The Circuit of Love
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Ontogenesis versus Phylogenesis

Introduction:

It always have been said that Ontogeny is reminiscent of Phylogeny. It means every evolutionary change that is occurred in the ancestors of each organism, will repeat in its development. Yet, I think it would be not necessary at all. In fact some morphological changes in phylogenetic evolution will cause completely different developmental occurrence, when they become to repeat in phenotypic evolution. I want to show you an exempli gratia.

In most of the living creatures (with the exception of Homo that evolve more mimetically than genetically) the material that changes through evolution is genome, itself. But it is not in direct connection with the environment. The phenotype is just external apparition of the genome, and as the part in contraction with the environment, it will be shaped, to fit with the multidimensional outer space. When we want to count the evolutionary steps that formed a taxon, we can choose one of these two; genotype or phenotype, and usually each one of them will lead in a different consequences. The main problem is variance between the changes that happened in past evolutionary history of each one of them. May be a single phenotypic differentiation, in response to a simple environmental change, occurred after a couple of changes in many genes, and may be change in a single gene, will effect on the different parts of the phenotype. In fact, the only thing, that its changes (if we can count these changes) would fit the virtual evolutionary events, is the connection between genotype and phenotype, that we call it "development". So, till the time that we could relate genotype and phenotype via developmental biology, we can't have a good sight to the nature of the evolutionary changes. Here you can see how morphology shows just a simple reduction in the digital formulae of the line leading from primitive five digited dinosaurs to the highly derived three digited neotetanurans (Neotetanura is a clade containing the most recent common ancestor of Allosaurus and Neornithes and all of its descendants), yet development of avian mani, reveals a more complicated history. Result of the controversy between the morphological data obtained from paleontological evidence, and developmental data, caused a hesitation in illo tempore sed in fine we found that it's just an example of the mentioned difference. In fact the critics by fans of non-dinosaurian origin of birds caused a great step to forward in comprehension of evolutionary mechanisms that lead the dinosaurs to become birds. In dubio pro reo!

Slide descriptions:

I, Title;

II, a cladogram of the Dinosauria, showing Ornithischia in the left side and Saurischia in the right, including Aves (birds); Scale: 20 synapomorphies;

III, a cladogram of the Suarischia, showing the position of Aves amongst them; Scale: 20 syanpomorphies;

IV, Euparkeria, a primitive archosaur, very close to common ancestor of Birds and Crocodiles;

V, Herrerasaurus, a primitive dinosaur, probably one of the most primitive members of Theropoda, this dinosaur had vestigial digits IV and V;

VI, Allosaurus, a primitive member of Tetanura, a clade of theropoda which reduced the number of fingers to three;

VII, Tyrannosaurs, a primitive member of coelurosauria, a clade of tetanurans which began a trend of dwarfism that ends to the birds, Tyrannosaurus belongs to a branch of Coelurosauria which evolved from small 1-2 meters long ancestors in Upper Jurassic but secondarily produced large scale giants in Upper Cretaceous; during this trend, the manus reduced to a small vestix with only two fingers;

VIII, Gallimimus, another primitive member of the clade coelurosauria with more bird like appearance, but probably the previous one –Tyrannosaurs- was closer to birds than this one;

IX, Compsognathus, another primitive member of the clade coelurosauria;

X, Sinornithoides, a highly derived coelurosaur, very close to ancestry of birds;

XI, Archaeopteryx, which is taxonomically the most primitive bird; note that the term "most primitive" is just taxonomical, and means that the Taxon Aves (=Avialae) diagnosed so: "The most recent common ancestor of Archaeopteryx and Neornithes and all of its descendants", so Archaeopteryx would be the most primitive member of the taxon, yet it is more derived than the previous mentioned dinosaurs;

