Resolving the Avian Tree of Life from Top to Bottom: The Promise and Potential Boundaries of the Phylogenomic Era

Abstract

Reconstructing relationships among extant birds (Neornithes) has been one of the most difficult problems in phylogenetics, and, despite intensive effort, the avian tree of life remains (at least partially) unresolved. Thus far, the most difficult problem is the relationship among the orders of Neoaves, the major clade that includes the most (~95%) named bird species. This clade appears to have undergone a rapid radiation near the end Cretaceous mass extinction (the K-Pg boundary). On the other hand, if one embraces a “glass half full” view, the fact that most orders in Neoaves can be placed into seven clades, recently designated the “magnificent seven,” could be viewed as remarkable progress. We propose that the dawning era of whole-genome phylogenetics will only resolve the remaining relationships, if we improve data quality, exploit information from other sources (i.e., rare genomic changes), and learn more about the functional and evolutionary landscape of avian genomes. Of course, it is possible that the remaining unresolved relationships are unresolvable regardless of the data available, but we suggest that the community should avoid this conclusion until more data collection has been completed and improved analyses have been conducted. We say this because there is ample evidence that estimates of avian phylogeny based on large-scale datasets may be affected by well-characterized artifacts (e.g., long-branch attraction, heterotachy, and discordance among gene trees) and by subtle “data-type effects” that reflect poor fit to empirical data for available models of sequence evolution. Even if these analytical challenges can be addressed, we need to integrate phylogenomic and fossil data. Finally, we also emphasize that, regardless of the resolution (or lack thereof) for relationships among major avian clades, we are only at the dawn of the phylogenomics of birds. Large-scale molecular data remain unavailable for the vast majority of the ~10,000 named bird species, and those named bird species probably represent an underestimate of the true number of distinct evolutionary lineages of birds (whether or not those lineages are assigned the rank of species) by as much as threefold. A true biodiversity genomics effort in birds is likely to reveal many additional examples of cases where it is very difficult to resolve relationships; the effort to resolve as many of those relationships as possible will represent a major scientific achievement and provide lessons for phylogenomic studies in other parts of the tree of life.