The first mistletoes: origins of aerial parasitism in Santalales.

Past molecular phylogenetic work has shown that aerial parasites have evolved five times independently in the sandalwood order (Santalales), but the absolute timing of these diversifications was not addressed. DNA sequences from nuclear SSU and LSU rDNA, and chloroplast rbcL, matK and trnL-F from 39 santalalean taxa were obtained. Separate and combined data partitions were analyzed with maximum parsimony and Bayesian inference. Time estimates were performed with Bayesian relaxed molecular clock and penalized likelihood methods using published fossil data. Both methods gave comparable divergence dates for the major clades. These data confirm five origins of aerial parasitism, first in Misodendraceae ca. 80 Mya and subsequently in Viscaceae (72 Mya), "Eremolepidaceae" (53 Mya), tribe Amphorogyneae in Santalaceae (46 Mya), and Loranthaceae (28 Mya). The rapid adaptive radiation and speciation in Loranthaceae coincides with the appearance of savanna biomes during the Oligocene. In all clades except Misodendraceae, it appears that aerial parasites evolved from ancestors that were polymorphic for either root or stem parasitism-a condition here termed amphiphagous. Convergences in morphological features associated with the mistletoe habit have occurred such as the squamate habit, seed attachment structures, unisexual flowers, and loss of chlorophyll.