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Forelimb-hindlimb developmental timing changes across tetrapod phylogeny.

Bininda-Emonds OR, Jeffery JE, Sánchez-Villagra MR, Hanken J, Colbert M, Pieau C, Selwood L, Ten Cate C, Raynaud A, Osabutey CK, Richardson MK - BMC Evol. Biol. (2007)

Bottom Line: Although exceptions are known, the two anurans we examined reversed the pattern and displayed a significant advance in hindlimb development.Major heterochronic changes in early limb development and chondrogenesis were absent within major clades except Lissamphibia, and their presence across vertebrate phylogeny are not easily correlated with adaptive phenomena related to morphological differences in the adult fore- and hindlimbs.Our results highlight the more important role generally played by allometric heterochrony in this instance to shape adult morphology.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Biology, University of Leiden, Kaiserstraat 63, 2311GP, Leiden, The Netherlands. Olaf.Bininda@uni-jena.de

ABSTRACT

Background: Tetrapods exhibit great diversity in limb structures among species and also between forelimbs and hindlimbs within species, diversity which frequently correlates with locomotor modes and life history. We aim to examine the potential relation of changes in developmental timing (heterochrony) to the origin of limb morphological diversity in an explicit comparative and quantitative framework. In particular, we studied the relative time sequence of development of the forelimbs versus the hindlimbs in 138 embryos of 14 tetrapod species spanning a diverse taxonomic, ecomorphological and life-history breadth. Whole-mounts and histological sections were used to code the appearance of 10 developmental events comprising landmarks of development from the early bud stage to late chondrogenesis in the forelimb and the corresponding serial homologues in the hindlimb.

Results: An overall pattern of change across tetrapods can be discerned and appears to be relatively clade-specific. In the primitive condition, as seen in Chondrichthyes and Osteichthyes, the forelimb/pectoral fin develops earlier than the hindlimb/pelvic fin. This pattern is either retained or re-evolved in eulipotyphlan insectivores (= shrews, moles, hedgehogs, and solenodons) and taken to its extreme in marsupials. Although exceptions are known, the two anurans we examined reversed the pattern and displayed a significant advance in hindlimb development. All other species examined, including a bat with its greatly enlarged forelimbs modified as wings in the adult, showed near synchrony in the development of the fore and hindlimbs.

Conclusion: Major heterochronic changes in early limb development and chondrogenesis were absent within major clades except Lissamphibia, and their presence across vertebrate phylogeny are not easily correlated with adaptive phenomena related to morphological differences in the adult fore- and hindlimbs. The apparently conservative nature of this trait means that changes in chondrogenetic patterns may serve as useful phylogenetic characters at higher taxonomic levels in tetrapods. Our results highlight the more important role generally played by allometric heterochrony in this instance to shape adult morphology.

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Average event-pair scores (EPSs) plotted on a phylogeny of the taxa examined, with visual examples of forelimb (FL) and hindlimb (HL) across the tree. Plot symbols in blue and green are significantly less than and greater than one, respectively; forelimb-hindlimb synchrony, in red. The tree is derived from references 33 and 34.
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Figure 1: Average event-pair scores (EPSs) plotted on a phylogeny of the taxa examined, with visual examples of forelimb (FL) and hindlimb (HL) across the tree. Plot symbols in blue and green are significantly less than and greater than one, respectively; forelimb-hindlimb synchrony, in red. The tree is derived from references 33 and 34.

Mentions: The average event-pair score (EPS; see Methods) was plotted for each species (Table 1, Fig. 1). The two anurans (Xenopus, Eleutherodactylus) show average EPS scores significantly less than one, indicating that hindlimb development generally precedes that of the forelimb (noted by [6,7]). The two birds (Taeniopygia, Gallus) also tend to show an advance in hindlimb development – small differences between fore- and hindlimb timing can be detected visually (for example, in the figures of Gallus in [8]) – but are not significantly different from forelimb-hindlimb synchrony together with the remaining diapsids Lacerta and Emys. Among mammals, the marsupials (Trichosurus, Dasyurus and Sminthopsis) and eulipotyphlan insectivores (Erinaceus and Talpa) all show significant advances in forelimb development. The generally smaller forelimb advances among the remaining eutherian mammals were not significantly different from synchronous development.


