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Convergence of anti-bee pollination mechanisms in the Neotropical plant genus Drymonia (Gesneriaceae)

Abstract

The neotropical plant genus Drymonia displays a remarkable variety of floral shapes and colors. One feature that is particularly important to coevolution with pollinators involves the variable shapes and widths of corolla tubes. To evaluate the evolutionary context for changes in corolla shape, we constructed a phylogeny of 50 of the 75 species of Drymonia using molecular markers from plastid (trnK-matK) and nuclear regions (ITS and ETS). Mapping tube shapes on the phylogeny supports open, bell-shaped (campanulate) corolla shape as the ancestral character state for Drymonia, with multiple independent origins of constriction in the corolla tube. Corollas with constrictions take one of three tube shapes: a constricted flower opening and throat with a large, expanded pouch on the lower surface (hypocyrtoid); a constricted flower opening and throat lacking an expanded pouch on the lower surface (urceolate); or a constricted opening and throat where the sides of the corolla appear laterally compressed. Fieldwork demonstrates euglossine bees (mostly Euglossa spp. and Epicharis spp.) visit campanulate corollas while hummingbirds visit corollas that are constricted. Results support eight independent origins of constricted corolla tubes from ancestors with campanulate corolla tubes: 3 hypocyrtoid clades, 3 laterally compressed clades, and 3 urceolate clades (one of which represents a shift from a hypocyrtoid ancestor). Constricted corollas are associated with shifts from the ancestral condition of poricidal anther dehiscence, which presents pollen to pollinators in multiple small doses, to the derived condition of longitudinal anther dehiscence, which presents all pollen to pollinators simultaneously. The association of hummingbird pollination with constricted corolla tubes suggests that narrowing evolved as a barrier mechanism that prohibits the visitation of flowers by bees.

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Acknowledgments

The authors would like to thank Alex Monro from The Natural History Museum in London (BM) for sharing leaf material of Gesneriaceae. This study was supported by grants from the National Science Foundation (DEB-0949270 and DEB-0841958 to JLC). Fieldwork was greatly facilitated by the following undergraduate students from The University of Alabama: Cassandra L. Coleman, Seema Kumar, and Laura A. Frost. Lucas McDonald from Hillcrest High School (Tuscaloosa, AL) also helped in collecting data during a 2011 expedition to Ecuador. Murray Cooper and Richard W. Dunn are gratefully acknowledged for contributing images. We express our appreciation to two anonymous reviewers for useful comments that improved an earlier version of the manuscript.

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Correspondence to John L. Clark.

Appendices

Appendix 1

See Table 3.

Table 3 Specimens sequenced in molecular phylogenetic study of Drymonia and closely related congeners with voucher specimen, institution and GenBank accession numbers for ITS, ETS, and trnK-matK

Appendix 2

See Table 4.

Table 4 Statistics of ITS, ETS and trnK-matK genic regions

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Clark, J.L., Clavijo, L. & Muchhala, N. Convergence of anti-bee pollination mechanisms in the Neotropical plant genus Drymonia (Gesneriaceae). Evol Ecol 29, 355–377 (2015). https://doi.org/10.1007/s10682-014-9729-4

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Keywords

  • Convergence
  • Drymonia
  • Gesneriaceae
  • Hypocyrtoid corollas
  • Laterally compressed corollas
  • Pollination biology
  • Poricidal anther dehiscence
  • Urceolate corollas