Resolving an Ancient, Rapid Radiation in Saxifragales

Abstract

Despite the prior use of approximately 9000 bp, deep-level relationships within the angiosperm clade, Saxifragales remain enigmatic, due to an ancient, rapid radiation (89.5 to 110 Ma based on the fossil record). To resolve these deep relationships, we constructed several new data sets: (1) 16 genes representing the three genomic compartments within plant cells (2 nuclear, 10 plastid, 4 mitochondrial; aligned, analyzed length = 21,460 bp) for 28 taxa; (2) the entire plastid inverted repeat (IR; 26,625 bp) for 17 taxa; (3) "total evidence" (50,845 bp) for both 17 and 28 taxa (the latter missing the IR). Bayesian and ML methods yielded identical topologies across partitions with most clades receiving high posterior probability (pp = 1.0) and bootstrap (95% to 100%) values, suggesting that with sufficient data, rapid radiations can be resolved. In contrast, parsimony analyses of different partitions yielded conflicting topologies, particularly with respect to the placement of Paeoniaceae, a clade characterized by a long branch. In agreement with published simulations, the addition of characters increased bootstrap support for the putatively erroneous placement of Paeoniaceae. Although having far fewer parsimony-informative sites, slowly evolving plastid genes provided higher resolution and support for deep-level relationships than rapidly evolving plastid genes, yielding a topology close to the Bayesian and ML total evidence tree. The plastid IR region may be an ideal source of slowly evolving genes for resolution of deep-level angiosperm divergences that date to 90 My or more. Rapidly evolving genes provided support for tip relationships not recovered with slowly evolving genes, indicating some complementarity. Age estimates using penalized likelihood with and without age constraints for the 28-taxon, total evidence data set are comparable to fossil dates, whereas estimates based on the 17-taxon data are much older than implied by the fossil record. Hence, sufficient taxon density, and not simply numerous base pairs, is important in reliably estimating ages. Age estimates indicate that the early diversification of Saxifragales occurred rapidly, over a time span as short as 6 million years. Between 25,000 and 50,000 bp were needed to resolve this radiation with high support values. Extrapolating from Saxifragales, a similar number of base pairs may be needed to resolve the many other deep-level radiations of comparable age in angiosperms.

Rosid radiation and the rapid rise of angiosperm-dominated forests

“…1). These results parallel those reported for Saxifragales (23), illustrating the value of the slowly evolving IR in deep-level phylogeny reconstruction. Despite far fewer parsimonyinformative sites than ''fast'' genes, the slowly evolving IR genes provide higher resolution and support for relationships, providing a topology identical to the total evidence ML tree.…”

“…This study and other recent analyses (5,6,23) suggest that with enough data, many, if not most, remaining deep-level ''radiations'' in the flowering plants can be resolved. For example, a putative rapid radiation in Saxifragales was resolved, despite long-branch attraction problems, with Ͼ25,000 base pairs (23).…”

“…To place this in perspective, this narrow window of initial diversification of 4-5 million years represents a timeframe comparable to the rapid radiation of the Hawaiian silversword alliance (Asteraceae), which arose from a North American ancestor 5 Mya (36). Saxifragales (23), Malpighiales (34,37), and Mesangiospermae (6) also each appear to have arisen and diversified over a very short period.…”

“…We sequenced the entire IR (see ref. 23) for 59 of the rosids used in our 12-gene analyses (due to expense, we did not sequence the IR for all taxa). We also extracted IR sequences for all publicly available complete plastid genome sequences for rosids, and for several outgroups ( Fig.…”

Phylogenetic utility of ycf1 in orchids: a plastid gene more variable than matK

“…The phylogenetic utility of ycf 1 has only recently begun to be explored. The less variable IR portion of ycf 1 has been included in phylogenetic analyses in one recent study (Jian et al 2008 ), but the SSC portion of the gene has never been utilized phylogenetically, to our knowledge. Preliminary observations suggested that the SSC portion of ycf 1 may be more variable than mat K, and thus potentially more valuable as a low--level phylogenetic marker.…”