Long branch attraction, taxon sampling, and the earliest angiosperms: Amborella or monocots?

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Background: Numerous studies, using in aggregate some 28 genes, have achieved a consensus in recognizing three groups of plants, including Amborella, as comprising the basal-most grade of all other angiosperms. A major exception is the recent study by Goremykin et al. (2003; Mol. Biol. Evol. 20:1499-1505), whose analyses of 61 genes from 13 sequenced chloroplast genomes of land plants nearly always found 100% support for monocots as the deepest angiosperms relative to Amborella, Calycanthus, and eudicots. We hypothesized that this conflict reflects a misrooting of angiosperms resulting from inadequate taxon sampling, inappropriate phylogenetic methodology, and rapid evolution in the grass lineage used to represent monocots. Results: We used two main approaches to test this hypothesis. First, we sequenced a large number of chloroplast genes from the monocot Acorus and added these plus previously sequenced Acorus genes to the Goremykin et al. (2003) dataset in order to explore the effects of altered monocot sampling under the same analytical conditions used in their study. With Acorus alone representing monocots, strongly supported Amborella-sister trees were obtained in all maximum likelihood and parsimony analyses, and in some distance-based analyses. Trees with both Acorus and grasses gave either a well-supported Amborella-sister topology or else a highly unlikely topology with 100% support for grasses-sister and paraphyly of monocots (i.e., Acorus sister to "dicots" rather than to grasses). Second, we reanalyzed the Goremykin et al. (2003) dataset focusing on methods designed to account for rate heterogeneity. These analyses supported an Amborella-sister hypothesis, with bootstrap support values often conflicting strongly with cognate analyses performed without allowing for rate heterogeneity. In addition, we carried out a limited set of analyses that included the chloroplast genome of Nymphaea, whose position as a basal angiosperm was also, and very recently, challenged. Conclusions: These analyses show that Amborella (or Amborella plus Nymphaea), but not monocots, is the sister group of all other angiosperms among this limited set of taxa and that the grasses-sister topology is a long-branch-attraction artifact leading to incorrect rooting of angiosperms. These results highlight the danger of having lots of characters but too few and, especially, molecularly divergent taxa, a situation long recognized as potentially producing strongly misleading molecular trees. They also emphasize the importance in phylogenetic analysis of using appropriate evolutionary models.




Stefanović, S., Rice, D. W., & Palmer, J. D. (2004). Long branch attraction, taxon sampling, and the earliest angiosperms: Amborella or monocots? BMC Evolutionary Biology, 4, 1–35. https://doi.org/10.1186/1471-2148-4-35

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