Range‐wide floral trait variation reflects shifts in pollinator assemblages, consistent with pollinator‐mediated divergence despite generalized visitation

Abstract

Floral trait evolution mediated by pollinators is important in the diversification of flowering plants, yet few studies have demonstrated the range-wide geographic variation in both floral traits and pollinators which represents a predicted precursor for pollinator-mediated speciation. This study explores whether geographic variation in pollinator interactions underlies the observed patterns of floral divergence both 1) among species of the Castilleja purpurea complex (C. purpurea, C. citrina and C. lindheimeri) and the congener C. sessiliflora, as well as 2) within C. sessiliflora, across its wide geographic range. We sampled floral visitors and floral traits (morphology and color) at 23 populations across a 1900 km-wide study area in 1-3 years, with reproductive fitness (fruit set) data for 18 of these populations. A wide diversity of pollinator functional groups visited the focal species, including bees, butterflies, hawkmoths and hummingbirds, and visitor assemblages varied among species and across geography. We identified relationships between floral traits and visitation by certain pollinator groups, which often aligned with predictions based on pollination syndromes. Despite visitor assemblages being largely generalized across most populations, we found that the observed changes in floral traits were associated with shifts in the relative frequencies of key pollinator functional groups. Hence this study demonstrates that variation in pollinator assemblages across the distributions of taxa may underlie divergence in floral traits and suggests that highly specialized relationships may not be required for early stages of pollinator-mediated floral divergence. Our extensive sampling of 23 populations over multiple years across a large geographic area highlights the value of range-wide studies for characterizing patterns of divergence mediated by ecological interactions.

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

“…Additionally, Manduca sexta preferred yellow flowers over red in controlled experiments with crosses of M. cardinalis and M. lewisii , lending support for this possibility (Byers and Bradshaw, 2021). Additionally, shifts from hummingbird to moth pollination have occurred repeatedly in other well characterized systems such as Aquilegia (Whittall and Hodges, 2007), and may reflect that many hawkmoths are generalist visitors (Wenzell et al, 2023, others), which are often underreported when pollinator observations take place only during daylight hours, as in previous observations of visitors to these floral morphs (Vickery 1992). Alternatively, observed floral trait variation could reflect selection from other biotic or abiotic drivers (Strauss and Whittall, 2006) or drift, which is expected to be stronger at range edges (Nadeau and Urban, 2019) where both yellow morphs occur.…”

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

“…While visitor assemblages to all focal species were generalized overall (Wenzell et al, 2023) In support of this expectation, we found that pollinator diversity was significantly lower in long-tubed populations (Figure 4b) based on both the GLMM (corolla length: χ 2 1,50 = 5.7, p = .017; dataset: χ 2 1,50 = 0.15, p = .7) and Kruskal-Wallis test (KW χ 2 1,41 = 6.1, p = .013). We did not find evidence that pollinator diversity varied significantly by latitude based on a GLMM (latitude: χ 2 1,51 = 2.01, p = .16; dataset: χ 2 1,49 = 0.22, p = .64) and Kruskal-Wallis test (KW χ 2 22 = 25.25, p = .29; N = 41), indicating that lower diversity to long-tubed populations of C. sessiliflora is not an artifact of a possible decrease in pollinator diversity due to latitude.…”

“…Previous work on variation in floral traits and floral visitors across the ranges of C. sessiliflora and the C. purpurea complex revealed that, despite being visited by broad assemblages of generalist pollinator groups, divergence in several key floral traits mirrored differences in visitation from local pollinators (Wenzell et al., 2023 ). Several of these floral traits were related to pollinator attraction, such as color (butterflies were associated with purple and pink flowers, while bumblebees were more likely to visit pale, yellow flowers and avoid red), while other traits were related to mechanical fit and efficiency of pollen transfer (e.g., small bee visitation was associated with less exserted stigmas, expected to increase pollen transfer).…”

High floral disparity without pollinator shifts in buzz‐bee‐pollinated Melastomataceae

“…Lineage diversification in the absence of pollinator shifts does not generally imply low floral disparity, however, as exemplified by the exceptionally high floral disparity reported among selected clades of bee‐pollinated members of the family Melastomataceae (Reginato & Michelangeli, 2016; Dellinger et al ., 2019b), or divergence in floral scent profiles in moth‐pollinated Lithophragma (Saxifragaceae, Friberg et al ., 2019). Subtle divergent selection in adaptation to locally variable pollinator communities has been proposed as driver of such patterns of high disparity (Macior, 1971; Dellinger et al ., 2019b; Wenzell et al ., 2023). In addition, processes such as competition for pollinators among co‐flowering relatives, or variable impacts by the abiotic environment, may drive the evolution of floral disparity in the absence of pollinator shifts (summarized by Ellis & Anderson, 2012).…”