XII, Mononychus, probably a primitive bird, which is placed in the next step after Archaeopteryx; yet it's dubious if this dinosaur is a bird at all or just a primitive coelurosaur, very close to already mentioned Gallimimus; the important thing about Mononychus is its highly reduced manus, with just one digit (plus metacarpi of two other lost digits);

XIII, Caudipteryx, was one of the first feathered dinosaurs have been found, probably more primitive than even Sinornithoides; yet its avian status is also mentioned;

XIV, Cathayornis, a highly derived bird, with more bird like appearance than primitive Archaeopteryx;

XV, a cladogram of theropod evolution to the line of birds, highlighting the most important characters those are now diagnostics of birds; note to the characters at the node 2, three fingered hand with semilunate carpal; sensu this cladogram, this character of avian manus would be evolved at the Lower to Middle Jurassic (50-30 milla anus before rise of birds) for first time in the neotetanurans like Allosaurus;

XVI, cladogram showing evolution of dinosaurian Mani, in relation with their posture, gate and weight; note to the clade theropoda and their highly derived three fingered hands (mani 9-13) that is evolved from ancestral five fingered hands (manus 7) those lost their digits number DIV and DV (manus 8);

XVII, mature pigeon (Columba)'s dissected manus;

XVIII, Mani and Metacarpi of Herrerasaurus, Coelophysis, Allosaurus, Velociraptor, Archaeopteryx, and Columba; note to the losing digits number DIV and DV and fixed three fingered mani of Allosaurus and later genera;

XIX, three fingered hands of a derived non-avian theropod, Archaeopteryx, and a living neognathaean bird; note that sensu these five last slides the three fingered mani of Aves is composed of DI, DII, and DIII;

XX, development of Mani of a crocodilian (as the closest living relative of the birds), a chicken, and a turtle; note that the first digit which is appeared in the five fingered Mani of alligator and turtle is DIV, so the first one in the avian manus is also DIV, that means the three fingered manus of chicken is composed of DII, DIII, and DIV;

XXI, A: Diagrammatic illustration of developing turtle limb bud to show general topography (R, radius, U, ulna, u, ulnare, I, intermedium, 4, carpal four, and digits III–V, 3–5). The primary axis therefore is highly conserved developmentally and invariably identifies digit IV, 4. B-D: developing limb buds in (B) turtle, (C) bird and (D) alligator. Respectively, illustrating the conserved developmental pattern of the primary (metapterygial) axis;

XXII, Definitive paired anterior fin and limb skeleton patterns in (A) the teleost zebra fish (Danio) with only endoskeletal radials shown; (B) a dipnoan, Neoceratodus ; (C) the osteolepiform, Eusthenopteron; (D) the Panderichthyid, Panderichthys (tetrapod sister group); (E) a generalised pentadactyl limb showing the Shubin-Alberch developmental skeletal bauplan. The hypothetical metapterygial axis is marked for A-D (doubtful for teleosts, A). In (E), it runs postaxially supposedly continuing as the digital arch, da. P, posterior;

XXIII, Patterns of connectivity among condrogenic condensations; CI-V, Condensations; *, metapterygial axis; a, alligator; b, ostrich;

XXIV, development of chicken manus and pes; note that the primary axis in the pes of the chicken is also toe IV, just like manus;

XXV, development of chicken manus, with line drawing showing the details of developmental stages;

XXVI, development of ostrich manus and pes; with the same basic pattern as the chicken shows; note that in ostrich, at least in one stage we can see the pentadactyl structure of autopodium, which manus loses the DI and DV to conserve DII-IV and become tridactyl manus;

XXVII, The pentadactyl hand of a 14(–15) day old ostrich (A), showing the anlagen for digits I, ‘‘thumb’’ (left) and V (right), compared to the hands of various dinosaurs illustrating the reduction of digits IV and V (disappearance of V in E). (B) Herrerasaurus (putative basal theropod, late Triassic); (C) Lesothosaurus (basal ornithischian, late Triassic); (D) Plateosaurus (basal sauropodomorph, late Triassic); (E) Syntarsus/Coelophysis (theropods, late Triassic); (F) Hypsilophodon (ornithopod, early Cretaceous); note that the phylogenetic way of evolution of tridactyl avian manus sensu these examples is losing DIV and DV, yet the ontogenetic way of development of tridactyl avian manus sensu the last eight slides is losing DI and DV; where the ontogeny is in controversy with phylogeny!

