Dinosaur to bird tail transition. Testing the theory. Genetics and the fossil record.

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TAIL DEVELOPMENT: Tail termination

One likely candidate for this deceleration is WNT3a. While somitogenesis is robustly proceeding, up to HH (Hamburger Hamilton [92]) stage 21, WNT3a is highly expressed in the tail mesenchyme, but as somite addition and the need for PSM nears its close, WNT3a is gradually downregulated between HH22 and HH25 [42]. RALDH2, an enzyme involved in the synthesis of RA from vitamin A, is correspondingly upregulated in the tail mesenchyme in the chick and is thought to be responsible for WNT3a and FGF8 downregulation. This creates an imbalance of signaling factors, and thereby promotes the effects of RA. Exposing mouse embryos to increasing levels of RA induces more severe axial truncation (Figure 6A) [93]. In addition to contributing to the loss of the growth factor Fgf8, RA causes differentiation of somitic cells and concomitant reduction in cell division; without Wnt3a, these effects act as barriers to further somite addition. In the mouse, RA is also promoted by downregulation of Cyp26a1 [42], an enzyme that normally metabolizes RA [94]. When Cyp26a1 is downregulated, RA concentration effectively increases, further inhibiting tail growth [95,96]. Interestingly, a critical level of RA signaling is required, as either augmenting or decreasing the amount of RA causes premature termination of somitogenesis [93,97,98]. In this finely tuned system, RA is required for maturation of recently made somites before the next pair of somites can form, but prolonged exposure to RA prevents further somite addition. Wnt3a expression also affects somitogenesis via its cross-talk with the Notch pathway. Specifically, Wnt3a and Notch pathway genes regulate each others' expression levels and patterns [57,99- 103], and Notch pathway genes are intrinsically tied to the segmentation clock and somite boundary formation [47,48,104]. As an indication of the coordination between these various pathways, loss of Fgf4 and Fgf8 in the mouse tail PSM results in loss of Wnt3a, downregulation of Notch signaling, and inhibition of Cyp26a1 [99], all of which act together to prematurely truncate the tail. Since Wnt3a also influences the expression of Fgf8 [103], downregulation of Wnt3a at the end of somitogenesis inhibits tail growth by influencing both RA effects as well as through inhibition of Notch-directed somite formation and maturation.

If the somites themselves are removed, neural crest cell delamination and subsequent migrationcome to a halt; an imbalance between Noggin and Bmp4 is thought to be responsible [110]. Reminiscent of the balance between Wnt3a, Fgf8 and RA, there is also a balance between Noggin, Shh and Bmps between different structures in the tail. The opposing functions of these proteins help to pattern the neural tube [111] and are also involved in somite segmentation and differentiation [112]. Disruption of this balance likely plays multiple roles in terminating elongation of the tail.

Hox genes. These delineate tail regions and determine the number of somites that are formed for each species. The Hox genes that are expressed right at the end of the tail act to terminate tail growth. Thus, over-express all Hox13 paralogs (that is, each gene in the A, B, C and D cluster) at the posterior end of the mouse or chick embryo and the tail is terminated prematurely. Against this, knock out these genes, and tail structures grow bigger and there are more of them. The tail elongates. There are several reasons for this knockout causing a longer tail - apoptosis in the PSM is interfered with, as are other signaling cascades which limit tail growth. Conversely, with the Hox13 paralogs in place, the termination signals are maintained as is apoptosis in the PSM.

The authors sum up this long and complex section of the paper as follows:-

To summarize, perturbations in virtually any of the tail elongation processes described above lead to termination of extension, and numerous perturbations are built into the axial extension system to ensure proper tail length. Imbalances in the Wnt/Fgf/RA and Noggin/Shh/Bmp gradients are largely responsible for stopping tail growth. Once disrupted, the signaling cascades generated from the gradients no longer properly coordinate with other cascades such as Notch, thereby disabling the elongation machinery. Hox13 paralog genes further inhibit tail elongation, likely through their interactions with the regulatory factors that control these gradients [81]. Finally, increased apoptosis at the termination of somitogenesis removes all remaining progenitor cells. All of these coordinating pathways are orchestrated through the different tail structures, and signaling between the structures maintains their inter-dependence so that if even one structure fails, the rest eventually follow suit. Species-specific differences in the way the orthologous pathways are modulated likely account for the varying tail lengths observed among vertebrates [123,124].

