Has Pollination Mode Shaped the Evolution of Ficus Pollen?

BACKGROUND The extent to which co-evolutionary processes shape morphological traits is one of the most fascinating topics in evolutionary biology. Both passive and active pollination modes coexist in the fig tree (Ficus, Moraceae) and fig wasp (Agaonidae, Hymenoptera) mutualism. This classic obligate relationship that is about 75 million years old provides an ideal system to consider the role of pollination mode shifts on pollen evolution. METHODS AND MAIN FINDINGS Twenty-five fig species, which cover all six Ficus subgenera, and are native to the Xishuangbanna region of southwest China, were used to investigate pollen morphology with scanning electron microscope (SEM). Pollination mode was identified by the Anther/Ovule ratio in each species. Phylogenetic free regression and a correlated evolution test between binary traits were conducted based on a strong phylogenetic tree. Seventeen of the 25 fig species were actively pollinated and eight species were passively pollinated. Three pollen shape types and three kinds of exine ornamentation were recognized among these species. Pollen grains with ellipsoid shape and rugulate ornamentation were dominant. Ellipsoid pollen occurred in all 17 species of actively pollinated figs, while for the passively pollinated species, two obtuse end shapes were identified: cylinder and sphere shapes were identified in six of the eight species. All passively pollinated figs presented rugulate ornamentation, while for actively pollinated species, the smoother types - psilate and granulate-rugulate ornamentations - accounted for just five and two among the 17 species, respectively. The relationship between pollen shape and pollination mode was shown by both the phylogenetic free regression and the correlated evolution tests. CONCLUSIONS Three pollen shape and ornamentation types were found in Ficus, which show characteristics related to passive or active pollination mode. Thus, the pollen shape is very likely shaped by pollination mode in this unique obligate mutualism.