Evolutionary flexibility in five hummingbird/plant mutualistic systems: testing temporal and geographic matching

Aim: Partners in co-evolutionary interactions must be ecologically interdependent and at least at some stage have matching traits and more or less overlapping ranges. As co-evolution is a process, neither the mutual dependence nor the trait and range matching are expected to be static or perfect. Here we investigate the extent of evolutionary flexibility in tight pollination mutualisms between hummingbirds and plants, ranging from straight-billed species to sicklebills. Location: The Americas. Methods: The five considered pollination mutualisms are between the following hummingbird and plant species: Calypte anna and Ribes speciosum (Grossulariaceae); Basilinna xantusii and Arbutus peninsularis (Ericaceae); two species of Sephanoides and Tristerix aphyllus/corymbosus (Loranthaceae); two species of Eutoxeres and 34 species of curved-corolla Centropogon (Campanulaceae); and six species of Oreotrochilus and seven species of Chuquiraga (Asteraceae). While ecological interdependence and trait matching in these mutualisms are well established, geographic occurrence data and molecular clock-based ages for the 10 clades were newly compiled. Results: We found matching bird and plant stem ages in two of the five systems and (much) older bird than plant ages in the other three. The implied adaptation of plant populations to already existing hummingbird species fits with the modelled distributions. In three of the systems, the ranges of the plants overlap those of their pollinators by > 90%; conversely, the range overlap between the bird species and the plant species they pollinate is much less than that. Surprisingly, the age mismatch was greatest in the Eutoxeres/Centropogon system, in spite of the perfect morphological fit among bills and corollas, illustrating the evolutionary flexibility of these mutualisms and the apparently rapid ‘addition’ of further plant species. Main conclusions: These findings illuminate the macroevolutionary assembly of hummingbird/plant mutualisms, which has been highly dynamic, even in specialized systems with perfect morphological trait fitting.