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Tetrapod Zoology

Tetrapod Zoology

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Ratites in trees: the evolution of ostriches and kin, and the repeated evolution of flightlessness (ratite evolution part II)

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There really aren't enough good reconstructions of Aepyornis, the recently extinct elephant bird of Madagascar, out there. So here's another one. Image by Brian Choo. Read on for more about elephant birds.

Regular Tet Zoo readers will recall the article from March on ratite and tinamou evolution. Ratites, just in case you don’t know, are the flightless kiwi, ostriches, rheas, emus and so on, while tinamous are their diminutive, flight-capable, superficially pheasant-like close relatives. Together, ratites and tinamous are grouped together as the palaeognaths (properly: Palaeognathae). Some archaic fossil groups from the Cenozoic – most notably the long-billed, flight-capable lithornithids of the European Paleogene – are regarded as palaeognaths outside of the tinamou + ratite clade.

As discussed or hinted at in the previous palaeognath-themed article, several major areas of controversy and uncertainty make our evolving understanding of palaeognaths an area of special interest. Thoughts about the history of these birds have involved major, long-running debates on biogeography, the evolution of flightlessness and large body size, the alleged important of paedomorphosis, the issue of whether the ratite body shape evolved once or several times, and the matter of whether palaeognaths are ‘primitive’ with respect to other birds or not. My initial plan was to publish all of my ratite/tinamou-themed thoughts in one go. But I clearly have precognitive abilities of some sort, since no sooner had I published the part I article than I learnt about a couple of new and exciting papers that were set to appear in the imminent future. It seemed wisest to wait for those papers to come out... so here we are. Read on.

Lest we forget, ratites can be weird, and also weirdly cute. Here's a Darwin's or Lesser rhea (Rhea/Pterocnemia pennata), lying on its belly on the grass. Weird. Photo by Darren Naish.

Ratite polyphyly: a neat idea, shame it’s not supported by evidence

In the previous article I discussed the sometimes popular (but likely erroneous) idea that ratites might owe their unusual anatomical features to paedomorphosis (the process in which developmental timing changes such that adults retain features more usually typical of their juvenile stage). I don’t think that the data supports the view that paedomorphy might have been important in ratite evolution, but the idea that it is ties in with another evolutionary hypothesis sometimes entertained about these birds: are they all really close relatives, or could they, actually, have arisen independently from distantly related ancestors? This is known as the polyphyly hypothesis (‘polyphyly’ being the term used for cases where members of a group do not share a single ancestor, but have some or many disparate evolutionary origins).

Nobody has ever formally proposed a model of palaeognath polyphyly like the one you see whimsically depicted here. However, some of the relationships hinted at in this diagram have been proposed by some supporters of palaeognath non-monophyly. Image by Darren Naish.

There was a time when the idea of ratite polyphyly was fairly popular. I was surprised to read, in Hans Hvass’s 1963 Birds of the World that “It was at one time thought that [ratites] were all related; but there is no doubt that they originate from different groups of early birds” (Hvass 1963, p. 199). As often with views of this sort, the notion of ratite polyphyly was never explained in detail, and usually only alluded to in cursory fashion. To be fair, Victorian arch-anatomist Richard Owen made some specific statements about the concept of ratite polyphly, suggesting that ostriches were allied to bustards, and that kiwi and moa were close to megapodes. And the idea that ostriches might be allied to (or descended from) a weird group of didactyl crane-like birds from the Eocene and Oligocene called eogruids was promoted for a while during the 1970s and 80s.

Diversity in ratite pelvic anatomy. They're different, but are they really _that_ different? Redrawn after a diagram in Feduccia (1996), image by Darren Naish.

But if you read the books and articles of Alan Feduccia and Storrs Olson, you get the impression that various ratites could have evolved independently from such groups as ducks, geese, ibises or the crane-like eogruids... it being, alas, about impossible to pin these authors down on specific statements, or on specific bits of evidence that might really link the different ratite lineages to any non-ratite ones. In fact, this view of ratite polyphyly seemingly arose because the several ratite lineages look different in detail.

Think about wings, for example. All ratites have a humerus that’s somewhat longer than the lower arm, but while ostriches and rheas have long wing feathers that attach to long, tridactyl, two-clawed hands, emus and cassowaries have very short wings with a substantially reduced, single-clawed carpometacarpus and poorly ossified (or unossified) splint for the alula. Kiwi have stick-thin wings where the manus is monodactyl, and moa have no wings at all. An interesting and perhaps surprising amount of variation is also seen in ratite scapulocoracoid and pelvic anatomy. Take this statement: “The diversity of ratite pelvic structure would be astounding if all derived directly from a single flightless common ancestor and is perhaps best explained by ratites having evolved through a combination of increasing body size and neoteny” (Feduccia 1996, p. 273).