Hox13 paralogs. The vertebrae are bigger and of a slightly different shape. And two extra vertebrae (asterisks) form in the tail. Because the Hox13

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TAIL DEVELOPMENT: Skeletal development of the bird synsacrum and tail1 thoracic, 6 lumbar, 2 sacral and 5 sacral-caudalossification centers = regions where ossification begins

sacrum = a triangular bone in the lower back formed from fused vertebrae

synsacrum = an elongated composite sacrum made up of fused or partly fused vertebrate and found in birds and some extinct reptiles.

transverse process = a small bony projection on the right and left side of each vertebrae.



Now that we know what tails are, how tails form and some of the things that make them stop growing, we can begin to look at mutations that affect tail growth. This is the topic of the next section. What is observed today, informs what possibly happened at the dinosaur bird transition.







To be continued ...




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MUTATIONS THAT CAUSE TAIL TRUNCATION




The paper now begins to discuss the observations that are directly relevant to possibilities regarding the dinosaur to bird tail transition. Given a genetic program that specifies an organism’s tail including at what point it has to stop extending lengthwise, what are the mutations that can cause a long tail to become a short one, and what are the mutations that can cause vertebrae fusion at the tail end.

The authors point out two possibilities mentioned previously. Given the nature of the program that causes the tail to grow then stop growing:-

1) There may have been only one critical mutation. That is, the current fossil record can be taken on face value. It is complete enough to show us that the transition was sudden.

2) There may have been several critical mutations. The fossil record at the moment makes the transition look sudden, but the record is actually incomplete.

The genetics of this transition is complicated by the fact that there are several kinds of mutations that could have been involved:-

1) Gene coding sequence mutations. That is, mutations to base pairs within the coding sequences that actually give rise to proteins.

2) Mutations to cis regulatory regions (CREs). These are short bits of DNA that reside outside of the gene itself, to which proteins attach themselves to regulate gene behaviour. (Other genes code for these proteins.)

3) DNA deletion.

4) DNA duplication.

Generally, researchers think that most morphologic change is due to mutatioins in the CREs. Such changes may have the advantage over changes to the genes themselves in that they are less likely to be harmful to the hosting organism. Because genes are often interlinked, a change to a gene can interfere with the expression of other genes, leading to physical defects. However, that is not always the case and as this paper shows, these (pleiotropic) interactions may have played a major role in the dinosaur to bird tail transition. Why CRE evolution may be potentially less damaging than gene evolution is explained in the box here.

However, researchers don’t have dinosaur DNA and so the problem is to be able to establish the likely mutational cause(s) of this transition.

The authors explain why the “evo/devo” approach is a good way to tackle the problem. Through evo/devo scientists can examine the pathways that underpin tail development and compare these pathways for differing organisms, in the process examining the candidate genes and their mutations that give rise to various morphological traits, and comparing traits with what is seen in the fossil record.

For this study the genetics of the mouse was focused on. The reason for this is that so much is known about mouse genetics in comparison to other relevant organisms. The mouse is used as a proxy for humans in many medical studies. Hence a lot is known about its genetics including the outcomes of mutations to its genes. Besides, as mentioned previously, the genetic program underpinning mouse and bird tails is the same program in broad detail, and it originated well before the time of the dinosaurs.

Although much of these data come from gene knockout studies, (which are not the same kind of studies as are those in which DNA is mutated to see what results), a lot of other data also come from the results of chemical, radiation and spontaneous mutation research.

No matter what the source of mutation, the point is that this large dataset exists from which researchers can begin to discern plausible genetic changes behind the dinosaur to bird tail transition.

In the next post we look at some of these mouse data.





To be continued ...

[rwatts]

MUTATIONS THAT CAUSE TAIL TRUNCATION: Morphological analysis of mouse mutants


So the researchers trawled the databases and the literature for a list of mouse mutants (see my reference 1). They found a number of interesting things that bear on the question of the tail transition:-



1) Given all the mutations examined, only a very small number actually increased tail length.

2) Tail truncation however, seems very easy to achieve, which makes sense from the discussion above.

They offer the scenario that decoupling hind-leg retraction from the tail, left the tail free to evolve in new directions. “Purifying selection” is the term used for the selective removal of alleles or mutations or variations that are deleterious, and the authors propose that this decoupling, relaxed the action of purifying selection on the tail. Presumably it no longer had this dual function to serve (of being a tail as well as offering support for hind leg retraction muscles) and so the genes that grew the tail could tolerate more deleterious mutations than would otherwise have been the case. They cited some recent research in support of this (see my reference 2 below).


