Are parrots actually pigeons?

i-ce30618f32cd35ef1e33abfa57717143-psittaciform_skeleton_wikipedia_May-2009.jpg

Historically, an apparent absence of transitional forms has made it difficult to reconstruct the evolutionary affinities of the different modern avian 'orders'. As you'll know if you've been keeping up with the results of the various big molecular and morphological analyses - and who hasn't - the avian cladogram is gradually coming together, though areas of debate and disagreement remain. One of the most vexing areas has been the origin of the parrots, or psittaciforms. An idea frequently mooted in the ornithological literature is that parrots are close kin of pigeons and doves - the columbiforms - and in fact some authors have even implied or stated that parrots are part of Columbiformes. Say what? I think we need to look at this in more detail...

i-e909bbe976908d7cd53f416e7d76c55e-Feduccia_1996_cover_May-2009.jpg

The idea that parrots might be columbiform derivatives is perhaps best known thanks to its promotion by Alan Feduccia, author of the only 'mainstream' volumes on Cenozoic bird evolution (the 1980 The Age of Birds and 1996 The Origin and Evolution of Birds). In the first of these books, he wrote 'shorebird derivatives include the sandgrouse, doves, and pigeons (Columbiformes), and, through the tooth-billed pigeons, the parrots (Psittaciformes)' (Feduccia 1980, p. 98). In his second book, Feduccia referred in passing to parrots as 'the columbiforms' presumed close allies' (Feduccia 1996, p. 252). Though the inference from Feduccia (1980) is that tooth-billed pigeons are ancestral to parrots, the figure caption on p. 99 states 'The tooth-billed pigeons are probably surviving relicts of a group that became specialized after diverging from the main stem of columbiform evolution, and they show many anatomical features that would be found in the ancestral stock of parrots'. This implies convergence between tooth-billed pigeons and parrots, not direct affinity. Incidentally, the Tooth-billed pigeon Didunculus strigirostris is from Samoa, though it's known from fossils to have lived on Fiji, and an unnamed species of the genus is known from Tonga.

While writing these contradictory comments, Feduccia probably had in mind Philip Burton's 1974 paper on parrot and pigeon jaw and tongue morphology. Burton (1974)
showed that Didunculus was more like a parrot than was any other kind of bird in many details of cranial musculature. Burton listed five features seen in Didunculus which 'showed some approach to [the condition in] parrots' and was also impressed by features such as the form of the palatines and quadrates, the fused lower jaw, the long pterygoids, the short, deep upper jaw, and the broad nasal bars (pp. 272-273) [D. strigirostris shown below].

i-8488bff073c77c61be5dc87c9eb5b915-Didunculus_HBW_May_2009.jpg

In the conclusions of the paper, Burton proposed that Didunculus may exhibit shared derived states with parrots. Rather than proposing that Didunculus might be near the ancestry of parrots however, Burton chickened out and wrote 'More likely Didunculus is a relict survivor of a specialized group of pigeons which became separated early from the main stock of Columbiformes. This may not be the actual group from which parrots evolved, but clearly shows many of the anatomical features which might have been expected in the stock ancestral to parrots' (p. 274).

So while Didunculus was used by Burton as evidence supporting a possible link between pigeons and parrots, the similarities discovered between Didunculus and parrots were regarded by him as convergent: in other words, they were were dismissed as evidence for a close affinity. As it happens, Didunculus is almost certainly nothing to do with the ancestry of parrots, but Burton would have been justified in proposing a possible affinity at the time. So: why propose an affinity of parrots and pigeons when the 'trump card' (= the cranial characters of Didunculus) is deemed an example of convergence? Yes, why indeed.

Recent work on columbiforms supports the view of Goodwin (1967) and others that Didunculus is well nested within pigeons and is not a disparate relict or part of a group well separated from other pigeons. Janoo (1996) wrote that 'despite the morphological skull divergence, Didunculus is a typical columbine'; molecular studies show that Didunculus is part of the same columbid clade as Goura (crowned pigeons), Caloenas (Nicobar pigeons) and dodos and solitaires (Shapiro et al. 2002); and morphological work supports similar affinities but finds Gallicolumba to be close to these pigeons too (e.g., Goodwin 1967, Worthy 2001, Mahler et al. 2003) [dodo skeleton and model shown below, from the Oxford University Museum].

i-3bdafb79633ffbe84911ba277f667c6f-Raphus_OUM_May_2009.jpg

The bottom line is that, while Didunculus is rather like a parrot in some aspects of cranial morphology, it represents the extreme among a group of robust-skulled frugivorous pigeons and is nothing to do with parrot ancestry at all. It should not, therefore, be inferred to be suggestive of a pigeon-parrot link.

