Bird-pollinated Macaronesian Lotus (Leguminosae) evolved within a group of entomophilous ancestors with post-anthesis flower color change

Abstract

a b s t r a c tWe analyzed the evolution of red/orange flowers in four putatively bird-pollinated species of Macaronesian Lotus, with the aim of investigating whether this floral trait evolved from a similar trait found in some entomophilous Lotus species, namely the ability to modify flower color to red after anthesis. First, we mapped the ability to modify flower color in this group on a well-resolved and densely sampled phylogenetic tree of the Macaronesian Lotus. Secondly, we determined differences in light reflectance and pigment composition between petals of (1) prechange and postchange flowers in bee-pollinated species and (2) between bee and putatively bird-pollinated species. Post-anthesis flower color change evolved three times within Macaronesian Lotus, and putatively bird-pollinated species evolved within a clade with this ability to change flower color to red after anthesis. The evolutionary transition to red/orange flowers in the putatively bird-pollinated species involved biochemical changes similar to those of the developmental transition to red postchange flowers. In both cases there are changes in the composition of flavonols and anthocyanidins within the same metabolic pathways, especially in the cyanidin branch of pigment production, but not the activation or inactivation of additional branches of this pathway. Postanthesis color change in Lotus, from yellow to red, is thought to be an adaptation to reduce bee visits to already pollinated flowers. Our results are consistent with the hypothesis that constitutive red coloration for bird-pollination evolved from facultative red flower color change in Lotus. As red post-anthesis coloration is widespread in plants, this may possibly represent a widespread exaptive mechanism for the evolution of bird pollination.

Temporal, but not spatial, changes in expression patterns of petal identity genes are associated with loss of papillate conical cells and the shift to bird pollination in Macaronesian Lotus (Leguminosae)

“…Pollinator shifts commonly involve a series of floral modifications, usually comprising those traits involved in pollinator attraction and reward. Besides the floral trait modifications previously reported in the Macaronesian Lotus (Dupont et al 2004; Ojeda et al 2012aOjeda et al , 2013, here we found evidence of a lateralisation effect in the dorsal and ventral petals in the birdpollinated species. The typical growth rate of the three types of petal observed in L. japonicus (Weng et al 2011) and also observed here ( Fig.…”

“…; Ojeda et al . , ), here we found evidence of a lateralisation effect in the dorsal and ventral petals in the bird‐pollinated species. The typical growth rate of the three types of petal observed in L. japonicus (Weng et al .…”

“…; Ojeda et al . ). Although the effectiveness of these passerine birds as pollinators has not yet been determined in field experiments, these four Lotus species are widely believed to be part of a bird‐pollinated element within the Macaronesian flora (Olesen ; Ollerton et al .…”

“…Lotus (Leguminosae) contains one such example of a pollination shift (Ojeda et al . ,b, ). Lotus is a large genus ( ca .…”

“…1A-C) that are not pollinated by bees, but rather visited by opportunistic generalist passerine birds (Olesen 1985;Stelzer 2005;Ollerton et al 2009). These four species possess many features that are known to be associated with bird pollination, such as large, red long-lived flowers with reflectance above 550 nm and copious hexose-rich nectar (Olesen 1985;Dupont et al 2004;Ollerton et al 2009;Olesen et al 2012;Ojeda et al 2013). Although the effectiveness of these passerine birds as pollinators has not yet been determined in field experiments, these four Lotus species are widely believed to be part of a birdpollinated element within the Macaronesian flora (Olesen 1985;Ollerton et al 2009;Ojeda 2013).…”