To correlate the mouse mutant tail data with dinosaur/bird tails from the fossil record, and tails of extant birds, the researchers drew up a set of parameters and looked at mutations affecting these. Bird tails are notable for:-

1) having a reduced number of caudal vertebrae,

2) having each vertebrae being relatively smaller in size, and

3) having the most distant vertebrae being fused into the pygostyle.

But there is more:-

4) Bone fusion is a characteristic of modern birds (the synsacrum, vertebrae just forward of the synsacrum, in the rear limbs, and in the ribs, particularly as “cross bridges” called ”uncinate processes”

Between 150 and 120 million years ago, these traits of modern birds were to be found in some of the primitive birds as well as in dinosaur lineages closely related to these birds.

From their database trawling, the authors note that the mutations that affected the mouse tail, also affected other characteristics. That is, pleiotropy was involved. Table 1 in the link at the OP is a useful reference. Therefore they wanted to know if there were any other new morphological traits that could be associated with vertebrae tail reductions in the mouse, brought on by mutations. And importantly they wanted to know if any similar kinds of associations could be seen in the fossil record.

And they found them:-

Among the mouse mutants with decreased numbers of caudal vertebrae (n = 105), it was interesting to note that 34% (36/105) also displayed vertebral fusions (including fusions of neural arches, articular surfaces/zygopophyses, transverse processes, spinous processes, or vertebral bodies). Of the 36 with vertebral fusions, 53% had fused ribs. Of all mutants with decreased numbers of caudal vertebrae, only three also had digit fusion, which does not constitute a significant degree of co-segregation but indicates that digit fusion is also possible with truncated tail mutations.

Then because primitive birds in the fossil record as well as modern birds showed both fused vertebrae and truncated tails, the scientists asked an opposing question. They asked about the chances of mouse mutants being found where tail vertebrae fusion was also associated with a reduction in the number of tail vertebrae.

Again, they found it:-

Seventeen of 23 caudal vertebral body fusion mutants, or 74%, also had truncated tails (Table 1). A high percentage of caudal vertebral body fusion mutants (48%) also displayed fused ribs.

Their conclusion is that if a mouse had vertebrae fusion in the tail then there was an even or near even chance that it also had fused ribs and a truncated tail.

Given that there is a reasonably high correlation of vertebrae fusion, rib fusion and tail truncation in mouse mutants, the researchers turned to the fossil record to see if the same associations could be found there. They looked at the dinosaur lineage closely related to that which gave rise to the birds, the non-avian maniraptorans, as well as the primitive long-tailed birds and short tailed birds. What they found is neatly diagramed on the left side of figure 3 in the link at the OP.

They cite this article:-

Insight into the evolution of avian flight from a new clade of Early Cretaceous ornithurines from China and the morphology of Yixianornis grabaui

- as part of their evidence to show what is seen in the fossil record. To quote a snippet:-

The complete vertebral series is preserved in articulation with the exception of several anterior caudal vertebrae (Fig. 2). Twenty-two presacral vertebrae are present. The atlas is preserved in articulation with the odontoid process of the axis (Fig. 3). Twelve vertebrae are anterior to the first with an associated elongate free rib. Transverse foramina partially enclosed by fused ribs are best exposed in the third to seventh vertebrae. Mid-series cervical vertebrae have well-arched post-zygopophyses. The centra of the twelfth vertebra is short and has a blade-like hypapophysis similar to that developed on the eleventh, whereas a more diminutive hypapophysis is developed on the tenth. Evaluation of cervical centra articulations across Avialae is problematic (Clarke, 2004). It appears that whereas some anterior cervical vertebrae may have a degree of heterocoely or ‘incipient’ heterocoely, the posterior cervicals are best described as completely amphyplatous.

Large lateral excavations are present in presacral vertebrae 11–22 as well as in the first sacral vertebra, although these are not as deep as in some other basal ornithurine taxa (e.g. Ichthyornis dispar; Clarke, 2004; Fig. 4). The estimated ten thoracic vertebrae have centra that are longer than wide with articular surfaces that are amphyplatous. Their parapophyseal facets are located near the anterior margin of these centra. There are nine sacral vertebrae (Fig. 5). The ankylosed sacral vertebrae and their costal processes are approximately of the same length and evenly spaced, respectively; the vertebrae in the middle of the series are not abbreviated anteroposteriorly (see character commentary in Clarke, 2004; Fig. 5). Five free caudal vertebrae are inferred to comprise the poorly preserved series. Four vertebrae are visibly incorporated into the short ploughshare-shaped pygostyle; their centra are fused, but portions of the neural spines remain distinguishable (Fig. 5).

