New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma

Autores
Diogo, Rui; Linde Medina, Marta; Abdala, Virginia Sara Luz; Ashley Ross, Miriam A.
Año de publicación
2012
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Most textbooks and research reports state that the structures of the tetrapod forelimbs and hindlimbs are serial homologues. From this view, the main challenge of evolutionary biologists is not to explain the similarity between tetrapod limbs, but instead to explain why and how they have diverged. However, these statements seem to be related to a confusion between the serial homology of the vertebrate pelvic and pectoral appendages as a whole, and the serial homology of the specific soft- and hard-tissue structures of the tetrapod forelimbs and hindlimbs, leading to an even more crucial and puzzling question being overlooked: why are the skeletal and particularly the muscle structures of the forelimb and hindlimb actually so strikingly similar to each other? Herein we provide an updated discussion of these questions and test two main hypotheses: (i) that the similarity of the limb muscles is due to serial homology; and (ii) that tetrapods that use hindlimbs for a largely exclusive function (e.g. bipedalism in humans) exhibit fewer cases of similarity between forelimbs and hindlimbs than do quadrupedal species. Our review shows that of the 23 arm, forearm and hand muscles/muscle groups of salamanders, 18 (78%) have clear ‘topological equivalents' in the hindlimb; in lizards, 14/24 (58%); in rats, 14/35 (40%); and in modern humans, 19/37 (51%). These numbers seem to support the idea that there is a plesiomorphic similarity and subsequent evolutionary divergence, but this tendency actually only applies to the three former quadrupedal taxa. Moreover, if one takes into account the total number of ‘correspondences’, one comes to a surprising and puzzling conclusion: in modern humans the number of forelimb muscles/muscle groups with clear ‘equivalents’ in the hindlimb (19) is substantially higher than in quadrupedal mammals such as rats (14), lizards (14) and even salamanders (18). These data contradict the hypothesis that divergent functions lead to divergent morphological structures. Furthermore, as we show that at least five of the 19 modern human adult forelimb elements that have a clear hindlimb ‘equivalent’ derive from embryonic anlages that are very different from the ones giving rise to their adult hindlimb ‘equivalents’, they also contradict the hypothesis that the similarity in muscle structures between the forelimb and hindlimb of tetrapods such as modern humans are due to their origin as serial homologues. This similarity is instead the result of phylogenetically independent evolutionary changes leading to a parallelism/convergence due to: (i) developmental constraints, i.e. similar molecular mechanisms are involved (particularly in the formation of the neomorphic hand), but this does not necessarily mean that similar anlages are used to form the similar adult structures; (ii) functional constraints, related to similar adaptations; (iii) topological constraints, i.e. limited physical possibilities; and even (iv) phylogenetic constraints, which tend to prevent/decrease the occurrence of new homoplasic similarities, but also help to keep older, ancestral homoplasic resemblances.
Fil: Diogo, Rui. Howard University College of Medicine; Estados Unidos
Fil: Linde Medina, Marta. University of Manchester; Reino Unido
Fil: Abdala, Virginia Sara Luz. Fundación Miguel Lillo. Dirección de Zoología. Instituto de Herpetología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Ashley Ross, Miriam A.. University Wake Forest; Estados Unidos
Materia
Comparative Anatomy
Development
Muscles
Limbs
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/26437

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spelling New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigmaDiogo, RuiLinde Medina, MartaAbdala, Virginia Sara LuzAshley Ross, Miriam A.Comparative AnatomyDevelopmentMusclesLimbshttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Most textbooks and research reports state that the structures of the tetrapod forelimbs and hindlimbs are serial homologues. From this view, the main challenge of evolutionary biologists is not to explain the similarity between tetrapod limbs, but instead to explain why and how they have diverged. However, these statements seem to be related to a confusion between the serial homology of the vertebrate pelvic and pectoral appendages as a whole, and the serial homology of the specific soft- and hard-tissue structures of the tetrapod forelimbs and hindlimbs, leading to an even more crucial and puzzling question being overlooked: why are the skeletal and particularly the muscle structures of the forelimb and hindlimb actually so strikingly similar to each other? Herein we provide an updated discussion of these questions and test two main hypotheses: (i) that the similarity of the limb muscles is due to serial homology; and (ii) that tetrapods that use hindlimbs for a largely exclusive function (e.g. bipedalism in humans) exhibit fewer cases of similarity between forelimbs and hindlimbs than do quadrupedal species. Our review shows that of the 23 arm, forearm and hand muscles/muscle groups of salamanders, 18 (78%) have clear ‘topological equivalents' in the hindlimb; in lizards, 14/24 (58%); in rats, 14/35 (40%); and in modern humans, 19/37 (51%). These numbers seem to support the idea that there is a plesiomorphic similarity and subsequent evolutionary divergence, but this tendency actually only applies to the three former quadrupedal taxa. Moreover, if one takes into account the total number of ‘correspondences’, one comes to a surprising and puzzling conclusion: in modern humans the number of forelimb muscles/muscle groups with clear ‘equivalents’ in the hindlimb (19) is substantially higher than in quadrupedal mammals such as rats (14), lizards (14) and even salamanders (18). These data contradict the hypothesis that divergent functions lead to divergent morphological structures. Furthermore, as we show that at least five of the 19 modern human adult forelimb elements that have a clear hindlimb ‘equivalent’ derive from embryonic anlages that are very different from the ones giving rise to their adult hindlimb ‘equivalents’, they also contradict the hypothesis that the similarity in muscle structures between the forelimb and hindlimb of tetrapods such as modern humans are due to their origin as serial homologues. This similarity is instead the result of phylogenetically independent evolutionary changes leading to a parallelism/convergence due to: (i) developmental constraints, i.e. similar molecular mechanisms are involved (particularly in the formation of the neomorphic hand), but this does not necessarily mean that similar anlages are used to form the similar adult structures; (ii) functional constraints, related to similar adaptations; (iii) topological constraints, i.e. limited physical possibilities; and even (iv) phylogenetic constraints, which tend to prevent/decrease the occurrence of new homoplasic similarities, but also help to keep older, ancestral homoplasic resemblances.Fil: Diogo, Rui. Howard University College of Medicine; Estados UnidosFil: Linde Medina, Marta. University of Manchester; Reino UnidoFil: Abdala, Virginia Sara Luz. Fundación Miguel Lillo. Dirección de Zoología. Instituto de Herpetología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Ashley Ross, Miriam A.. University Wake Forest; Estados UnidosWiley2012-09info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/26437Diogo, Rui; Linde Medina, Marta; Abdala, Virginia Sara Luz; Ashley Ross, Miriam A.; New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma; Wiley; Biological Reviews; 88; 1; 9-2012; 196-2141464-7931CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1111/j.1469-185X.2012.00247.xinfo:eu-repo/semantics/altIdentifier/url/http://onlinelibrary.wiley.com/doi/10.1111/j.1469-185X.2012.00247.x/abstractinfo:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-10T13:11:41Zoai:ri.conicet.gov.ar:11336/26437instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-10 13:11:42.216CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma
title New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma
spellingShingle New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma
Diogo, Rui
Comparative Anatomy
Development
Muscles
Limbs
title_short New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma
title_full New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma
title_fullStr New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma
title_full_unstemmed New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma
title_sort New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma
dc.creator.none.fl_str_mv Diogo, Rui
Linde Medina, Marta
Abdala, Virginia Sara Luz
Ashley Ross, Miriam A.
author Diogo, Rui
author_facet Diogo, Rui
Linde Medina, Marta
Abdala, Virginia Sara Luz
Ashley Ross, Miriam A.
author_role author
author2 Linde Medina, Marta
Abdala, Virginia Sara Luz
Ashley Ross, Miriam A.
author2_role author
author
author
dc.subject.none.fl_str_mv Comparative Anatomy
Development
Muscles
Limbs
topic Comparative Anatomy
Development
Muscles
Limbs
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Most textbooks and research reports state that the structures of the tetrapod forelimbs and hindlimbs are serial homologues. From this view, the main challenge of evolutionary biologists is not to explain the similarity between tetrapod limbs, but instead to explain why and how they have diverged. However, these statements seem to be related to a confusion between the serial homology of the vertebrate pelvic and pectoral appendages as a whole, and the serial homology of the specific soft- and hard-tissue structures of the tetrapod forelimbs and hindlimbs, leading to an even more crucial and puzzling question being overlooked: why are the skeletal and particularly the muscle structures of the forelimb and hindlimb actually so strikingly similar to each other? Herein we provide an updated discussion of these questions and test two main hypotheses: (i) that the similarity of the limb muscles is due to serial homology; and (ii) that tetrapods that use hindlimbs for a largely exclusive function (e.g. bipedalism in humans) exhibit fewer cases of similarity between forelimbs and hindlimbs than do quadrupedal species. Our review shows that of the 23 arm, forearm and hand muscles/muscle groups of salamanders, 18 (78%) have clear ‘topological equivalents' in the hindlimb; in lizards, 14/24 (58%); in rats, 14/35 (40%); and in modern humans, 19/37 (51%). These numbers seem to support the idea that there is a plesiomorphic similarity and subsequent evolutionary divergence, but this tendency actually only applies to the three former quadrupedal taxa. Moreover, if one takes into account the total number of ‘correspondences’, one comes to a surprising and puzzling conclusion: in modern humans the number of forelimb muscles/muscle groups with clear ‘equivalents’ in the hindlimb (19) is substantially higher than in quadrupedal mammals such as rats (14), lizards (14) and even salamanders (18). These data contradict the hypothesis that divergent functions lead to divergent morphological structures. Furthermore, as we show that at least five of the 19 modern human adult forelimb elements that have a clear hindlimb ‘equivalent’ derive from embryonic anlages that are very different from the ones giving rise to their adult hindlimb ‘equivalents’, they also contradict the hypothesis that the similarity in muscle structures between the forelimb and hindlimb of tetrapods such as modern humans are due to their origin as serial homologues. This similarity is instead the result of phylogenetically independent evolutionary changes leading to a parallelism/convergence due to: (i) developmental constraints, i.e. similar molecular mechanisms are involved (particularly in the formation of the neomorphic hand), but this does not necessarily mean that similar anlages are used to form the similar adult structures; (ii) functional constraints, related to similar adaptations; (iii) topological constraints, i.e. limited physical possibilities; and even (iv) phylogenetic constraints, which tend to prevent/decrease the occurrence of new homoplasic similarities, but also help to keep older, ancestral homoplasic resemblances.