Diversity in the hands of living ratites. At top left, a de-feathered ostrich wing (photo by John Hutchinson); at lower left, de-feathered emu wing (photo by Mathew Wedel); at right, manual skeletons from Parker (1888).

Personally, I think that things have been over-stated, since you can see profound disparity in the skeletons of numerous animal groups where lineages have been separate for some tens of millions of years. Nevertheless, the point remains that ratites are different enough in anatomy for us to at least suspect that something weird has gone on as goes the evolution of their bauplan. In other words, the very different wing and pelvic anatomies seen in the different ratite lineages might indicate that those different lineages evolved their ratite-type morphology independently. [Image below by Rei.]

Ostrich wings are proportionally longer than those of many other ratites, and their long, showy remiges make them look much larger in the live animal. Image by Rei, licensed under Creative Commons Attribution-Share Alike 3.0 Unported license.

But does this mean that the different ratite groups emerged independently from different neognaths? Could ducks or ibises or cranes or whatever evolve into ‘ratites’ if only they were given enough time? (this being the possibility that Feduccia and Olson appear to favour). The short answer is no: ratites are united by a list of anatomical characters that aren’t seen in other birds (e.g., Bledsoe 1988, Lee et al. 1997, Livezey & Zusi 2007, Mayr & Clarke 2003, Bourdon et al. 2009), and a large number of molecular studies consistently find ratites to group together, and to group together with tinamous (e.g., Haddrath & Baker 2001, Hackett et al. 2008, Harshman et al. 2008, Suh et al. 2011, Smith et al. 2013, Yuri et al. 2013, Mitchell et al. 2014). There have, in other words, never been good indications from quantitative analyses that palaeognaths are not monophyletic.

A tree for ratites

Palaeognaths: an impressive amount of diversity in size and shape. Or is that disparity? Image by Darren Naish.

Within the palaeognath clade, how might the different lineages be related to one another? Over the decades, people have of course proposed several good, sensible and perfectly logical ideas about palaeognath phylogeny. Tinamous (endemics to the Americas) are small, capable of flight and without the anatomical specialisations of ratites, so they’re presumably the sister-group to ratites. Moa and kiwi are both endemic to New Zealand, so it seems logical to assume a close affinity between both groups. Cassowaries and emus both inhabit Australia and look fairly alike anyway, and ostriches and rheas look about enough alike to indicate that they’re presumably close relatives, that pesky Atlantic Ocean being a bit of a pain.

The history of ideas about palaeognath phylogeny are complex (err, just as they always are) and I’m not about to provide a thorough summary here (if you want to see such a summary, consult Sibley & Ahlquist (1990)). Three things about ‘historical’ views on palaeognath evolution are especially intereting. (1) Tinamous were often grouped with galliforms, mostly because authors were confused either by convergence, or by the shared presence of primitive characters; (2) several authors favoured ideas about ratite polyphyly like those discussed above; and (3) at least some authors who interpreted ratites as monophyletic arranged the lineages in a fairly ‘modern’ phylogeny (e.g., Mivart 1877).

The ‘modern era’ of palaeognath phylogeny originated with Joel Cracraft’s 1974 study (Cracraft 1974). Based mostly on the distribution of select skeletal characters, he proposed that kiwi and moa were close kin, and that they were outside a clade that contained all other ratites, the topology of which was (elephant birds + ((emus + cassowaries) + (ostriches + rheas))). Note, however, that he only used 25 characters (Cracraft 1974), and subsequent workers pointed to problems with certain aspects of his analysis.

Cracraft's (1974) hypothesis of palaeognath phylogeny. I used the same taxonomic names that he did (some of which are a bit odd compared to those used by others). Image by Darren Naish.

Modern palaeognath phylogenies - this one is based on that recovered by van Tuinen et al. (1998) - have tended to find ostriches to be the sister-group to remaining ratites. Image by Darren Naish.

The idea that ostriches and rheas are close relatives (a hypothesis supported by Cracraft) has often been popular – they look superficially similar and are fairly alike in ecology and behaviour – but it isn’t supported by molecular analysis, nor by more recent examinations of the distribution of anatomical details. Ostriches have most frequently been recovered as the sister-group to the remaining ratites (Prager et al. 1976, van Tuinen et al. 1998, Harshman et al. 2008, Phillips et al. 2010, Smith et al. 2013, Baker et al. 2014, Mitchell et al. 2014), though note that rheas have occupied this position in some other studies (Lee et al. 1997). Cassowaries and emus are uncontroversially recovered as sister-taxa in just about all analyses. What about kiwi? The fact that moa are endemic to New Zealand has of course contributed to the idea that they’re most closely related to kiwi. Cracraft (1974) found two tarsometatarsal characters that seemed to support this possibility. For a while, this meant that people thought of the proportionally enormous kiwi egg as a sort of evolutionary holdover from far bigger-bodied ancestors. This is a somewhat weird idea, given how labile traits like egg size are in other bird groups. [In image below, moa photo by Ghegoghedo.]