- and later:-





Proximally, metacarpals I, II and III are fused to each other and to the semilunate carpal (Fig. 7). There is no sign of an unincorporated third free carpal as is present in more basal taxa; it is inferred that this carpal has been fused in formation of the carpometacarpus.

They note that this kind of thing, the co-segregation of short tails and a pygostyle applies to a wide range of non-avian maniraptorans and primitive birds. For more examples, return to figure 3 at the link in the OP and look to the bottom lefthand side, the black lines. For example here is Sapeornis.

They argue that much of this tail transition could have been down to a single mutation which had multiple genetic effects. An example of pleiotropy in other words. They are not arguing that the same mutation(s) occurred in all cases, given that the mouse model shows that different mutations can have similar or the same effects. So different mutations may have been at play in what is seen in the fossil record. Furthermore, in defence of the multiple mutation scenario, the scientists point out that not all dinosaurs with a pygostyle had a short tail, offering Beipiaosaurus as an example (see reference 3).

They discuss the short tail correlation in mice, with fused ribs. The explanation for this association is that because vertebral ribs also arise from somites, mutations that affect the somites affect the ribs, just as they can the tail. They speculate that if rib fusion is correlated in reality with tail vertebrae fusion mutations, then these rib fusions may have played a role in widening the ilium (synsacrum) by fusing at the point where the ribs attach to the axial skeleton. And they may have played a role in increasing the breadth of the sternum. They cite experiments done with mice showing just this kind of thing. See reference 4, in particular figure 1.



(It’s important to note with regard to reference 4, figure 1, that the experiments on which the figure is based, are gene knockout experiments. You will note that the results often give very asymmetrical, distorted skeletons. Gene mutations are not the same as gene knockouts and presumably in reality, mutations would give rise to skeleton changes that are not asymmetrically distorted.)

The authors also speculate that rib branching, seen in some mutant mice, could have given rise to the bird uncinate processes. They count this as unlikely however, but do note that the fusion of the uncinate process to the ribs may well be associated with tail mutations.



In summary, their understanding of mutational changes to mice tails appears to be reflected in the fossil record at the time of the dinosaur to bird transition.



Next they investigate mouse mutants more closely.


To be continued ...






References



Often, by Googling the titles, you can find the original article, even if the article in its associated journal remains behind a pay-wall. It’s always worth a try.

Any numbers to the left are the numbers supplied by the paper. Thus, 131 at the first reference below is that provided in the paper.

1) 131. Eppig JT, Blake JA, Bult CJ, Kadin JA, Richardson JE: The Mouse Genome Database Group. 2012. The Mouse Genome Database (MGD): comprehensive resource for genetics and genomics of the laboratory mouse. Nucleic Acids Res 2012, 40:D881–D886.


2) 132. Hunt BG, Ometto L, Wurm Y, Shoemaker D, Yi SV, Keller L, Goodisman MA:
Relaxed selection is a precursor to the evolution of phenotypic plasticity. Proc Natl Acad Sci U S A 2011, 108:15936–15941.



If you Google the title you should be able to find the original article.



3) 134. Xu X, Tang Z-L, Wang X-L: A therizinosaurid dinosaur with integumentary structures from China. Nature 1999, 399:350–354.

4) 139. Plummer NW, Spicher K, Malphurs J, Akiyama H, Abramowitz J, Nurnberg B, Birnbaumer L: Development of the mammalian axial skeleton requires signaling through the Galpha(i) subfamily of heterotrimeric G proteins. Proc Natl Acad Sci U S A 2012, 109:21366–21371.



If you Google the title you should be able to locate the PNAS article in full.

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MUTATIONS THAT CAUSE TAIL TRUNCATION: Genetic analysis of mouse mutants

In this section, the researchers briefly describe the link between the results of their trawling of the mouse mutational databases and the previous discussions on how tails grow and what causes their growth to stop.

Table 1 in the link at the OP is the main reference here, as is their Additional file 3.

Table 1 lists 23 mutations, and most of these affect the pathways which are important in tail growth and growth termination and which were discussed in the previous sections:-

1) 10 involve Notch or Notch/Wnt signalling.

