Modern Birds: The Neornithes
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The most basal (oldest) division in the tree of living birds has been identified. It is the division between the Paleognaths (Ostrich, Rheas, Cassowaries, Emus, Kiwis, Tinamous) and the rest of the living birds (Neognaths). The names Paleognath (old jaw) and Neognath (new jaw) reflect differences in the skulls of the two types of bird.
The split may have occurred during the early Cretaceous, more than 100 million years ago. The Paleognaths also appear in the Sibley-Monroe list. More recent evidence has strengthened the notion that the Paleognaths form a natural group, and that they include the recently extinct Elephant Birds of Madagascar (Aepyornithidae) and Moas of New Zealand (Dinornithidae). However, the traditional division of the Paleognaths into the flightless Ratites and volant Tinamous has recently been called into question (Harshman et al., 2008).
Harshman et al. suggest that flightlessness has evolved in the Paleognaths at least three times, and probably four: ostriches, rheas, cassowaries/emus/kiwis/elephant birds, and probably separately in the moas. The taxonomy here is based on Harshman et al. (2008) and Hackett et al. (2008).
Galloanserae
Following the publication of Sibley and Ahlquist's book, ornithologists have gradually realized that the deepest division in the Neognaths separates the waterfowl and gallinaceous birds (Galloanserae) from everything else (Neoaves). These divisions are recognized in recent checklists such as AOU, ABA, and Howard-Moore 3rd edition. In contrast, the modified Sibley-Ahlquist-Monroe list of Gill (1995) places the Anseriformes after the Pelecaniformes with the Phoenicopteriformes, Ciconiiformes, and Falconiformes separating them from the Galliformes.
The Galloanserae in turn divide into the Anseriformes and Galliformes. One of the Anseriform families is the extinct Presbyornithidae. I've included them in the detailed tree diagram so you can see how these numerous and well-known fossils fit in a modern taxonomy (Ericson, 1997). The oldest Presbyornis fossils date back about 60 million years.
Neoaves
The higher taxonomy of the remaining bird families remains unsettled. We can group the families in Neoaves into a reasonable collection of orders (42 in this classification, 35 of them in the Neoaves), but correct placement of roughly a third of the orders remains uncertain. Eventually, we expect to be able to read enough DNA of enough species to untangle this, but for now, it is not possible to read and analyze the entire DNA of all of the birds. Until recently, the best DNA studies were either deep but narrow, including many genes from a few species, or are shallow and wide, including fewer genes from many more species. Hackett et al. (2008) changed that, using a dataset that set new standards in both depth and width. Even so, many of the major branches remain somewhat uncertainly positioned. They also provide the most complete analysis of the higher taxonomy of Neoaves, and generally reinforce and refine the results of Ericson et al. (2006a). Beginning with version 2.1, this taxonomy is used in these web pages. Key features of this arrangement depend on the analysis of a single gene, and may be subject to change.
The analyses of Fain and Houde (2004), Ericson et al. (2006a), and Hackett et al. (2008) divide Neoaves into two parts: Metaves and Coronaves.
The Metaves Hypothesis
In 2004, Fain and Houde published their Parallel Radiations paper, which proposed that many hard-to-classify bird orders were part of a basal branch in Neoaves, Metaves. Besides the always troublesome Hoatzin, Metaves contains pigeons and doves, sandgrouse, kagu, sunbittern, grebes, flamingos, mesites, tropicbirds, nightjars and relatives, swifts, and hummingbirds. It adds up to 10 orders containing over 900 species, almost 10% of all living bird species. Fain and Houde called the other 85% of living birds, Coronaves.
There had been hints before that some of the Metaves were related (e.g., grebes and flamingos), and that some bird families might be wrongly placed (e.g., tropicbirds), but existence of a whole group like Metaves came as a surprise. Ericson et al. (2006a) followed this up with a more detailed analysis that probably does a decent job of portraying the higher taxonomy of much of Neoaves. Hackett et al. (2008) also recovered Metaves, except for the hoatzin, which ended up in Coronaves at the base of the waterbird clade.
At present, we have reasonable confidence that owlet-nightjars, hummingbirds, and swifts group together. The frogmouths, oilbirds, nightjars, and potoos are believed to be their closest relatives, although genetic support for this is weak. Grebes and flamingos also seem related, as do kagu and sunbittern, but their relationships to other, but neither group has strong affinities with anything else. The pigeons and doves are also problematic. Perhaps the sandgrouse are related, maybe the mesites, but again the divisions between them are deep and they aren't closely related to anything else. With only one gene pulling these disparate groups together, Metaves is controversial.
In particular, studies based on mitochondrial DNA do not support the Metaves hypothesis (e.g., Gibb et al. 2007; Slack et al. 2007; Brown et al. 2008; Morgan-Richards et al. 2008; Pratt et al. 2009). Metaves depends on the interpretation of one rather messy gene fragment (the seventh intron of the β-fibrinogen gene). Although there's not anything obviously wrong, it cannot be used in consistent fashion across such a broad swath of species. As it also lacks support from other genes, this leaves open the possibility that the Metaves hypothesis is just plain wrong. That said, most currently available alternate topologies do not give any better results for the taxa in Metaves, and major features seem to change with each subsequent analysis.