XXVIII, Late embryos of (a) Hoatzin (Opisthocomus: Neognathae); and (b,c) Kiwi (Apteyx: Palaeognathae); DI-III, digits; CII-IV, Condensations; MCI-III, Metacarpals; note that the first digit in the manus of Hoatzin is just like the first manus of more primitive theropods, and it seems that it's the first digit, developed from condrogenic condensation number CII;

XXIX, We hypothesize a frame shift that forces CII in to the developmental trajectory of Digit DI, CIII into Digit DII and CIV into Digit DIII. This frame-shift is probably appeared in the first tetanurans with fixed tridactyl mani;

XXX et XXXI, The sequence of growth of a tetrapod limb bud, reading from top to bottom, showing how stylopod (humerus, femur), zeugopod (forearm, shin), and autopod (hand, foot) differentiate. The pattern is determined by turning on (filed squares) and off (open squares) of Hox genes D-9 to D-13. The identity of developing digits is at first unspecified, despite their positions and digits acquire their ossified characteristics upon interaction with gradients of bone morphogenetic proteins;

XXXII, a possible model is provided by the recent discovery that the boundary between cervical and thoracic vertebrae is controlled by Hox genes which may be manipulated to switch the boundary. (Gallis, 2001); Work by Drossopoulou et al., 2000 demonstrated the dissociation of digit number from identity. The gene Shh plays a role in the first and Bmp level in the second.

XXXIII et XXXIV et XXXV, Frame-Shift, is just like regaining of a lost organ; Is there any other example in the history of life? Ichthyostega, one of the most primitive tetrapods, with 7-8 toes; then, in the common ancestor of amniotes, the number of digits and toes fixed to 5; yet many genera of Ichthyosauria, as a highly derived taxon of amniota show six digits in their secondarily fin formed mani.
It’s just another example!

XXXVI, Thank you for your attention!

Discussion:

During the Jurassic period, a branch of flesh eating dinosaurs began a trend of dwarfism, because of probable geographic isolation in the small islands of an archipelago spreading in the Eurasia. Before the end of the Jurassic, they become cosmopolitan yet conserved their ecological niches and with a few exceptions (e.g. Tyrannosauridae, Therizinosauridae, etc.) they remain dwarf. Archaeopteryx was a usual member of them, but finally, in the mass extinction of the K-T boundary, those were relatives of Archaeopteryx which passed to Cenozoic Era. Now, we call these highly derived theropod dinosaurs with the common name Birds. Birds are dinosaurs –ergo reptiles­-, as the human is mammal.

In the last decade, we found many fossils of feathered theropod, most of them more primitive than Archaeopteryx. So, we found that many features of birds, including their plumage was already present in their non-flying, non-avian ancestors.

But, just one thing remained dubious, here; the controversy of digital development which it shows a different trend than we expect to be. If accept the dinosaurian origin of birds, then they should have digits DI-III in their hands, because their ancestors become tridactyl by losing the DIV and DV. If we accept the embryological evidence of development of avian Mani, then they should be also originated from a hypothetical linage that lost the DI and DV. It's the controversy.

The answer to this problem is so easy! There is a frame-shift in the development of avian Mani. They lose their CI and CV, and conserve CII-IV. Then they develop CII into the DI, CIII into the DII, and CIV into the DIII. Now there is enough developmental data that support the possibility of such a frame-shift. In fact, the morphologic identity of each digit is related to the gradients of bone morphogenetic proteins.