And - what are the affinities of parrots and pigeons? They are sort of close in one analysis (Livezey & Zusi 2007), but belong to fundamentally different branches of the neornithine tree in others (Fain & Houde 2004, Ericson et al. 2006, Mayr 2007, Hackett et al. 2008). Notably, no recent study has recovered a parrot-pigeon clade, least of all the inclusion of parrots within Columbiformes.

Coming next soon: the Birds Come First hypothesis!

Refs - -

Burton, P. J. K. 1974. Jaw and tongue features in Psittaciformes and other orders with special reference to the anatomy of the Tooth-billed pigeon (Didunculus
strigirostris
). Journal of Zoology 174, 255-276.

Ericson, P. G. P., Anderson, C. L., Britton, T., Elzanowski, A., Johansson, U. S., Källersjö, M., Ohlson, J. I., Parsons, T. J., Zuccon, D. & Mayr, G. 2006. Diversification of Neoaves: integration of molecular sequence data and fossils. Biology Letters 2, 543-547.

Goodwin, D. 1967. Pigeons and Doves of the World. British Museum (Natural History)

Fain, M. G. & Houde, P. 2004. Parallel radiations in the primary clades of birds. Evolution 58, 2558-2573.

Feduccia, A. 1980. The Age of Birds. Harvard University Press.

- . 1996. The Origin and Evolution of Birds. Yale University Press.

Hackett, S. J., Kimball, R. T., Reddy, S., Bowie, R. C. K., Braun, E. L., Braun, M. J., Cjojnowski, J. L., Cox, W. A., Han, K.-L., Harshman, J., Huddleston, C. J., Marks, B., Miglia, K. J., Moore, W. S., Sheldon, F. H., Steadman, D. W., Witt, C. C. & Yuri, T. 2008. A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763-1768.

Janoo, A. 1996. On a hitherto undescribed dodo cranium, Raphus cucullatus L. (Aves, Columbiformes), with a brief taxonomical overview of this extinct flightless Mascarene Island bird. Bulletin du Muséum national d'Histoire naturelle, Paris 4e série, 18, Section C, no 1, 57-77.

Livezey, B. & Zusi, R. L. 2007. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion. Zoological Journal of the Linnen Society 149, 1-95.

Mahler, B., Araujo, L. S. & Tubaro, P. L. 2003. Dietary and sexual correlates of carotenoid pigment expression in dove plumage. The Condor 105, 258-267.

Mayr, G. 2007. Avian higher- level phylogeny: well-supported clades and what we can learn from a phylogenetic analysis of 2954 morphological characters. Journal of Zoological Systematics and Evolutionary Research 46, 63-72.

Shapiro, B., Sibthorpe, D., Rambaut, A., Austin, J., Wragg, G. M., Bininda-Emonds, O. R. P., Lee, P. L. M. & Cooper, A. 2002. Flight of the dodo. Science 295, 1683.

Worthy, T. 2001. A giant flightless pigeon gen. et sp. nov. and a new species of Ducula (Aves: Columbidae), from Quaternary deposits in Fiji. Journal of The Royal Society of New Zealand 31, 763-794.

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Yeah, parrots are wierd. Isn't there evidence of a Cretaceous parrot? A beak or something?

Also, yeah, love that Birds Come First "hypothesis." I've read many variations. Maniraptors are proto-birds but originated in the Triassic (helluva ghost lineage) and share a sister-group relationship with Theropoda proper. Or Theropoda (proper) branched off FROM birds in the Triassic or, perhaps my favorite theory, ALL THEROPODS (proper) are descended from unbelievably basal birds during the Triassic, like Proavis or Scansoriopteryx (I guess).

The proof? Scansoriopteryx has an elongate third finger. So does Herrerasaurus. CASE CLOSED.

