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The Origin of Tetrapod Limbs and Girdles: Fossil and Developmental Evidence
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Around 375 million years ago, the first tetrapods appeared, marking one of the most important events in vertebrate evolutionary history. The fin to limb transition saw the appearance of fingers and a weight bearing pelvic girdle. While very little research has been done on the evolution of the tetrapod pelvic girdle, a fair amount has been done on the origins of fingers but some aspects remained controversial. A combination of palaeontology, developmental biology and comparative morphology was therefore used in this thesis to better understand the fin to limb transition. The pectoral fin of Panderichthys, a sarcopterygian fish closely related to tetrapods was CT-scanned and modeled in three dimensions and its pelvic girdle and fin were examined with traditional techniques. This information from the fossil record was integrated with comparisons of the development of the Australian lungfish, Neoceratodus forsteri, our closest living fish relative and the axolotl (Ambystoma mexicanum), a salamander representing well the condition of early tetrapods. Development of bone and cartilage was studied through clearing and staining and development of skeletal muscles through immunostaining. In situ hybridizations were performed on the lungfish to study the expression of Hoxd13, associated with the formation of digits in tetrapods.

This work shows that the late expression phase of Hoxd13 is present in Neoceratodus and is associated with the formation of radials. Redescription of the pectoral fin of Panderichthys reveals that distal radials are present, which, in addition to other information, lead us to conclude that digits are not novelties in tetrapods but rather have evolved from the distal radials present in the fins of all sarcopterygian fish. The earliest tetrapods lack a full set of wrist + carpals/ankle + tarsal bones. Here, we propose that this region of the limbs evolved after fingers and toes through an expansion of the region between the proximal limb bones and the digits. As for the pelvic girdle, it is very primitive in Panderichthys but comparison of its development in Neoceratodus and Ambystoma suggest that the ischium evolved through the posterior expansion of the pubis and the ilium, through an elongation of the iliac process already present in sarcopterygian fishes.

The results of this thesis help to better understand the fin to limb transition and show that it is more gradual than previously believed.

 

Place, publisher, year, pages
Uppsala: Acta Universitatis Upsaliensis, 2009. 53 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 613
National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-98911 (URN)978-91-554-7448-5 (ISBN)oai:DiVA.org:uu-98911 (OAI)diva2:201539 (DiVA)
Public defence
2009-04-09, Lindhalsalen, EBC, Norbyvägen 14, Uppsala, 13:00 (English)
Opponent
Supervisors
Available from2009-03-13 Created:2009-03-04 Last updated:2009-04-03Bibliographically approved
List of papers
1. Fish fingers
Open this publication in new window or tab >>Fish fingers : digit homologues in sarcopterygian fish fins
Show others...
2007 (English)In: Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, ISSN 1552-5007, Vol. 308B, no 6, 757-768Article in journal (Refereed) Published
Abstract [en]

A defining feature of tetrapod evolutionary origins is the transition from fish fins to tetrapod limbs. A major change during this transition is the appearance of the autopod (hands, feet), which comprises two distinct regions, the wrist/ankle and the digits. When the autopod first appeared in Late Devonian fossil tetrapods, it was incomplete: digits evolved before the full complement of wrist/ankle bones. Early tetrapod wrists/ankles, including those with a full complement of bones, also show a sharp pattern discontinuity between proximal elements and distal elements. This suggests the presence of a discontinuity in the proximal-distal sequence of development. Such a discontinuity occurs in living urodeles, where digits form before completion of the wrist/ankle, implying developmental independence of the digits from wrist/ankle elements. We have observed comparable independent development of pectoral fin radials in the lungfish Neoceratodus (Osteichthyes: Sareopterygii), relative to homologues of the tetrapod limb and proximal wrist elements in the main fin axis. Moreover, in the Neoceratodus fin, expression of Hoxd13 closely matches late expression patterns observed in the tetrapod autopod. This evidence suggests that Neoceratodus fin radials and tetrapod digits may be patterned by shared mechanisms distinct from those patterning the proximal fin/limb elements, and in that sense are homologous. The presence of independently developing radials in the distal part of the pectoral (and pelvic) fin may be a general feature of the Sarcopterygii.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-16283 (URN)10.1002/jez.b.21197 (DOI)000251331100006 ()17849442 (PubMedID)
Available from2008-05-19 Created:2008-05-19 Last updated:2010-02-11Bibliographically approved
2.
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3. The humerus of Panderichthys in three dimensions and its significance in the context of the fish-tetrapod transition
Open this publication in new window or tab >>The humerus of Panderichthys in three dimensions and its significance in the context of the fish-tetrapod transition
2009 (English)In: Acta Zoologica (Stockholm), ISSN 0001-7272, E-ISSN 1463-6395, Vol. 90, no suppl 1, 297-305Article in journal (Refereed) Published
Abstract [en]

