CORRELATED EVOLUTION OF POLLEN MORPHOLOGY AND POLLINATION BIOLOGY IN CONIFERS AND OTHER SEED PLANTS

Inflated regions of the pollen wall, or sacci, are common in extinct seed plants and many living conifer species. These structures, which increase the buoyancy of pollen grains in water, are thought to function in as part of a specific pollination mechanism that also depends on seed orientation and the production of a liquid droplet, or pollination drop. The presence of sacci has been linked with these features in previous studies, but this has not been tested within an explicit phylogenetic framework. In this study, we use a large, well-sampled phylogeny containing 466 species of conifers to test the correlation between sacci, seed orientation, and the presence of pollination drops. Using maximum likelihood transition rate models, we find that correlated models of character evolution best explain the distribution of character states in living taxa. Specifically, the best-supported models suggest that the loss of sacci follows changes in seed cone orientation or drop production that would eliminate the need for buoyant pollen grains at pollination. Our models also indicate that once sacci are lost, they are not regained in descendant clades. The loss of sacci therefore irreversibly dismantles the flotation-based pollination mechanism used by many conifers, decoupling the evolution of pollen morphology from seed cone morphology. This sequence of character changes has wider implications for reproductive evolution in seed plants, however, because sacci are widespread Paleozoic and Mesozoic seed plant groups. In particular, understanding the directionality of sacci loss may help to resolve relationships among extinct seed plant groups, which has proven difficult in the past.