The Best Hypothesis is Birds Come Twice fom Apes:

Non-maniraptoran theropods are derived German paleontologists.
Maniraptors (and birds) are basal British ornithologists.

;-)

Sorry, in the Comment n°3 I've used an Italian Acronym.

By Andrea Cau (not verified) on 23 May 2009 #permalink

I think there is at least two jaws believed to be from Psittaciformes that date from the Maastrichian, but they are usually assumed to be from non-neornithe maniraptors.

If I'm not mistaken the most recent genetic studies show an affinity between parrots, passerines, falcons/new world vultures and seriemas. Other than the Gondwannan origin is there anything to suggest any sort of affinities between said bird clades?

Oh, and pigeons are basal members of Neognathae, according to said study. Doesn't help very much

I think there is at least two jaws believed to be from Psittaciformes that date from the Maastrichian, but they are usually assumed to be from non-neornithe maniraptors.

AFAIK there's just one (Stidham 1998), and that one either belongs to a lorisid (!!!) or not to a psittaciform at all. The latter looks more parsimonious to me.

By David MarjanoviÄ (not verified) on 24 May 2009 #permalink

Zach: I think Darren is referring to Olshevsky's "Birds Came First" theory, which basically claims that all theropods are descended from volant ancestors.

my interpretation of the passages quoted would be that they're trying to avoid calling Didunculus a living fossil from the times of parrigeons (which would, of course, be bullshit) by describing them rather as the evolved descendants of the group of pigeons from which parrots branched.

Feduccia's writing in this case seems rather sloppy.(insert mean remark about other things he's written, here..)To me it seems like he couldn't really make his mind up about the origin of parrots but was really looking for a way to tie them to his beloved 'transitional shore-birds'. Even if this required proposing a pseudo-phylogeny-that-really-isn't-pseudo-but-probably-is to derive parrots from pigeons.
While it's true that particular view (parrots and pigeons as closest kin) has been popular in the past, it was already out of date by the time Feduccia's book was written. Once again, Feduccia's intuitive scenario appeared to him to blast apart any modern research by means of his I-am-sceptical-therefore-it's-not-true beams of apparent logic.
Anyhow, if parrots do belong to a clade of cariamaeans, falcons and passeriforms (for which the name Mirandornithes would have been most fitting!) the most recent common ancestor of parrots and their closest relatives probably was a small, vocal and inquisitive bird spending time on both the ground and in trees...a far more appealing image then a fat, bigheaded pigeon. Note that I'm not trying to insult Didunculus here..it's a bird I'd love to see alive.

[â¦] a pseudo-phylogeny-that-really-isn't-pseudo-but-probably-is [â¦]

Once again, Feduccia's intuitive scenario appeared to him to blast apart any modern research by means of his I-am-sceptical-therefore-it's-not-true beams of apparent logic.

:-D

How true, how true.

By David MarjanoviÄ (not verified) on 24 May 2009 #permalink

"Anyhow, if parrots do belong to a clade of cariamaeans, falcons and passeriforms"

Don't forget new world vultures are appearently involved as well, within falcons of course. I think the bird drawn in the cover of Feduccia's book serves perfectly, even if it looks like a nightjar

Carlos: I could swear you're referencing Hackett (2008) which found a falcon/parrot/passerine/seriema clade - cathartids were found to be basal Accipitriformes. In fact I've only seen cathartids floating around "Conglomerati"/"Cracrafti" or as basal Falconiformes/Accipitriformes... unless there's something I missed.

Hackett, Shannon J. et al. 2008. A Phylogenomic Study of Birds Reveals Their Evolutionary History. Science 320, 1763-1768.

David:

AFAIK there's just one (Stidham 1998), and that one either belongs to a lorisid (!!!) or not to a psittaciform at all.

Does "lorisid" refer to loris (as in the prosimian mammal) or lory (as in a certain kind of psittaciform)?

The author of the blog stated that the inclusion of New World vultures at the base of Accipriformes was an accident when making the cladogram image, because it was stated in the blog that cathartids were closer to falcons (and the author even apoligised for the mistake). Of course, that might had been an older opinion that was changed in favor of new data

Carlos:

the bird drawn in the cover of Feduccia's book serves perfectly, even if it looks like a nightjar

That bird is the Pleistocene owlet-nightjar Aegotheles novaezeelandiae from New Zealand; it was, according to Feduccia, "flightless or nearly so".


novaezeelandiae

...and that should be novaezealandiae. Sorry for the typo.