For example, the deep mitochondrial study by Morgan-Richards et al. (2008) groups tropicbirds with accipiters and kagu with woodpeckers and passerines while Gibb et al. (2007) attribute their own grouping of owls with parrots to long-branch attraction. Ericson et al. (2006a, supplement) also present a tree that excludes the β-fibrinogen gene, which places the tropicbirds as sister to the turacos and kagu and sunbittern sister to the cuckoos, while Brown et al. (2008) put the tropicbirds next to the penguins. It is also notable that the oilbird, potoos, frogmouths, and nightjars do not group together when the β-fibrinogen gene is ignored.
Although these mitochondrial studies raise issues concerning the Metaves hypothesis, they have not reached the point where they can produce a comprehensive phylogenetic tree. Indeed, the limited taxon sampling means that branches may move substantially as data is added. Just compare the recent effort by Pratt et al. (2009) with Morgan-Richards et al. (2008) or Gibb et al. (2007).
Another recent alternate is Cracraft et al. (2004). At present, this is the only modern alternative that is both sensible and truly comprehensive.
There are also alternative forms of the Metaves hypothesis. One is given by Ericson et al. (2006a) in the supplementary material. In that tree, the Hoaztin is basal in Neoaves. The next branch includes the rest of the Columbimorphae. After that, the next division is between the Cypselomorphae and Coronaves. Hackett et al.'s (2008) version is a bit different from either of the Ericson versions, with the absence of the hoatzin being the major difference. They also mention the possibility that Metaves may not be a clade, although it shows as a clade in their maximum likelihood estimates.
The taxonomy presented here presumes that Metaves is a natural grouping, containing birds that are more closely related to each other than to the rest of Neoaves. It relies on Fain-Houde (2004), Ericson et al. (2006a) and especially Hackett (2008) for the organization of the non-passerines. I have inserted several higher level groups to organize the tree. See the next page for more on Metaves and Coronaves.
Evolutionary Timeline
Ericson et al. (2006a) also presented a timeline of avian evolution. Their paper suggests that at the very minimum, a dozen avian lineages survived the mass extinction at the end of the Cretaceous (the K/T extinction, about 65 million years ago). It's likely that the Paleognath lineages had already separated, so the number is probably higher. Indeed, Brown et al. (2007) argue that a minimum of two dozen lineages of modern birds survived the K/T extinction. More recently, Brown et al. (2008) suggest that at least 37 lineages date to the Cretaceous. They find that the actual number could be as high as 90.
In any event, by the end of the Eocene (about 34 million years ago), all of the modern bird orders (and many of the families) were distinct lineages. Similar results have been obtained in other studies such as Cooper and Penny (1997).
It's interesting to note that Brown et al's point estimate for the Passeriform lineage is almost 90 million years ago. It was not long ago that ornithologists considered the passerines to be a recent lineage, and many reacted with disbelief when DNA data suggested they might be near the base of Neoaves. The tree presented here places the root of the Passeriform branch in a basal position in Passerae. The Passeriformes come at the end of our list because of our convention of putting the largest group last.
Bird Fossils
The molecular estimates should be viewed somewhat skeptically. This applies even to calibrated estimates as in Ericson et al. (2006a), Brown et al. (2007), and Brown et al. (2008). Fossil support for these genetic estimates of timing has been very weak. This is a concern since molecular clocks cannot always be trusted (e.g., Groth and Barrowclough, 1999). Although there are possible Cretaceous fossils of modern birds, most are pretty fragmentary and one can't be sure they belong to modern birds (Neornithes). There are plenty of fossils of other birds---Ichthyornithes, Hesperornithines, and Enantiornithes---just not Neornithes.
Should the lack of fossils be a big concern? No! The fossil record is incredibly sparse. How sparse? Caley (2007) gives a figure of around 2000 birds known only through fossils, compared with an estimate of 1.6 million bird species that have existed. That means we have only found fossils of 1 out of every 800 bird species.
How many Neornithes were there in the Cretaceous? They seem to have been a minor component of the avifauna. Suppose there were 100 at the end of the Cretaceous. Recall that we may only need one or two dozen survivors. Suppose this had been a typical figure for the previous 25 million years and that the average species last for a million years. Then there were about 2500 Neornithe birds in the Cretaceous, so we should expect about 3 fossils. The numbers could be off by an order a magnitude, so not finding fossils is not too surprising.
It has also been suggested that location contributes to the problem. Since the vast majority of fossil collection has been in the northern hemisphere, one possible explanation for the paucity of supporting fossils is that most modern birds initially had a Gondwanan distribution (Cracraft, 2001; Ericson et al., 2002a). In that case, the lack of fossils merely reflects low collection effort in the right location.
The best fossil candidate does come from Gondwana, more specifically, Antarctica. It is Vegavis (Clarke et al., 2005). Clarke argues that Vegavis is very closely related to the Anatidae. It may even be in the Anatidae. Its existence implies that the Paleognaths, Galliformes, Anhimidae, and Anseranatidae were already separate lineages before the K/T extinction, as was at least one lineage in Neoaves.