Adaptation to hummingbird pollination is associated with reduced diversification inPenstemon

Abstract

A striking characteristic of the Western North American flora is the repeated evolution of hummingbird pollination from insect‐pollinated ancestors. This pattern has received extensive attention as an opportunity to study repeated trait evolution as well as potential constraints on evolutionary reversibility, with little attention focused on the impact of these transitions on species diversification rates. Yet traits conferring adaptation to divergent pollinators potentially impact speciation and extinction rates, because pollinators facilitate plant reproduction and specify mating patterns between flowering plants. Here, we examine macroevolutionary processes affecting floral pollination syndrome diversity in the largest North American genus of flowering plants, Penstemon. Within Penstemon, transitions from ancestral bee‐adapted flowers to hummingbird‐adapted flowers have frequently occurred, although hummingbird‐adapted species are rare overall within the genus. We inferred macroevolutionary transition and state‐dependent diversification rates and found that transitions from ancestral bee‐adapted flowers to hummingbird‐adapted flowers are associated with reduced net diversification rate, a finding based on an estimated 17 origins of hummingbird pollination in our sample. Although this finding is congruent with hypotheses that hummingbird adaptation in North American Flora is associated with reduced species diversification rates, it contrasts with studies of neotropical plant families where hummingbird pollination has been associated with increased species diversification. We further used the estimated macroevolutionary rates to predict the expected pattern of floral diversity within Penstemon over time, assuming stable diversification and transition rates. Under these assumptions, we find that hummingbird‐adapted species are expected to remain rare due to their reduced diversification rates. In fact, current floral diversity in the sampled Penstemon lineage, where less than one‐fifth of species are hummingbird adapted, is consistent with predicted levels of diversity under stable macroevolutionary rates.

Ancient and recent introgression shape the evolutionary history of pollinator adaptation and speciation in a model monkeyflower radiation (MimulussectionErythranthe)

“…Together, our genomic and experimental results underline the necessity of an explicitly phylogenomic context for understanding trait evolution and speciation in rapid radiations. Hummingbird pollination undoubtedly evolves convergently both within [51] and among [2,43,52] genera, but pollination syndromes may be particularly prone to complex evolutionary histories that mimic phenotypic convergence at low phylogenetic resolution. Like anti-predator mimicry phenotypes in Heliconius butterflies [12], specialized pollination syndromes (e.g., hummingbird, moth) evolve to match a pre-existing model [53].…”

“…Given the revision of the species tree, it is also worth revisiting the inference that bee-pollination is ancestral [23], especially given the presence of yellow carotenoid pigments in both outgroup taxa such as (bee-pollinated) M. bicolor and the hummingbird-pollinated Erythranthe . Across flowering plants, transitions from bee to hummingbird pollination appear far more likely than the reverse [47], due either to genetic constraints [51] and/or the ecology of pollination [55]. Bees tend to ignore red flowers and have nowhere to land on narrowly tubular and reflexed “hummingbird” corollas whereas hummingbirds often visit classic bumblebee flowers; for example, hummingbirds made nearly 20% of the visits to Sierran M. lewisii in experimental arrays with M. cardinalis and hybrids [33].…”

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

“…The vast majority of biological systems and plant–pollinator interactions is not part of this group, however. Phylogenetic comparative methods offer a powerful tool to analysing tempo, mode and mechanisms of floral trait evolution in these systems (Smith & Kriebel, 2018; Wessinger et al ., 2019; Dellinger et al ., 2019c). In recent years, authors have often tested the importance of a single or a few isolated traits in explaining diversification (Lagomarsino et al ., 2016).…”

Macroevolution of Flower Color Patterning: Biased Transition Rates and Correlated Evolution with Flower Size

“…Many studies have dissected the biochemistry and development of flower color patterning but none have evaluated their macroevolutionary dynamics. In fact, there are few studies on the tempo and directionality of macroevolution for ecologically relevant floral traits in general (however, see Smith and Goldberg, 2015 ; Wessinger et al., 2019 for pigment presence/absence; and Ree and Donoghue, 1999 for symmetry). Bull’s-eye pigmentation patterns can be manifested by the spatial regulation of pigments in multiple ways.…”