2) 7 involve Wnt signaling probably independent of Notch.

3) 2 are associated with BMP/Shh cascades.

4) 1 is involved in Hox signalling.

5) 1 is involved in RA signalling.

These mutated genes have developmental roles associated with aspects of tail growth, such as the formation of somites, the genesis of the neural tube and notochord, patterning and so on. And of those associated with Notch (10 of them), most had roles in somite segmentation or somite differentiation.

The authors specially note that, with respect to the chick, several genes that are equivalent to the mouse genes involved in these pathways, actually down regulate as somite formation slows while their equivalent mouse genes maintain their up regulated state, because tail growth continues. They write:-





It is intriguing to note that in the chick, the Notch pathway members Lnfg, Nrarp, and Meso (the chick homolog of Mesp2), are all downregulated as somitogenesis slows [42], at an equivalent point at which the mouse tail would still be actively extending.

And they emphasize the tolerance for many of these mutations, as well as the pleiotropy involved:-



Interestingly, several mutations among members of this particular pathway, including Dll3, Hes7, Lnfg, Lrp6 [142], Mesp2, and Tbx6, are reasonably well tolerated and cause spondylocostal dystosis (SCD) disease in humans [3]. Individuals suffering from this disease display fused ribs and vertebrae with unaffected reproductive capacity, as in the mouse mutants.

The reader is forced to continually think of the link between these genetic studies and the dinosaur/bird transition, because patterns continually reoccur and the evidence is clear, the same genetic program that underpins bird and mouse tail formation, also underpinned dinosaur tail formation.

Thus a very short section concludes.

Next they turn their attention back to the bird and discuss experimental manipulations and one spontaneous mutation that affects chick tail morphology.



To be continued ...



[rwatts]

MUTATIONS THAT CAUSE TAIL TRUNCATION:Experimental manipulations and one spontaneous mutation that affects chick tail morphology.


The scientists point out that, as with other vertebrates, chick tails have been a neglected area of research - in comparison to the mouse presumably. The reason for this is, as I’ve stated before, the mouse is a model organism, often used as a proxy for humans. And so, relatively speaking, an awful lot is known about it.

However, some research on chick tails has been done and it is revealing in the context of the paper’s topic.

For example, when retinoic acid (RA) is injected into the chick embryonic tail bud in places it is not normally expressed, tail truncation occurs, as well as enhanced “neural differentiation”. By this it is meant that premature additional neural tube and notochord tissues were seen, something that also happens in mice that are similarly treated, and something that is seen in a Chilean chicken called the “Araucana”, which is rumpless or tailless.

And to the best of their knowledge, no mutations have been done which actually increased the length of the chicken tail by increasing the number of somites/vertebrae. To date, studies that have attempted to do this, have achieved nothing. This is consistent with the fact that in the mouse model, tail lengthening is the least likely outcome of mutations affecting tail growth genetic pathways.

There is one known spontaneous mutation that truncates the bird axial skeleton. This is to a gene known as the Iroquois - Irx1 and Irx2. And this happens in the Araucana, mentioned just above. These two genes are tied to Notch, Wnt and BMP/Shh signaling which we have seen mentioned a lot in the previous posts, pathways which influence tail growth and tail truncation.



Figure 8 in the link at the OP is of relevance here. Again, the figure is at the end of the paper while the caption is in the section itself.



They also note with the rumpless chicken, that if either one of the Iroquois genes has different versions (because of mutation, with one version from the female and one from the male) then two to four caudal vertebrae are “irregularly fused”, making this another mutation that causes both short tails and fused vertebrae. However, the most distant vertebrae never form and so the pygostyle is missing.



So there seem to be intriguing similarities between the mouse and the chick although the authors offer the following caveat:-

While there is no equivalent gain-of- function mouse mutant, loss-of-function mutations in either Irx1 or Irx2 in the mouse do not cause posterior truncation or fused vertebrae, emphasizing an important caveat with this study that mutation of the same genes can be manifested differently depending on the nature of the mutation.



Thus, even though the same genetic program underlies mouse and bird (and dinosaur) tail development, there are differences between species, often because different genes within the different species play the same roles.

Tail truncation they note, is not necessarily a rare thing in chick populations:-





It was previously estimated that among a variety of normal-tailed chicken breeds, a tailless phenotype was consistently observed in approximately one out of every thousand chicks hatched, ...