Extinct ratites: where do they fit in the phylogeny? At left, the moa Emeus and Pachyornis (image by Ghedoghedo, licensed under Creative Commons Attribution-Share Alike 3.0 Unported license.); at right, the elephant bird Aepyornis (image in public domain). Note the interesting difference in toe length and sternum size.

What about the extinct ratites: the elephant birds (or aepyornithids) and the moa (or dinornithiforms)? The news about moa isn’t news anymore – it was a huge surprise when first announced but is now familiar stuff. Moa, it seems, are the sister-group to tinamous. This relationship was first reported by Phillips et al. (2010) and later reported or discovered by Smith et al. (2013), Baker et al. (2014) and Mitchell et al. (2014). Note that a few other studies had also found tinamous to be nested somewhere within ratites (Harshman et al. 2008, Hackett et al. 2008, Faircloth et al. 2012). If correct*, this all means that ratites as conventionally conceived aren’t monophyletic, since tinamous – which have never been regarded as ratites under any understanding of the word – are deeply nested within the clade that includes all ratite lineages.

* I’ve recently learnt about an unpublished thesis that points to problems with published phylogenies nesting tinamous within ratites (Scherz 2013). I’m not convinced that it overturns the signal that seems to be emerging, but it does point to ongoing problems concerning lack of data.

Tinamous are really ok once you get to know them. This is a Patagonian or Ingouf's tinamou (Tinamotis ingoufi); image by CHUCAO, licensed under Creative Commons Attribution-Share Alike 3.0 Unported license.

Finding tinamous to be nested within ratites is a big deal [adjacent tinamou image by CHUCAO]. Given that ratites are flightless, does this mean that flight re-evolved in the lineage leading to tinamous? That would be pretty radical and surprising, not least because this has (so far as we know) never happened elsewhere in any other bird lineage. It would also be a big deal because all the ratite lineages – that is, all the outgroups to tinamous in these new phylogenetic topologies – possess a set of features which seemingly prevent them from ever evolving the ability to fly again (like those significantly simplified, reduced wings, modified sternum and scapulocoracoid, absence of the furcula and heavy-boned, massive hindlimbs).

What’s the alternative? Obviously, that flightlessness evolved independently on several occasions within palaeognaths (Harshman et al. 2008, Phillips et al. 2010, Smith et al. 2013). Exactly how many times depends on the preferred topology. Three or four times looks most likely, but it was perhaps as many as five times... in ostriches, in the cassowary-emu clade, in kiwi, in rheas, and in moa (what about elephant birds? Hold on) (Harshman et al. 2008, Phillips et al. 2010, Smith et al. 2013). So, here we have an explanation as to why the members of the different ratite lineages look so distinct as goes their wings and hips and so on: they evolved their big, flightless forms independently from smaller, flight-capable ancestors. If this is true, ratites like ostriches and rheas and elephant birds are a good example of parallelism – the phenomenon whereby close relatives convergently evolve similar appearances.

The newest palaeognath phylogeny: according to Mitchell et al. (2014), tinamous are close to moa (again), but now kiwi have a sister-group relationship with elephant birds. Say what? Image by Darren Naish.

The newest news on palaeognath phylogeny concerns Mitchell et al.’s (2014) paper in Science. They successfully retrieved mitochondrial DNA from the elephant bird taxa Aepyornis hildebrandti and Mullerornis agilis, which is a big deal in itself. But while elephant birds look something like moa or ostriches, the DNA shows “unequivocally” that they’re closest to kiwis, a surprising result that not only seems discordant with anatomy and ecology but also with distribution. In fact, it seems to absolutely contradict the idea that ratites were ancestrally flightless and owe their distribution to continental breakup, and can only sensibly be explained by over-water dispersal (Mitchell et al. 2014).

The point has already been made elsewhere online that an entire kiwi could just about fit inside the egg of Aepyornis; both taxa now seem to be close relatives. Image by Kyle Davis and Paul Scofield, Canterbury Museum.

The shape of palaeognath phylogeny now suggests that flight capability was widespread, even ubiquitous, across the clade, with large size and flightlessness evolving independently, apparently early on in the Cenozoic and in the wake of the KPg extinction event. Mitchell et al. (2014) in fact even suggest that big-bodied palaeognath groups evolved large size because they were among the first animals with this evolutionary potential within their respective ecosystems: those groups that arrived later on in the same places were then 'denied' the opportunity to also evolve large size in the same way. So, kiwi and tinamous are small because moa and rheas, respectively, ‘got their first’. Intriguing stuff.

This is far from all that there is to say about palaeognath evolution and history, of course, but (for now) we have to stop there. We’ll no doubt be coming back to this fascinating group again. For previous Tet Zoo articles on ratites and neornithine bird evolution in general, see...

Refs - -

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The views expressed are those of the author and are not necessarily those of Scientific American.

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