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Mol Phylogenet Evol. 2014 Nov;80:231-66. doi: 10.1016/j.ympev.2014.08.013. Epub 2014 Aug 22.

Phylogenetic analysis at deep timescales: unreliable gene trees, bypassed hidden support, and the coalescence/concatalescence conundrum.

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Department of Biology, University of California, Riverside, CA 92521, USA. Electronic address:
Department of Biology, University of California, Riverside, CA 92521, USA.


Large datasets are required to solve difficult phylogenetic problems that are deep in the Tree of Life. Currently, two divergent systematic methods are commonly applied to such datasets: the traditional supermatrix approach (= concatenation) and "shortcut" coalescence (= coalescence methods wherein gene trees and the species tree are not co-estimated). When applied to ancient clades, these contrasting frameworks often produce congruent results, but in recent phylogenetic analyses of Placentalia (placental mammals), this is not the case. A recent series of papers has alternatively disputed and defended the utility of shortcut coalescence methods at deep phylogenetic scales. Here, we examine this exchange in the context of published phylogenomic data from Mammalia; in particular we explore two critical issues - the delimitation of data partitions ("genes") in coalescence analysis and hidden support that emerges with the combination of such partitions in phylogenetic studies. Hidden support - increased support for a clade in combined analysis of all data partitions relative to the support evident in separate analyses of the various data partitions, is a hallmark of the supermatrix approach and a primary rationale for concatenating all characters into a single matrix. In the most extreme cases of hidden support, relationships that are contradicted by all gene trees are supported when all of the genes are analyzed together. A valid fear is that shortcut coalescence methods might bypass or distort character support that is hidden in individual loci because small gene fragments are analyzed in isolation. Given the extensive systematic database for Mammalia, the assumptions and applicability of shortcut coalescence methods can be assessed with rigor to complement a small but growing body of simulation work that has directly compared these methods to concatenation. We document several remarkable cases of hidden support in both supermatrix and coalescence paradigms and argue that in most instances, the emergent support in the shortcut coalescence analyses is an artifact. By referencing rigorous molecular clock studies of Mammalia, we suggest that inaccurate gene trees that imply unrealistically deep coalescences debilitate shortcut coalescence analyses of the placental dataset. We document contradictory coalescence results for Placentalia, and outline a critical conundrum that challenges the general utility of shortcut coalescence methods at deep phylogenetic scales. In particular, the basic unit of analysis in coalescence analysis, the coalescence-gene, is expected to shrink in size as more taxa are analyzed, but as the amount of data for reconstruction of a gene tree ratchets downward, the number of nodes in the gene tree that need to be resolved ratchets upward. Some advocates of shortcut coalescence methods have attempted to address problems with inaccurate gene trees by concatenating multiple coalescence-genes to yield "gene trees" that better match the species tree. However, this hybrid concatenation/coalescence approach, "concatalescence," contradicts the most basic biological rationale for performing a coalescence analysis in the first place. We discuss this reality in the context of recent simulation work that also suggests inaccurate reconstruction of gene trees is more problematic for shortcut coalescence methods than deep coalescence of independently segregating loci is for concatenation methods.


Deep coalescence; Gene tree; Mammalia; Species tree; Supermatrix

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