From this the authors conclude:-





Well-tolerated, relatively common tail truncating mutations (especially if dominant and germ-line) that conferred certain advantages would theoretically promulgate the evolutionary transition from long- to short-tailed birds.




In the next section the scientists offer some additional considerations to the scenario they think the above evidence points to.







To be continued ....




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MUTATIONS THAT CAUSE TAIL TRUNCATION: Additional considerations.


In this section the authors explore the possibility of a mutation reversing itself, if it was a single mutation that triggered the morphological change to short tails. If this could happen fairly easily then one could expect to find evidence of a reversal in the fossil record. But there is no evidence of this.



They discount the likelihood of reversal for several reasons. Quoting them:-

1) “Indirect mutations that would re-activate a particular pathway are possible but also unlikely, considering the mutation(s) would have to reintroduce the fine balance of factors required for axial extension without being detrimental. 

In essence, the mutations that brought about short tails also brought about a continuous balance in morphology that allowed the dinosaur/bird to keep flying efficiently. It’s unlikely that a reversal would easily maintain this balance."



(It probably needs to be pointed out here, given the switch between the word “mutation” and “mutations” that when they talk of a single mutation that brought about short tails, there can be an implication of other non-tail mutations being in effect, or there can be an implication of other tail mutations being in effect which have no bearing on morphology, until this one mutation came along to change everything about the tail. These kinds of mutations are called “potentiating mutations”).



2) “Dollo's law states that accumulation of mutations over time, especially for those genes whose functions are no longer selected for, can prohibit certain morphological traits from resurfacing [152]. Birds with fully formed teeth, for example, have never been observed in modern times because the genes for enamel, no longer selected for, were inactivated in the bird genome [153,154].”



This one is perhaps easy to see, particularly in the case of genes that code for a function that has become somewhat useless. These is no selection acting to keep the genes from decaying by the accumulation of mutations.



A link to the online version of their reference 152 can be found here - Dollo's law and the death and resurrection of genes. And please note that what is in disucssion here is “substantively reversible” as opposed to “impossible to reverse”.



3) “Third, since long tails hinder flight, and flight mechanics evolved primarily with short tails [36], reintroduction of long tails would have likely impeded survival.”



4) “Lastly, traits that influence sexual selection cannot be underestimated. The appearance of the pygostyle, possibly with the fan-shaped array of mobile tail feathers, may have indelibly affected mate choice among birds, which would have ensured the persistence of the pygostyle phenotype”.



There is a body of research around showing that the formation of novel traits can really influence mate selection in a positive way. For example with humans, if everyone is clean shaven and a male grows a beard, then he can make himself stand out. On the other hand, if every male has beards, then a male who decides to cut it all off, likewise makes himself stand out. Similar effects are seen with other organisms.




A couple of points raised above with respect to the mechanics of flight when tails go from short to long, obviously bear on the opposite problem, going from long to short. There is some research that addresses part of this question at least. The reduction in mass of that caudofemoralis muscle connecting the hind leg to the anterior part of the tail, and loss of the long tail itself would have shifted the animal's center of mass forward. However, there is an argument that the loss of the caudofemoralis muscle would not have prevented the associated organism from being a very efficient runner - see my reference 1. And the forward shift in the center of mass seemingly assists in flight - see reference 2.



In the sect section, the authors bring the paper to a conclusion.






To be continued ....






References



Often, by Googling the titles, you can find the original article, even if the article in its associated journal remains behind a pay-wall. It’s always worth a try.

Any numbers to the left are the numbers supplied by the paper. Thus, 131 at the first reference below is that provided in the paper.

1) 155. Hutchinson JR: Biomechanical modeling and sensitivity analysis of bipedal running ability. I. Extant taxa. J Morphol 2004, 262:421–440.

2) 30. Gatesy SM, Dial KP: Locomotor modules and the evolution of avian flight. Evolution 1996, 50:331–340.







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CONCLUSIONS

In their conclusion, the researchers pull it all together.

They begin by pointing out the obvious - that, at this time, we have no way of knowing exactly what or how many mutations were involved in this transition. Nor do we know the true basal dinosaur in which this transition began.

Nevertheless, despite all the caveats this kind of research presents, it does indicate possibilities. It shows that plausibly, a single mutation in a paravian dinosaur may have been involved in the major part of the transition, namely the shortening of the tail and the development of the pygostyle. Paravian dinosaurs are those more closely related to birds than to oviraptorosaurs.