But why such a complex change should be happened? We know that the pollex (DI) has its unique functional advantages. It composed of only two phalanges, and its metacarpal is anterior to other ones. It's the position of pollex in the primates like human. But in the raptorial bipedal dinosaurs, like ancestors of the birds, the pollex had a similar situation. So when they go to become bipedal, the plesiomorphic pentadactyl manus was not necessary and they conserved just the three first ones. The losing of two excessive digits, was because of saving material and energy during the development. But till there was a vestix of DIV and DV and their metacarpi in the Mani of theropod, surely they should produce pentadactyl embryos those stop the growth of their DIV and DV in a vestigial stage. But in the first theropods that had the fixed tridactyl Mani, the mentioned frame-shift helped them to not lose energy for developing the most lateral and smallest condrogenic condensations (CI and CV). Yet the functional advantages of the DI conserved its morphological properties in the digit developed from the second condrogenic condensation. So we should count two evolutionary steps for changing from a theropod with vestigial DIV and DV into a theropod with just fixed true tridactyl manus; one for losing the CI and CV, and one for the frame-shift that happened to develop the same phalangeal formula, from the new precursors.

Conclusion:

Other than the embryological importance of such a frame shift, it shows us, the importance of understanding developmental mechanisms that relate the genotype and phenotype. In fact the evolving material in the process of evolution is neither phenotype nor genotype; it's just the molecular pathways those make an organism's body according to its genome.

Acknowledgement:

This presentation was a part of my homework for the embryology unit. I should thank Dr. Bahman Zeynali for his help, supervision, review and comments on this works.

Important readings:

Burke, A. C. & Feduccia, A. (1997) Developmental Patterns and the Identification of Homologies in the Avian Hand; Science 278, 666-668 Download: 593 Kb

Drossopoulou, G. etal. (2000) A model for anteroposterior patterning of the vertebrate limb based on sequential long- and short-range Shh signaling and Bmp signaling; Development 127, 1337-1348 Download: 273 Kb

Feduccia, A., (1999) 1, 2, 3 = 2, 3, 4: Accommodating the cladogram; Proc. Natl. Acad. Sci. USA 96, 4740–4742 Download: 255 Kb

Feduccia, A. (2002) Birds are dinosaurs: Simple answer to a complex problem; The Auk 119(4):1187–1201 Download: 1,045 Kb

Feduccia, A. & Nowicki, J. (2002) The hands of birds revealed by early ostrich embryos; Naturwissenschaften 89, 391–393 Download: 199 Kb

Galis F. (2001) Digit identity and digit number: indirect support for the descent of birds from theropod dinosaurs; Trends Ecol. Evol. 16, 16 Download: 24 Kb

Hinchliffe, J. R. (2002) Developmental basis of limb evolution; Int. J. Dev. Biol. 46, 835-845 Download: 379 Kb

Magnol, J. P. etal. (2004) L'origine des oiseaux et la question de l'homologie des doigts de leur main: données contradictoires de la Systématique phylogénétique et de la Biologie du développement; Revue Méd. Vét., 155, 3, 187-196 Download: 504 Kb

Mindell, D. P. & Meyer, A. (2001) Homology evolving; Trends Ecol. Evol. 16, 434-440 Download: 66 Kb

Nikbakht, N. & McLachlan, J. C. (1999) Restoring avian wing digits; Proc. R. Soc. Lond. B. 266, 1101-1104 Downoload: 302 Kb

Sereno, P. C. (1997) The origin and evolution of dinosaurs, Annu. Rev. Earth Planet. Sci. 25, 435–489 Download: 551 Kb

Sereno, P. C. (1999) The evolution of dinosaurs; Science 284, 2137-2147 Download: 490 Kb

Wagner, G. P. & Gauthier, J. A. (1999) 1, 2, 3 = 2, 3, 4: A solution to the problem of the homology of the digits in the avian hand; Proc. Natl. Acad. Sci. USA 96, 5111–5116. Download: 416 Kb