Beyond buzz‐pollination – departures from an adaptive plateau lead to new pollination syndromes

Abstract

Summary Pollination syndromes describe recurring adaptation to selection imposed by distinct pollinators. We tested for pollination syndromes in Merianieae (Melastomataceae), which contain bee‐ (buzz‐), hummingbird‐, flowerpiercer‐, passerine‐, bat‐ and rodent‐pollinated species. Further, we explored trait changes correlated with the repeated shifts away from buzz‐pollination, which represents an ‘adaptive plateau’ in Melastomataceae. We used random forest analyses to identify key traits associated with the different pollinators of 19 Merianieae species and estimated the pollination syndromes of 42 more species. We employed morphospace analyses to compare the morphological diversity (disparity) among syndromes. We identified three pollination syndromes (‘buzz‐bee’, ‘mixed‐vertebrate’ and ‘passerine’), characterized by different pollen expulsion mechanisms and reward types, but not by traditional syndrome characters. Further, we found that ‘efficiency’ rather than ‘attraction’ traits were important for syndrome circumscription. Contrary to syndrome theory, our study supports the pooling of different pollinators (hummingbirds, bats, rodents and flowerpiercers) into the ‘mixed‐vertebrate’ syndrome, and we found that disparity was highest in the ‘buzz‐bee’ syndrome. We conclude that the highly adaptive buzz‐pollination system may have prevented shifts towards classical pollination syndromes, but provided the starting point for the evolution of a novel set of distinct syndromes, all having retained multifunctional stamens that provide pollen expulsion, reward and attraction.

Evolutionary tinkering allows buzz pollinated plants to escape from an adaptive dead‐end

“…Developmental constraints may help explain why mixed‐vertebrate and passerine pollinated flowers in this group retain poricidal anthers as suggested by Dellinger et al . (). It is also possible that poricidal anthers are still favoured by natural selection as a mechanism to restrict access to pollen and reduce pollen theft by other ineffective floral visitors (Hargreaves et al ., ; Vallejo‐Marín et al ., ).…”

“…The study of Dellinger et al . () focused on 61 of the 300 species in the tribe Merianieae, and benefited from an unpublished phylogeny of the tribe, which allowed them to estimate ancestral character states and transitions in both floral morphological traits and types of floral visitors. Dellinger et al .…”

“…Dellinger et al . () characterized flowers using morphological measurements of 61 floral traits thought to be associated with pollination. Information about taxonomic identity of floral visitors of 19 species was obtained from the literature and field observations.…”

“…Dellinger et al . () have elegantly documented the morphological changes associated with derived pollination systems that represent a dramatic shift from bees to vertebrate pollinators. A key discovery of their phylogenetic and morphological analysis is that the transitions to vertebrate pollination in this group are associated with the reinvention of floral attraction and pollination functions, mostly through the modification of stamens.…”

“…In this issue of New Phytologist , Dellinger et al . (, pp. 1136–1149) provide the best‐documented example to date of the evolution of new pollination syndromes from a buzz‐pollinated ancestor.…”