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The evolution of bird pollination in Macaronesian Lotus section Rhyncholotus (Leguminosae) Ojeda Alayon, Isidro

Abstract

In order to understand the evolutionary transition from bee pollination (melittophily) to bird pollination (ornithophily), I studied a group of Lotus from Macaronesia. First, I provided a combined phylogenetic framework using nuclear and plastid genes, where I showed that the morphological features adapted to opportunistic passerine birds in Tenerife and La Palma are derived and evolved recently within the last 1.2 Ma in four species. I also identified Lotus sessilifolius as the most likely closely related species with melittophily. I showed that L. sessilifolius and the clade where this syndrome evolved had a pre-adaptation to produce a color change to red flowers (and the associated anthocyanidin pigment, cyanidin) as a possible strategy to increase bee foraging efficiency. The transition from yellow to red flowers in this group required only a redirection in the flux of pigment production and a modification in the proportions of flavonols and anthocyanidins, especially within the cyanidin branch. I also found that petal micromorphology is highly modified between the two syndromes. I found that ornithophilous flowers lack the typical papillose conical cells, which are distributed in the exposed sides of the petals in bee-pollinated flowers. This reduction of conical cells is associated with an early down-regulation of a dorsal identity gene in legumes, LjCYC2. Bird-pollinated flowers also have a higher proportion of tabular rugose cells in all three types of petals in comparison with the bee-pollinated species. The increase of this epidermal type is associated with an up-regulation of LjCYC3, a lateral petal identity gene, during early stages of flower development in the dorsal and lateral petals. Lotus sessilifolius also seems to have this early expression in comparison with other bee-pollinated species. All this evidence suggests that the transition from bee to bird pollination in this group required only heterochronic modifications of the genes involved in flower color and petal micromorphology. It seems that ornithophily in Lotus evolved within a group which has at least two pre-adaptations, production of pigments required for red colors and an increase in the amount of tabular rugose cells, which likely facilitated the evolution of phenotypes associated with this pollination syndrome in the Canary Islands.

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