Even though multiple mutations may have been involved in reality, in support of their single mutation hypothesis, the authors note that:-

...of the 37 posterior vertebral body-fusion mutants we examined [see Additional file 3], all but four are known to be caused by single mutational events, and have substantial phenotypic alterations not just to the tail, but to other parts of the skeleton as well.

These mouse mutations though, were to regions within genes. As mentioned a while ago, mutations can occur to regulatory regions, regions that control genes and evidence is that mutations here:-



...would likely have resulted in fewer pleiotropic effects in both mice and early birds.

That is, these kinds of mutations would have likely been less severe to the hosting organism, with the associated possibility of multiple mutations in fact being the reality.

Yet, pleiotropic effects, whether or not single or multiple mutation events were involved, remain to be considered for a couple of reasons. What is seen in the mouse model, mirrors what is seen in the fossil record. Additional alterations which include non tail fusions to vertebrae, even fusions to ribs and perhaps digits, are seen at the same time as the tail transformation. Thus pleiotropic effects may well account for the relatively sudden appearance of short tailed birds.

The authors note that:-





If a vertebral fusion mutation occurred in a primitive bird like Jeholornis, which fused additional vertebrae in its synsacrum, truncated its tail, and fused some ribs, the resulting creature would have come a long way towards resembling Confuciusornis.

While both birds were contemporaneous, and the former had flight structures very similar to the latter, Jeholornis differed markedly from Confuciusornis in the latter part of its body.

The scientists reason that once the “jump” had been made, the associated genes would have been fixed thanks to the advantages this conferred on flight and sexual selection.

Based on this research of the mouse tail and the consequences of mutations to its underlying genetic program, they offer the conjecture that genes involved in axial extension of the tail were the ones key to the transition from dinosaur long tail to modern bird short tail. What genes were likely the key ones? Again, based on the mouse model:-





most mutations causing distally fused caudal vertebrae and shortened tails lie in the Notch/Wnt pathway, in somite segmentation, differentiation or somite boundary formation.

Clearly the research described here is just a beginning. So much more will be learnt about the embryonic growth of organisms including the exact genes involved and how these all relate to each other. Each new advance in this understanding will open up the kind of reasearch described here, and offer more chances of testing their idea. The authors conclude:-





Future comparative studies of signaling cascades between birds, long-tailed reptiles and mice should help to uncover these long-lost mutations, and further our understanding of the evolution of birds from non-avian maniraptoran dinosaurs.

Thus ends the major part of this essay.




In my next post I’ll offer some of my own concluding remarks.





Final post next ....

[rwatts]

THE END AND SOME OF MY THOUGHTS


We now come to the end of this set of posts with some of my own thoughts.

In science, theories about things and about processes have two components. The first is evidence that the thing or the process actually exists. The second is understanding what the thing is made of and how it works. Thus, with the atomic theory of matter there is the body of evidence for the existence of the atom. Then there is the body of evidence describing what atoms are and how they work. It’s the same with evolution. There is the body of evidence for the reality of the process, and there is the evidence for how the process works.

The research which this set of essays describes, falls into the second category - understanding how the process works.

In this case, the researchers relied on the evidence showing that the same genetic program underpins the development of the bird, mouse and dinosaur tail. It’s just that the specifics of the program changes between the various species. Because of this, and given that so much is known about how mutations to mouse genes affects embryonic tail growth, the researchers were able to use these data in an attempt to understand what happened long ago to cause the long tail of the dinosaur to transition to the short tail of the bird. This putative understanding was possible in part because many of the physical effects seen in the mouse mutants could also be seen in the fossil record, allowing the researchers to propose the kinds of mutations that may have underlaid that ancient transition.

Of course, as they point out, their argument cannot be showing exactly what did happen. But it is showing what could have happened. Nevertheless, it’s clear from reading the paper that a lot more research can be done with regards to this question to pin down with more certainty, the kinds of genes which underlaid the transition. The problem for the moment is that this research remains to be done. Accordingly, as the genetics and tail developmental programs of other different organisms becomes understood (for example, birds and reptiles), so future researchers will return to this problem and throw more light onto the question of what happened to bring about the unique short bird tail from the long dinosaur tail.