Forelimb-hindlimb developmental timing changes across tetrapod phylogeny.

Bininda-Emonds OR, Jeffery JE, Sánchez-Villagra MR, Hanken J, Colbert M, Pieau C, Selwood L, Ten Cate C, Raynaud A, Osabutey CK, Richardson MK - BMC Evol. Biol. (2007)

Average event-pair scores (EPSs) plotted on a phylogeny of the taxa examined, with visual examples of forelimb (FL) and hindlimb (HL) across the tree. Plot symbols in blue and green are significantly less than and greater than one, respectively; forelimb-hindlimb synchrony, in red. The tree is derived from references 33 and 34.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2194785&req=5

Figure 1: Average event-pair scores (EPSs) plotted on a phylogeny of the taxa examined, with visual examples of forelimb (FL) and hindlimb (HL) across the tree. Plot symbols in blue and green are significantly less than and greater than one, respectively; forelimb-hindlimb synchrony, in red. The tree is derived from references 33 and 34.
Mentions: The average event-pair score (EPS; see Methods) was plotted for each species (Table 1, Fig. 1). The two anurans (Xenopus, Eleutherodactylus) show average EPS scores significantly less than one, indicating that hindlimb development generally precedes that of the forelimb (noted by [6,7]). The two birds (Taeniopygia, Gallus) also tend to show an advance in hindlimb development – small differences between fore- and hindlimb timing can be detected visually (for example, in the figures of Gallus in [8]) – but are not significantly different from forelimb-hindlimb synchrony together with the remaining diapsids Lacerta and Emys. Among mammals, the marsupials (Trichosurus, Dasyurus and Sminthopsis) and eulipotyphlan insectivores (Erinaceus and Talpa) all show significant advances in forelimb development. The generally smaller forelimb advances among the remaining eutherian mammals were not significantly different from synchronous development.

Bottom Line: Although exceptions are known, the two anurans we examined reversed the pattern and displayed a significant advance in hindlimb development.Major heterochronic changes in early limb development and chondrogenesis were absent within major clades except Lissamphibia, and their presence across vertebrate phylogeny are not easily correlated with adaptive phenomena related to morphological differences in the adult fore- and hindlimbs.Our results highlight the more important role generally played by allometric heterochrony in this instance to shape adult morphology.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Biology, University of Leiden, Kaiserstraat 63, 2311GP, Leiden, The Netherlands. Olaf.Bininda@uni-jena.de

ABSTRACT

Background: Tetrapods exhibit great diversity in limb structures among species and also between forelimbs and hindlimbs within species, diversity which frequently correlates with locomotor modes and life history. We aim to examine the potential relation of changes in developmental timing (heterochrony) to the origin of limb morphological diversity in an explicit comparative and quantitative framework. In particular, we studied the relative time sequence of development of the forelimbs versus the hindlimbs in 138 embryos of 14 tetrapod species spanning a diverse taxonomic, ecomorphological and life-history breadth. Whole-mounts and histological sections were used to code the appearance of 10 developmental events comprising landmarks of development from the early bud stage to late chondrogenesis in the forelimb and the corresponding serial homologues in the hindlimb.

Results: An overall pattern of change across tetrapods can be discerned and appears to be relatively clade-specific. In the primitive condition, as seen in Chondrichthyes and Osteichthyes, the forelimb/pectoral fin develops earlier than the hindlimb/pelvic fin. This pattern is either retained or re-evolved in eulipotyphlan insectivores (= shrews, moles, hedgehogs, and solenodons) and taken to its extreme in marsupials. Although exceptions are known, the two anurans we examined reversed the pattern and displayed a significant advance in hindlimb development. All other species examined, including a bat with its greatly enlarged forelimbs modified as wings in the adult, showed near synchrony in the development of the fore and hindlimbs.

Conclusion: Major heterochronic changes in early limb development and chondrogenesis were absent within major clades except Lissamphibia, and their presence across vertebrate phylogeny are not easily correlated with adaptive phenomena related to morphological differences in the adult fore- and hindlimbs. The apparently conservative nature of this trait means that changes in chondrogenetic patterns may serve as useful phylogenetic characters at higher taxonomic levels in tetrapods. Our results highlight the more important role generally played by allometric heterochrony in this instance to shape adult morphology.

Show MeSH
Related in: MedlinePlus