Fil: Diogo, Rui. Howard University College of Medicine; Estados Unidos
Fil: Linde Medina, Marta. University of Manchester; Reino Unido
Fil: Abdala, Virginia Sara Luz. Fundación Miguel Lillo. Dirección de Zoología. Instituto de Herpetología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Ashley Ross, Miriam A.. University Wake Forest; Estados Unidos
description Most textbooks and research reports state that the structures of the tetrapod forelimbs and hindlimbs are serial homologues. From this view, the main challenge of evolutionary biologists is not to explain the similarity between tetrapod limbs, but instead to explain why and how they have diverged. However, these statements seem to be related to a confusion between the serial homology of the vertebrate pelvic and pectoral appendages as a whole, and the serial homology of the specific soft- and hard-tissue structures of the tetrapod forelimbs and hindlimbs, leading to an even more crucial and puzzling question being overlooked: why are the skeletal and particularly the muscle structures of the forelimb and hindlimb actually so strikingly similar to each other? Herein we provide an updated discussion of these questions and test two main hypotheses: (i) that the similarity of the limb muscles is due to serial homology; and (ii) that tetrapods that use hindlimbs for a largely exclusive function (e.g. bipedalism in humans) exhibit fewer cases of similarity between forelimbs and hindlimbs than do quadrupedal species. Our review shows that of the 23 arm, forearm and hand muscles/muscle groups of salamanders, 18 (78%) have clear ‘topological equivalents' in the hindlimb; in lizards, 14/24 (58%); in rats, 14/35 (40%); and in modern humans, 19/37 (51%). These numbers seem to support the idea that there is a plesiomorphic similarity and subsequent evolutionary divergence, but this tendency actually only applies to the three former quadrupedal taxa. Moreover, if one takes into account the total number of ‘correspondences’, one comes to a surprising and puzzling conclusion: in modern humans the number of forelimb muscles/muscle groups with clear ‘equivalents’ in the hindlimb (19) is substantially higher than in quadrupedal mammals such as rats (14), lizards (14) and even salamanders (18). These data contradict the hypothesis that divergent functions lead to divergent morphological structures. Furthermore, as we show that at least five of the 19 modern human adult forelimb elements that have a clear hindlimb ‘equivalent’ derive from embryonic anlages that are very different from the ones giving rise to their adult hindlimb ‘equivalents’, they also contradict the hypothesis that the similarity in muscle structures between the forelimb and hindlimb of tetrapods such as modern humans are due to their origin as serial homologues. This similarity is instead the result of phylogenetically independent evolutionary changes leading to a parallelism/convergence due to: (i) developmental constraints, i.e. similar molecular mechanisms are involved (particularly in the formation of the neomorphic hand), but this does not necessarily mean that similar anlages are used to form the similar adult structures; (ii) functional constraints, related to similar adaptations; (iii) topological constraints, i.e. limited physical possibilities; and even (iv) phylogenetic constraints, which tend to prevent/decrease the occurrence of new homoplasic similarities, but also help to keep older, ancestral homoplasic resemblances.
publishDate 2012
dc.date.none.fl_str_mv 2012-09
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
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info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/26437
Diogo, Rui; Linde Medina, Marta; Abdala, Virginia Sara Luz; Ashley Ross, Miriam A.; New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma; Wiley; Biological Reviews; 88; 1; 9-2012; 196-214
1464-7931
CONICET Digital
CONICET
url http://hdl.handle.net/11336/26437
identifier_str_mv Diogo, Rui; Linde Medina, Marta; Abdala, Virginia Sara Luz; Ashley Ross, Miriam A.; New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma; Wiley; Biological Reviews; 88; 1; 9-2012; 196-214
1464-7931
CONICET Digital
CONICET
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