The humerus of Panderichthyshas been considered to represent a transitionalform between that of tetrapodomorph fish such asEusthenopteronandtetrapods such asAcanthostega. The previous description was based onflattened material and was analysed in the context of the few fossils known atthe time. Since then, several new forms have been described such asGogonasus,Tiktaalikand an isolated humerus from the Catskill Formation. The humeralmorphology ofPanderichthys rhombolepisand its interpretation in this newcontext are therefore reassessed with the help of a three-dimensional modelproduced with themimicssoftware based on a computed tomography scan ofan unflattened specimen as well as comparisons with the originally describedmaterial. The humerus ofPanderichthysdisplays a combination of primitive,derived, intermediate and unique characteristics. It is very similar to themorphology ofTiktaalikbut when it differs from it, it is most often morederived despite the more basal phylogenetic position thatPanderichthysoccupies. What emerges from this study is a much more gradual transformationof the humerus morphology from fish to tetrapods and the ability to distinguishautapomorphies more easily. The picture is more complex than previouslybelieved, with many morphological specializations probably reflecting thebreadth of ecological specializations already present at the time.

Keyword
fish-tetrapod transition, sarcopterygian, humeri, pectoral musculature
National Category
Biological Sciences
Research subject
Pathology
Identifiers
urn:nbn:se:uu:diva-98908 (URN)10.1111/j.1463-6395.2008.00389.x (DOI)000266242000025 ()
Available from2009-03-04 Created:2009-03-04 Last updated:2011-03-11Bibliographically approved
4. The pelvic fin and girdle of Panderichthys and the origin of tetrapod locomotion.
Open this publication in new window or tab >>The pelvic fin and girdle of Panderichthys and the origin of tetrapod locomotion.
2005 (English)In: Nature, ISSN 0028-0836, Vol. 438, no 7071, 1145-1147Article in journal (Refereed) Published
Keyword
palaeontology, vertebrate, sarcopterygian, tetrapod, Devonian, elpistostegid, Panderichthys
National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-80505 (URN)doi:10.1038/nature04119 (DOI)
Available from2006-05-18 Created:2006-05-18 Last updated:2011-01-11
5. Comparative pelvic development of the axolotl (Ambystoma mexicanum) and the Australian lungfish (Neoceratodus forsteri)
Open this publication in new window or tab >>Comparative pelvic development of the axolotl (Ambystoma mexicanum) and the Australian lungfish (Neoceratodus forsteri) : conservation and innovation across the fish-tetrapod transition
2013 (English)In: EvoDevo, ISSN 2041-9139, Vol. 4, 3-Article in journal (Refereed) Published
Abstract [en]

Background: The fish-tetrapod transition was one of the major events in vertebrate evolution and was enabled by many morphological changes. Although the transformation of paired fish fins into tetrapod limbs has been a major topic of study in recent years, both from paleontological and comparative developmental perspectives, the interest has focused almost exclusively on the distal part of the appendage and in particular the origin of digits. Relatively little attention has been paid to the transformation of the pelvic girdle from a small unipartite structure to a large tripartite weight-bearing structure, allowing tetrapods to rely mostly on their hindlimbs for locomotion. In order to understand how the ischium and the ilium evolved and how the acetabulum was reoriented during this transition, growth series of the Australian lungfish Neoceratodus forsteri and the Mexican axolotl Ambystoma mexicanum were cleared and stained for cartilage and bone and immunostained for skeletal muscles. In order to understand the myological developmental data, hypotheses about the homologies of pelvic muscles in adults of Latimeria, Neoceratodus and Necturus were formulated based on descriptions from the literature of the coelacanth (Latimeria), the Australian Lungfish (Neoceratodus) and a salamander (Necturus). Results: In the axolotl and the lungfish, the chondrification of the pelvic girdle starts at the acetabula and progresses anteriorly in the lungfish and anteriorly and posteriorly in the salamander. The ilium develops by extending dorsally to meet and connect to the sacral rib in the axolotl. Homologous muscles develop in the same order with the hypaxial musculature developing first, followed by the deep, then the superficial pelvic musculature. Conclusions: Development of the pelvic endoskeleton and musculature is very similar in Neoceratodus and Ambystoma. If the acetabulum is seen as being a fixed landmark, the evolution of the ischium only required pubic pre-chondrogenic cells to migrate posteriorly. It is hypothesized that the iliac process or ridge present in most tetrapodomorph fish is the precursor to the tetrapod ilium and that its evolution mimicked its development in modern salamanders.

Keyword
Fish-tetrapod transition, Pelvic girdle, Heterochrony, Extant phylogenetic bracketing method, Evolutionary novelty, Muscle development
National Category
Natural Sciences
Research subject
Developmental Biology
Identifiers
urn:nbn:se:uu:diva-98909 (URN)10.1186/2041-9139-4-3 (DOI)000318902000001 ()
Funder
Knut and Alice Wallenberg FoundationSwedish Research Council
Available from2009-03-04 Created:2009-03-04 Last updated:2014-01-07Bibliographically approved

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