Orchids, hawkmoths and Darwin revisited: How adaptation to pollination by hawkmoths spurred the speciation of Old and New World angraecoids

Specialised pollination has often been proposed as a major driver of the unrivalled diversification of angiosperms. With its unparalleled variation in flower depth, ranging from spurless to 40 cm spurred flowers pollinated by hawkmoths, angraecoid orchids (Angraecinae) provide unique opportunities to reveal the impact of floral specialisation on diversification rates in the Afrotropics and Neotropics. We compiled floral characters for 327 angraecoid species, and assigned these species to newly formalised floral syndrome categories calibrated against pollination case studies. We then estimated ancestral character states and state-dependent speciation rates using the latest time-calibrated phylogeny of angraecoids. We found that white flowers consistent with micro-sphingophily (2 cm[≥] spurs <8.7 cm), macro-sphingophily (8.7 cm[≥] spurs <18.6 cm) and mega-sphingophily (spurs [≥]18.6 cm) evolved repeatedly in angraecoids, and are ancestral in some non-sphingophilous clades. Reversals to non-sphingophily and pigmented flowers suggest higher evolutionary lability of these traits than what is traditionally thought. Increasing floral specialisation with long spurs does not seem to enhance angraecoid orchids speciation rates, since micro-sphingophily appears to be associated with the highest speciation rates. An abundance of short-proboscid hawkmoths in Madagascar, as an ecological opportunity, may have accelerated the speciation of micro-sphingophilous taxa.