can play significant roles in interactions with both pollinators and other organisms, including microbes, herbivores and nectar thieves (Galen et al., 2011; Huang et al., 2012; Junker et al., 2011).…”

“…Arabis alpina is suitable for studies of phenotypic plasticity and the potential costs of floral scent production for several reasons. First, the floral scent of A. alpina has previously been characterized (Petrén et al., 2021), facilitating compound identification and optimization of scent collection protocols. Additionally, the mating system variation provides the opportunity to compare the sensitivity of fragrance to environmental conditions between plants that putatively rely heavily on floral attractive traits for reproduction (self‐incompatible plants) and plants for which volatile production may be less important for fitness (self‐compatible plants; cf.…”