But the external appearence could had been similar to that of the last common ancestor between the mentioned avian orders, except for the rostrum (note: external appearence)

In the most recent molecular phylogenies the parrots are specifically a sister group of the passerines with high statistical support. The areas of the brain involved in vocal imitation appear to be very similarly positioned in these two clades. In the pigeons there is no evidence for any form of vocal imitation. So the emergence of neural and structural cognates of intricate sound production might be an ancestral feature of the parrot-passerine clade.

Does "lorisid" refer to loris (as in the prosimian mammal) or lory (as in a certain kind of psittaciform)?

Of course I mean the latter... so maybe it's "loriid". I keep confusing these names.

and that should be novaezealandiae.

Are you sure it shouldn't be novaezelandiae? There's no ea in Dutch.

By David MarjanoviÄ (not verified) on 24 May 2009 #permalink

A clade uniting passeriforms, falconids, cariamiforms and parrots would be consistent with a Neogondwanan origin. Ericson's phylogeny put Cathartiforms next to Accipitrids, but since cathartids were a South American group I prefer them as closer to this Neogondwanan cluster. Unless... proto-catharids flew over Atlantic from African during Upper Eocene (together with monkeys and agoutis?)

By J.S Lopes (not verified) on 24 May 2009 #permalink

Unless... proto-catharids flew over Atlantic from African during Upper Eocene (together with monkeys and agoutis?)

*blink* Monkeys and agoutis flew across the Atlantic?

I seem to recall hearing of a study (with a badly saturated dataset) that found Chiroptera paraphyletic wrt the rest of Mammalia. Time to reconsider this option?

By Andreas Johansson (not verified) on 24 May 2009 #permalink

And what's up with the formating there? Why does the "*blink*" extend into the left margin?

By Andreas Johansson (not verified) on 24 May 2009 #permalink

eh...sorry... I didn't mean to say that monkeys and rodents flew over ATlantic... but they came from Africa - it's sure.

By J.S. Lopes (not verified) on 24 May 2009 #permalink

Post #19 deserves this blog's version of Pharyngula's "Molly" award!

David:

Of course I mean the latter... so maybe it's "loriid". I keep confusing these names.

Yeah, I'm almost certain that the birds should properly be 'loriids', not 'lorisids'. Which is why I asked; you don't usually make etymological mistakes, ever.

Are you sure it shouldn't be novaezelandiae? There's no ea in Dutch.

novaezealandiae is how it's spelled in both Feduccia (1996) and, e.g., Holdaway (1989). Bad Dutch but standard cod Latin?

Incidentally, Holdaway, who puts this species in another genus, Megaegotheles, says that this owlet-nightjar may actually have survived into the 19th century.

Reference:

Holdaway, R.N. 1989. New Zealand's pre-human avifauna and its vulnerability. New Zealand Journal of Ecology 12 (Supplement), 11-25.

Brian:

To me it seems like he couldn't really make his mind up about the origin of parrots but was really looking for a way to tie them to his beloved 'transitional shore-birds'. Even if this required proposing a pseudo-phylogeny-that-really-isn't-pseudo-but-probably-is to derive parrots from pigeons.

Not to defend Feduccia's views (and I don't know precisely what he wrote about this topic in his 1980 book) but I think the 'transitional shorebird' connection would follow naturally from loosely considering the sandgrouse as 'intermediate' between shorebirds and pigeons. Thus, if you'd assume a columbiform ancestry for psittacids, you'd get
shorebird -> sandgrouse -> pigeon -> parrot.

Of course, some later molecular studies have cast doubt on the close relationship between shorebirds and sandgrouse+pigeons (or between sandgrouse and pigeons, for that matter). But to assume, on morphological grounds, that sandgrouse are reasonable proxies of a shorebird - pigeon intermediate would have been pretty uncontroversial in 1980.

And what's up with the formating there? Why does the "*blink*" extend into the left margin?

Because you didn't leave an entire empty line after the blockquote.

In general, the new ScienceBlogs format sucks, even worse than the old one. Obviously their web designers never comment here. Should all be fired, along with the moron who hired them.