The kind of testing described in the paper is just one of may different ways of testing evolution. A few of the other ways are as follows:-

Lenski’s long term evolution experiment - letting bacteria evolve in the lab over decades:-

Genomic Analysis of a Key Innovation in an Experimental E. coli Population
http://europepmc.org/articles/PMC3461117/reload=0;jsessionid=lkRVnOHQFNsZzL1B6qio.40


Thornton’s ancient protein reconstruction experiments:-

Structural analysis of the evolution of steroid specificity in the mineralocorticoid and glucocorticoid receptors
http://www.biomedcentral.com/1471-2148/7/24


Fiddling with developmental programs to see if fossil record observations can be recovered:-
Replaying evolutionary transitions from the dental fossil record


Undertaking a large comparison of homologous molecules between organisms of various degrees of relatedness:-
The Evolution of Respiratory Chain Complex I from a Smaller Last Common Ancestor Consisting of 11 Protein Subunits
http://link.springer.com/article/10.1007/s00239-011-9447-2#page-1


Using mutation data to model the step by step process in an evolutionary transition:-
Evolutionary Potential of a Duplicated Repressor-Operator Pair: Simulating Pathways Using Mutation Data
http://www.ploscompbiol.org/article/info%3Adoi%2F10.1371%2Fjournal.pcbi.0020058




Anyway, here endeth a very long essay. 




Not to be continued.

[rwatts]

A DIFFERENT KIND OF TEST - teeth and replaying evolution.

In a very recent issue of Nature is the following paper:-

Replaying evolutionary transitions from the dental fossil record

It’s a more direct kind of test than the one described above and this time it has to do with teeth.

Teeth are very complex things it seems. I’d heard that scientists can pick up a tooth and tell you the kind of animal it belongs to, down to the level of species (I think). That was always a bit hard to understand, until I began reading the article. Then I understood why this could be so. Teeth really do have an awful lot of variation - big cusps, little cusps, and ridges connecting them. While the large cusps tend to remain stable at higher taxonomic classifications, the smaller cusps can vary a lot. Then there are ridges that may or may not connect the cusps. And there are stepped teeth, as well as other bumps and holes, all of which produce this diversity.

In the above paper, scientists have been able to show how the tweaking of just one or two genes produces a lot of this variation and in the process can replay some of the important evolutionary transitions as seen in the fossil record.



I was reading the paper in an attempt to understand it, so that I could describe it to you. However, better still, I found the layperson’s writeup on line. It does a much better job than I could do. Here it is:-



Tooth structure re-engineered



Enjoy.

But if you tackle the main paper, have Google handy. You might need it.

[rwatts]

A very different paper. This is about the wrist, as opposed to the tail. Hot off the press. Well very recent, put it that way.


New Developmental Evidence Clarifies the Evolution of Wrist Bones in the Dinosaur–Bird Transition

From early dinosaurs with as many as nine wrist bones, modern birds evolved to develop only four ossifications. Their identity is uncertain, with different labels used in palaeontology and developmental biology. We examined embryos of several species and studied chicken embryos in detail through a new technique allowing whole-mount immunofluorescence of the embryonic cartilaginous skeleton. Beyond previous controversy, we establish that the proximal–anterior ossification develops from a composite radiale+intermedium cartilage, consistent with fusion of radiale and intermedium observed in some theropod dinosaurs. Despite previous claims that the development of the distal–anterior ossification does not support the dinosaur–bird link, we found its embryonic precursor shows two distinct regions of both collagen type II and collagen type IX expression, resembling the composite semilunate bone of bird-like dinosaurs (distal carpal 1+distal carpal 2). The distal–posterior ossification develops from a cartilage referred to as “element x,” but its position corresponds to distal carpal 3. The proximal–posterior ossification is perhaps most controversial: It is labelled as the ulnare in palaeontology, but we confirm the embryonic ulnare is lost during development. Re-examination of the fossil evidence reveals the ulnare was actually absent in bird-like dinosaurs. We confirm the proximal–posterior bone is a pisiform in terms of embryonic position and its development as a sesamoid associated to a tendon. However, the pisiform is absent in bird-like dinosaurs, which are known from several articulated specimens. The combined data provide compelling evidence of a remarkable evolutionary reversal: A large, ossified pisiform re-evolved in the lineage leading to birds, after a period in which it was either absent, nonossified, or very small, consistently escaping fossil preservation. The bird wrist provides a modern example of how developmental and paleontological data illuminate each other. Based on all available data, we introduce a new nomenclature for bird wrist ossifications.

Yes, different labeling does make it very confusing.

Thanks to poster “teeth” at TR for bringing this to our attention.