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Comparative pelvic development of the axolotl (Ambystoma mexicanum) and the Australian lungfish (Neoceratodus forsteri): conservation and innovation across the fish-tetrapod transition
Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för fysiologi och utvecklingsbiologi, Evolutionär organismbiologi.
Macquarie University.
Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för fysiologi och utvecklingsbiologi, Evolutionär organismbiologi.
2013 (Engelska)Ingår i: EvoDevo, ISSN 2041-9139, E-ISSN 2041-9139, Vol. 4, s. 3-Artikel i tidskrift (Refereegranskat) 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.

Ort, förlag, år, upplaga, sidor
2013. Vol. 4, s. 3-
Nyckelord [en]
Fish-tetrapod transition, Pelvic girdle, Heterochrony, Extant phylogenetic bracketing method, Evolutionary novelty, Muscle development
Nationell ämneskategori
Naturvetenskap
Forskningsämne
Miljömedicinsk utvecklingsbiologi
Identifikatorer
URN: urn:nbn:se:uu:diva-98909DOI: 10.1186/2041-9139-4-3ISI: 000318902000001OAI: oai:DiVA.org:uu-98909DiVA, id: diva2:201522
Forskningsfinansiär
Knut och Alice Wallenbergs StiftelseVetenskapsrådetTillgänglig från: 2009-03-04 Skapad: 2009-03-04 Senast uppdaterad: 2017-12-13Bibliografiskt granskad
Ingår i avhandling
1. The Origin of Tetrapod Limbs and Girdles: Fossil and Developmental Evidence
Öppna denna publikation i ny flik eller fönster >>The Origin of Tetrapod Limbs and Girdles: Fossil and Developmental Evidence
2009 (Engelska)Doktorsavhandling, sammanläggning (Övrigt vetenskapligt)
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.

 

Ort, förlag, år, upplaga, sidor
Uppsala: Acta Universitatis Upsaliensis, 2009. s. 53
Serie
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 613
Nationell ämneskategori
Mikrobiologi
Identifikatorer
urn:nbn:se:uu:diva-98911 (URN)978-91-554-7448-5 (ISBN)
Disputation
2009-04-09, Lindhalsalen, EBC, Norbyvägen 14, Uppsala, 13:00 (Engelska)
Opponent
Handledare
Tillgänglig från: 2009-03-13 Skapad: 2009-03-04 Senast uppdaterad: 2009-04-03Bibliografiskt granskad

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