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. 2014 Nov 22;281(1795):20140888.
doi: 10.1098/rspb.2014.0888.

Escape From Extreme Specialization: Passionflowers, Bats and the Sword-Billed Hummingbird

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Free PMC article

Escape From Extreme Specialization: Passionflowers, Bats and the Sword-Billed Hummingbird

S Abrahamczyk et al. Proc Biol Sci. .
Free PMC article

Abstract

A striking example of plant/pollinator trait matching is found between Andean species of Passiflora with 6-14-cm-long nectar tubes and the sword-billed hummingbird, Ensifera ensifera, with up to 11-cm-long bills. Because of the position of their anthers and stigmas, and self-incompatibility, these passionflower species depend on E. ensifera for pollination. Field observations show that the bird and plant distribution match completely and that scarcity of Ensifera results in reduced passionflower seed set. We here use nuclear and plastid DNA sequences to investigate how often and when these mutualisms evolved and under which conditions, if ever, they were lost. The phylogeny includes 26 (70%) of the 37 extremely long-tubed species, 13 (68%) of the 19 species with tubes too short for Ensifera and four of the seven bat-pollinated species for a total of 43 (69%) of all species in Passiflora supersection Tacsonia (plus 11 outgroups). We time-calibrated the phylogeny to infer the speed of any pollinator switching. Results show that Tacsonia is monophyletic and that its stem group dates to 10.7 Ma, matching the divergence at 11.6 Ma of E. ensifera from its short-billed sister species. Whether pollination by short-billed hummingbirds or by Ensifera is the ancestral condition cannot be securely inferred, but extremely long-tubed flowers exclusively pollinated by Ensifera evolved early during the radiation of the Tacsonia clade. There is also evidence of several losses of Ensifera dependence, involving shifts to bat pollination and shorter billed birds. Besides being extremely asymmetric-a single bird species coevolving with a speciose plant clade-the Ensifera/Passiflora system is a prime example of a specialized pollinator not driving plant speciation, but instead being the precondition for the maintenance of isolated populations (through reliable seed set) that then underwent allopatric speciation.

Keywords: Passiflora; asymmetric coevolution; coevolution; hummingbirds; molecular clock; phylogenetics.

Figures

Figure 1.
Figure 1.
Representative species of Passiflora supersection Tacsonia. (a) Passiflora tarminiana, Peru, dependent on E. ensifera for pollination; (b) Passiflora ampullacea, Ecuador, dependent on E. ensifera for pollination. (c) Passiflora peduncularis, Peru, pollinated by bats. (d) Passiflora unipetala, Bellavista Cloud Forest Reserve, Pichincha, Ecuador, being visited by Anoura fistulata. Photo credits: figure (a) by P. M. Joergensen, (b) by G. Onore, (c) by T. Boza and (d) by N. Muchhala.
Figure 2.
Figure 2.
(a) Phylogeny for 37 species of Passiflora supersection Tacsonia based on 2867 aligned nucleotides of plastid and nuclear DNA markers. Species names in black refer to Passiflora species with nectar tubes 6–14 cm long and thus dependent on E. ensifera for pollination; names in red refer to species with nectar tubes less than 6 cm and pollinated by short-billed hummingbirds; in blue are species pollinated by bats; in green species pollinated by bees. Electronic supplementary material, table S2, provides the basis for each species’ scoring. (b) Distribution map of E. ensifera from Birdlife International (2014) (www.birdlife.org). The distribution of supersection Tacsonia (in grey) completely matches that of Ensifera (in black). (Online version in colour.)
Figure 3.
Figure 3.
Molecular clock tree for 37 species of Passiflora supersection Tacsonia, with species colour-coded by pollinator type: bee, bat, short-billed hummingbird and E. ensifera. Electronic supplementary material, table S2, provides the basis for each species' scoring. The photos show (a) E. ensifera, (b) Xylocopa carpenter bee on a leaf of Rubus, (c) short-billed hummingbird (Hylocharis cyanus) and (d) the bat Glossophaga commissarisi, which pollinates species of Tacsonia. Electronic supplementary material, figure S2, shows the 95% confidence intervals around divergence times, figure S3 a parsimony-based ancestral state reconstruction and figure S4 a likelihood-based reconstruction of pollination syndromes. Photo credits: (a) J. C. Boone, (b) H. Mouret, (c) D. Sanchez and (d) K. Schneeberger (all from Wikipedia.org).

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