By David MarjanoviÄ (not verified) on 25 May 2009 #permalink

Although⦠I note with delight that the blockquotes are now indented again! For a few weeks they were, well, slightly edented. Made them difficult to recognize.

By David MarjanoviÄ (not verified) on 25 May 2009 #permalink

Comparing this "Southern" clade including parrots-falcons-songbirds-cariamas to another clade including woodpeckers-rollers-accipitrids-owls-mousebirds we found a lot of convergences: falconids x accipitrids, cariamas x sagittariids, passerines x mousebirds (and Paleogene fossils), parrots x trogons. It seems reasonable if we consider a paleobiogeographic scenario with "parrot-allies" evolving in South America-Antarctica-Australia and "owl-allies" evolving in Old World-Africa.

By J.S. Lopes (not verified) on 25 May 2009 #permalink

Many of these supposed affinities are so laughable, that we need another blog post on dinosaurs immediately!

Falcons more related to songbirds than to accipiters...

Feduccia: I don't wish to sound rude, but it is not just his 'bird origins' ideas that are whackaloon/wackaloon. Virtually all of the ideas promoted in his works on neornithine relationships are also problematic and unparsimonious. In fact, it is very unfortunate that he is the only person who writes big books on bird evolution. Come on paleo-ornithologists, why so lazy?

By Daniella Perea (not verified) on 25 May 2009 #permalink

Daniella:

he is the only person who writes big books on bird evolution.

Don't forget Gerald Mayr.

The idea of a passerine/falcon/seriema/parrot clade converging with one of accipiterids/owls/mousebirds/piciformes/coraciiformes is quite interesting; both clades are usually classified as "higher landbirds", which suggest that said clade went through a massive radiation during the Paleo/Eocene

Mayr's books is on the Paleocene and Eocene taxa, it is not a general text on bird evolution as a whole. We are still in need of such a book.

By Daniella Perea (not verified) on 25 May 2009 #permalink

"It seems reasonable if we consider a paleobiogeographic scenario with "parrot-allies" evolving in South America-Antarctica-Australia and "owl-allies" evolving in Old World-Africa."

Stem-group cariamans (idiornithids, bathornithids, ameghinornithids), parrots (quercypsittids etc.), probably passerines (zygodactylids etc.) and possibly falcons are known from Paleogene Europe/North America, though. In response to some previous comments: yes, the latest molecular studies find cathartids closer to accipitrids than to falconids, and I should also mention that some of the oldest cathartids (Diatropornis, Parasarcoramphus) come from Europe. Note that I don't have Gerald Mayr's new book yet, so I might have missed some new developments.

By Lars Dietz (not verified) on 25 May 2009 #permalink

I know about Europeans putative Cariamaeans, and this relationship is very intriguing, since cariamas were not strong flyers nor good swimmers. A possible link between South American and European Eocene faunas could be Indo-Madagascar. Maybe a Neogondwanan proto-Cariamaean stock could be splitted into an South American-Antarctic (Neogondwanan) subgroup and an Indo-Madagascarian one, with the Indian stock reaching Africa and/or Asia later. This pattern of diffusion was detected in freshwater fishes, turtles and anurans.

By J.S. Lopes (not verified) on 25 May 2009 #permalink

Ostriches are also likely of indian origin; they appeared in the european fossil record well before than in the african one, and thus it could be that Paleotis and kin invaded Eurasia from India. The same might apply for some other bird clades as well

Carlos wrote...

Ostriches are also likely of indian origin; they appeared in the european fossil record well before than in the african one, and thus it could be that Paleotis and kin invaded Eurasia from India.

Check out Leonard et al. (2006). While they didn't comment on Palaeotis (but are surely aware of it: look at the full authorship), they regarded Struthio coppensi from the Lower Miocene as the oldest ostrich, and noted that the majority of Miocene ostrich remains are African (the only non-African records are from the Middle and Upper Miocene of Turkey and Moldovia). They concluded that 'the early radiation of ostriches took place in Africa, followed by later dispersal and subsequent extinction in Europe' (p. 393). Hmm.

Ref - -

Leonard, L. M., Dyke, G. J. & Walker, C. A. 2006. New specimens of a fossil ostrich from the Miocene of Kenya. Journal of African Earth Sciences 45, 391-394.

