Phylogeny and diversification of the largest avian radiation

Abstract

The order Passeriformes ("perching birds") comprises extant species diversity comparable to that of living mammals. For over a decade, a single phylogenetic hypothesis based on DNA-DNA hybridization has provided the primary framework for numerous comparative analyses of passerine ecological and behavioral evolution and for tests of the causal factors accounting for rapid radiations within the group. We report here a strongly supported phylogenetic tree based on two single-copy nuclear gene sequences for the most complete sampling of passerine families to date. This tree is incongruent with that derived from DNA-DNA hybridization, with half of the nodes from the latter in conflict and over a third of the conflicts significant as assessed under maximum likelihood. Our historical framework suggests multiple waves of passerine dispersal from Australasia into Eurasia, Africa, and the New World, commencing as early as the Eocene, essentially reversing the classical scenario of oscine biogeography. The revised history implied by these data will require reassessment of comparative analyses of passerine diversification and adaptation.

Fig. 1.

Relationships among passerine birds based on analysis of combined RAG-1 and -2 sequences (146 taxa, 4,126 aligned nucleotide positions). The topology presented is the best ML estimate, rooted using Gallus and Coracias. Multiple exemplars of genera and certain higher taxa have been collapsed for clarity (number of species indicated in parentheses after genus or group). Nodal support is indicated by symbols and symbol fills. Stars indicate estimated Bayesian posterior probability ≥0.95 (nodes with oblongs or no symbol have estimated probabilities <0.95), black fill indicates parsimony (left half), and ML (right half) bootstrap percentages ≥75. Numbers refer to selected nodes that are dated in Table 2 or discussed in the text. The quotes around the taxon “Passerida” indicate that Sibley and Ahlquist's (1, 3) definition of the group excludes the underlined taxa within this clade and includes the underlined taxa shown here as falling outside the clade. Their Corvida includes all oscines (node 7) not in the Passerida. Likewise, the quotes around the taxon “Suboscines” indicate that this group traditionally contains the Acanthisittidae, here shown as basal within passerines.

Fig. 2.

Schematic of spatial and temporal patterns in passerine diversification. The height of the bars to the right of the tree is proportional to the number of species in the corresponding clades, and the proportion of colors in each bar represent the current geographic distribution of species (red, Australasia; green, Africa and Eurasia; blue, North and South America). Continuity of the terminal bars does not imply monophyly of species distributed in each region, except for specific clades within the “Passerida” and “core Corvoidea,” which are highlighted by triangles and labeled. Ancestral areas for groups (as inferred by dispersal–vicariance analysis, see Methods) are depicted by coloring of corresponding triangles and subtending branches using the same scheme (gray indicates ambiguous reconstructions). Nodal depths are proportional to inferred dates (Table 2), and the left vertices of individual clades are located at their estimated basal divergence times (major clades; e.g., NW Suboscines, node 5) or at the divergence from their sister taxa (subclades; e.g., Vireonidae). Numbered nodes correspond to Fig. 1. A geological and temporal scale is provided below, and letters associated with this scale indicate the approximate timing of events listed in the upper left-hand corner (references in supporting information; ANT, Antarctica; AUS, Australia; EUR, Eurasia; IND, India; NZ, New Zealand; SA, South America).