An origin of aerial branch parasitism in the mistletoe family, Loranthaceae

Abstract

The large mistletoe family, Loranthaceae, contains 75 genera and approximately 1000 species. The family originated in the Southern Hemisphere and dispersed, apparently early, between fragments of Gondwana. It is now widely distributed on land surfaces of the former supercontinent. The Loranthaceae has three terrestrial, root-parasitic genera-a habit considered ancestral-and 72 genera of aerial, branch parasites. For almost two centuries, the origin of the mistletoe habit has been of interest to biologists. Two main evolutionary pathways have been proposed to explain the transition from terrestrial to aerial parasitism in the family. One theorizes the presence of an intermediate climbing ancestor in the path to the aerial habit. The other proposes a direct transfer from terrestrial to epiphytic growth following the germination of seeds on tree branches. Here we present molecular and morphological evidence that (1) the terrestrial species Nuytsia floribunda is ancestral within the Loranthaceae, (2) aerial parasitism has had multiple origins in the family, (3) the first aerial branch parasites had epicortical roots, and (4) the origin of aerial parasitism in one Old World clade involved the direct transfer from terrestrial to epiphytic growth following the germination of seeds on tree branches. Our results suggest that it is not necessary to evoke a climbing intermediate in the origins of aerial parasitism in the Santalales.