Yeah - I've got no doubt that Megaegotheles could've persisted into the 19th century. I've seen a skull that was picked up loose, perfectly preserved, from a limestone cave. Very very delicate zygomatic arches intact (showing my ignorance here- is that what they're called in birds too?). Sure didn't look like a sub-fossil even.

What's even more amazing is that it came through intact like that in the post ! I delivered it to the National Museum by hand...

By Ian Govey (not verified) on 25 May 2009 #permalink

Well, early Miocene is already after the contact between Africa and Eurasia/Laurasia (around the Oligocene/Miocene boundary), so this doesn't help. Someone will have to sit down with Palaeotis (and Remiornis and Eleutherornis and I forgot what else!) and do a serious phylogenetic analysis. (With lots of lithornithids and tinamous, of course. And Diogenornis and whatnot.)

By David MarjanoviÄ (not verified) on 25 May 2009 #permalink

David writes...

Well, early Miocene is already after the contact between Africa and Eurasia/Laurasia (around the Oligocene/Miocene boundary), so this doesn't help.

I see your point, but are you sure it 'doesn't help'? Even if Africa and Eurasia are in contact at the time, doesn't a preponderance of African record imply an African origin for the group? Parsimony says it does.

As for the phylogenetic position of Palaeotis within palaeognaths, Dyke & van Tuinen (2004) reported it to be the sister-taxon to Ratitae.

Refs - -

Dyke, G. J. & van Tuinen, M. 2004. The evolutionary radiation of modern birds (Neornithes): reconciling molecules, morphology and the fossil record. Zoological Journal of the Linnean Society 141, 153-177.

"Ratitae" as in the old sense of the word or did he included tinamous in his study? (since it seems tinamous might be within ratites)

I see your point, but are you sure it 'doesn't help'? Even if Africa and Eurasia are in contact at the time, doesn't a preponderance of African record imply an African origin for the group? Parsimony says it does.

For the Miocene-and-later clade, yes, of course. Before that, it doesn't really say anything.

And then, of course, no paleognaths whatsoever are known from the Paleogene of Africa, unless Eremopezus counts, and it probably doesn't. In Europe and North America there are at least several candidates.

As for the phylogenetic position of Palaeotis within palaeognaths, Dyke & van Tuinen (2004) reported it to be the sister-taxon to Ratitae.

Fine, except that, as it turned out last year and as Carlos mentions, there is no such thing as Ratitae.

It might also be interesting that those same analyses find Struthio as the sister-group to the rest of Palaeognathae...

By David MarjanoviÄ (not verified) on 26 May 2009 #permalink

Ostriches would be considered as an Indian stock only if Holarctic Lithornithids were basal Struthioniforms. All "true" ostrich fossils point to an African origin. It would be interesting if North African Paleogene sites provided some evidence of ostrich ancestors.

By J.S.Lopes (not verified) on 26 May 2009 #permalink

There are transitions between "aepyornithid-like" and ostrich eggshells from Miocene Namibia (Diamantornis). Of course, this doesn't tell us where ostrich ancestors lived before that, especially as the same kind of eggshells were also found in Abu Dhabi. Lithornithids appear to be a (paraphyletic?) group of stem paleognaths, but I agree that we need a good phylogenetic analysis of all fossil paleognaths.

By Lars Dietz (not verified) on 26 May 2009 #permalink

A question that occurs me is: what were the prototypes of neornithean irradiations?
The proto-paleognath would be ground-dwelling, walking, quail-like bird? Herbivore? Omnivore?
And the proto-neognath? A small flying insectivore? omnivore?

By J.S. Lopes (not verified) on 26 May 2009 #permalink

Appearently the prototype of neornithe evolution was a shorebird like thing; it makes sense, since the closest relatives of modern birds back in the Cretaceous teamed from shorebird like things

What's the "Molly" award? Is it bad?

No. (That's why it's an award.)

And the proto-neognath? A small flying insectivore? omnivore?

No, pretty much the same as the first paleognath. Compare galliforms and screamers (Anhimidae).

It looks like Feduccia was wrong about that, too...

By David MarjanoviÄ (not verified) on 26 May 2009 #permalink