Unraveling the evolutionary history of the Manakins

Different methods largely converge on the same species tree.

Constructing a phylogeny from genomic data is a challenging exercise. Some researchers have proposed a concatenation approach where you combine all genes into one long sequence and analyze them as one huge gene. This straightforward strategy has the major limitation that it assumes all genes share the same evolutionary history. This is mostly not the case: different genes tend to tell different evolutionary stories. So, how can you extract the “true” phylogeny from this forest of discordant gene trees. Here, the multispecies coalescent (MSC) can be useful. This statistical framework uses a set of discordant gene trees to estimate the species tree, while taking into account their diverse evolutionary trajectories (often caused by incomplete lineage sorting). Although there has been intense debate on this method, it does seem to be a reliable way to reconstruct species trees. A good strategy is to apply multiple methods and try to understand any incongruent results that pop up. In my own research on the evolution of geese, for example, I applied both concatenation and multispecies coalescent approaches. Both methods converged on the same species tree, suggesting that it reflects the main evolutionary history of these birds. Recently, a study in the journal Molecular Phylogenetics and Evolution used a variety of methods to unravel the phylogenetic relationships of manakins (family Pipridae). Let’s see if they succeeded.

Many Methods

Rafael Leite and his colleagues sequenced two types of molecular markers for several manakin species: ultraconserved elements (UCEs) and exons. UCEs are genomic sequences that are highly conserved across vertebrates and can thus be easily sequenced across a wide range of species. Their flanking regions are more variable and can be used for phylogenetic analyses (see for example this study on honeyeaters). Exons are the expressed sections of gene sequences and can be obtained with specific target capture methods. These two types of molecular markers were subsequently analyzed with both concatenation and multispecies coalescent approaches.

The researchers used the UCE data to create two datasets: one with at least 75% of the species sampled (75% UCE) and one with at least 95% of the species sampled (95% UCE). Next, they performed the following phylogenetic analyses: concatenated analyses on three datasets (75% UCE, 95% UCE and exons) and multispecies coalescent on two datasets (75% UCE and 95% UCE). For the latter analyses, they relied on two approaches: ASTRAL (which uses the gene trees as input) and SVDquartets (which uses the sequence data as input).

Phylogenetic tree of the manakins (family Pipridae) based on Maximum Likelihood analyses of the UCE concatenated datasets. The numbers in the boxes indicate support values for the 75% UCE and 95% UCE datasets. From: Leite et al. (2021) Molecular Phylogenetics and Evolution.

Non-monophyletic Clades

I will not bother you with a detailed description of all the resulting phylogenies. The researchers noted that their results “were largely congruent across analyses, and led to a robust hypothesis about the phylogenetic relationships of manakins.” In line with previous molecular studies, the analyses pointed to an early split between the sexually monomorphic genera Neopelma and Tyranneutus (group A, subfamily Neopelminae), and the dichromatic “core” manakins (group B, subfamily Piprinae). In addition, the results suggest sub-clades B1 (Ilicura, Masius, Corapipo, Chiroxiphia and Antilophia) and B2 (Xenopipo, Chloropipo, Cryptopipo, Lepidothrix, Heterocercus, Manacus, Pipra, Machaeropterus, Pseudopipra and Ceratopipra) within the Piprinae.

Most genera turned out to be monophyletic, but there are some notable exceptions. First, several species of the genus Tyranneutus – namely the Tiny Tyrant-manakin (T. virescens) and the Dwarf Tyrant-manakin (T. stolzmanni) – are nested with the genus Neopelma. Second, the analyses indicated that two species of the genus Antilophia – the Helmeted Manakin (A. galeata) and the Araripe Manakin (A. bokermanni) – cluster within the genus Chiroxiphia. Moreover, different methods pointed to different phylogenetic relationships between the members of these genera (although Antilophia was always nested within Chiroxiphia). More work is needed here to sort out the details, but a taxonomic revision seems warranted.

Different methods resulted in different topologies for the genera Antilophia and Chiroxiphia. From: Leite et al. (2021) Molecular Phylogenetics and Evolution.

Future Work

Despite some phylogenetic conflicts between the methods and a few clades with low statistical support, this study generated a reliable backbone for the manakin phylogeny. This phylogenetic framework can now be applied to macroevolutionary questions to better understand the evolution of the unique behaviors and morphological variation of these beautiful birds.

References

Leite, R. N., Kimball, R. T., Braun, E. L., Derryberry, E. P., Hosner, P. A., Derryberry, G. E., Anciaes, M., McKay, J. S., Aleixo, A., Ribas, C. C., Brumfield, R. T. & Cracraft, J. (2021). Phylogenomics of manakins (Aves: Pipridae) using alternative locus filtering strategies based on informativeness. Molecular Phylogenetics and Evolution155, 107013.

Featured image: Graphical abstract from the study.

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