The evolution and loss of oil-offering flowers: new insights from dated phylogenies for angiosperms and bees

Abstract

The interactions between bees that depend on floral oil for their larvae and flowers that offer oil involve an intricate mix of obligate and facultative mutualisms. Using recent phylogenies, new data on oil-offering Cucurbitaceae, and molecular-dating, we ask when and how often oil-offering flowers and oil-foraging bees evolved, and how frequently these traits were lost in the cause of evolution. Local phylogenies and an angiosperm-wide tree show that oil flowers evolved at least 28 times and that floral oil was lost at least 36-40 times. The oldest oil flower systems evolved shortly after the K/T boundary independently in American Malpighiaceae, tropical African Cucurbitaceae and Laurasian Lysimachia (Myrsinaceae); the ages of the South African oil flower/oil bee systems are less clear. Youngest oil flower clades include Calceolaria (Calceolariaceae), Iridaceae, Krameria (Krameriaceae) and numerous Orchidaceae, many just a few million years old. In bees, oil foraging evolved minimally seven times and dates back to at least 56 Ma (Ctenoplectra) and 53 Ma (Macropis). The co-occurrence of older and younger oil-offering clades in three of the four geographical regions (but not the Holarctic) implies that oil-foraging bees acquired additional oil hosts over evolutionary time. Such niche-broadening probably started with exploratory visits to flowers resembling oil hosts in scent or colour, as suggested by several cases of Muellerian or Batesian mimicry involving oil flowers.

Figure 1.

Maximum-likelihood phylogeny obtained from 626 rbcL sequences representing 440 families of angiosperms (Angiosperm Phylogeny Group 2003), with an over-sampling of oil-offering species. The Iridaceae Sisyrinchium montanum is not known to offer oil (Cocucci & Vogel 2001), but this species is the only Sisyrinchium for which an rbcL sequence was available. Of known oil-offering taxa, the phylogeny lacks the Plantaginaceae Basistemon and Monopera, the Scrophulariaceae Colpias, the Stilbaceae Anastrabe and Bowkeria, and numerous oil-offering orchids (listed in table 1). The tree therefore does not reflect the true number of independent origins of oil in the angiosperms (detailed version provided as figure 1_large in the electronic supplementary material).

Figure 2.

Maximum parsimony tree showing the relationships of the most important bee groups (modified after Danforth et al. 2006, based on five nuclear DNA regions plus morphological data). Eucerini, Tapinotaspidini and Tetrapediini were not sampled in the original study, but are here added based on the results of Schaefer & Renner (2008). Oil foraging lineages in grey.

Figure 3.

Scheme showing the gradual build-up of oil flower/oil bee interactions in two of the World's four regional oil flower systems. The Eurasian Macropis/Lysimachia system and the African/Asian Ctenoplectra/Cucurbitaceae system did not involve switches to hosts outside these plant clades. The latter system, however, involved the repeated acquisition of new cucurbit hosts through time, a finer scale host expansion not shown here.