Do Developmental Constraints and High Integration Limit the Evolution of the Marsupial Oral Apparatus?
Identifieur interne : 001895 ( PubMed/Curation ); précédent : 001894; suivant : 001896Do Developmental Constraints and High Integration Limit the Evolution of the Marsupial Oral Apparatus?
Auteurs : Anjali Goswami [Royaume-Uni] ; Marcela Randau [Royaume-Uni] ; P David Polly [États-Unis] ; Vera Weisbecker [Australie] ; C Verity Bennett [Royaume-Uni] ; Lionel Hautier [France] ; Marcelo R. Sánchez-Villagra [Suisse]Source :
- Integrative and comparative biology [ 1557-7023 ] ; 2016.
Abstract
Developmental constraints can have significant influence on the magnitude and direction of evolutionary change, and many studies have demonstrated that these effects are manifested on macroevolutionary scales. Phenotypic integration, or the strong interactions among traits, has been similarly invoked as a major influence on morphological variation, and many studies have demonstrated that trait integration changes through ontogeny, in many cases decreasing with age. Here, we unify these perspectives in a case study of the ontogeny of the mammalian cranium, focusing on a comparison between marsupials and placentals. Marsupials are born at an extremely altricial state, requiring, in most cases, the use of the forelimbs to climb to the pouch, and, in all cases, an extended period of continuous suckling, during which most of their development occurs. Previous work has shown that marsupials are less disparate in adult cranial form than are placentals, particularly in the oral apparatus, and in forelimb ontogeny and adult morphology, presumably due to functional selection pressures on these two systems during early postnatal development. Using phenotypic trajectory analysis to quantify prenatal and early postnatal cranial ontogeny in 10 species of therian mammals, we demonstrate that this pattern of limited variation is also apparent in the development of the oral apparatus of marsupials, relative to placentals, but not in the skull more generally. Combined with the observation that marsupials show extremely high integration of the oral apparatus in early postnatal ontogeny, while other cranial regions show similar levels of integration to that observed in placentals, we suggest that high integration may compound the effects of the functional constraints for continuous suckling to ultimately limit the ontogenetic and adult disparity of the marsupial oral apparatus throughout their evolutionary history.
DOI: 10.1093/icb/icw039
PubMed: 27260858
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Sánchez-Villagra</name><affiliation wicri:level="1"><nlm:affiliation>Palaeontological Institute and Museum, University of Zürich, Karl-Schmid-Strasse 4, CH-8006, Zürich, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Palaeontological Institute and Museum, University of Zürich, Karl-Schmid-Strasse 4, CH-8006, Zürich</wicri:regionArea></affiliation></author></analytic><series><title level="j">Integrative and comparative biology</title><idno type="eISSN">1557-7023</idno><imprint><date when="2016" type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Developmental constraints can have significant influence on the magnitude and direction of evolutionary change, and many studies have demonstrated that these effects are manifested on macroevolutionary scales. Phenotypic integration, or the strong interactions among traits, has been similarly invoked as a major influence on morphological variation, and many studies have demonstrated that trait integration changes through ontogeny, in many cases decreasing with age. Here, we unify these perspectives in a case study of the ontogeny of the mammalian cranium, focusing on a comparison between marsupials and placentals. Marsupials are born at an extremely altricial state, requiring, in most cases, the use of the forelimbs to climb to the pouch, and, in all cases, an extended period of continuous suckling, during which most of their development occurs. Previous work has shown that marsupials are less disparate in adult cranial form than are placentals, particularly in the oral apparatus, and in forelimb ontogeny and adult morphology, presumably due to functional selection pressures on these two systems during early postnatal development. Using phenotypic trajectory analysis to quantify prenatal and early postnatal cranial ontogeny in 10 species of therian mammals, we demonstrate that this pattern of limited variation is also apparent in the development of the oral apparatus of marsupials, relative to placentals, but not in the skull more generally. Combined with the observation that marsupials show extremely high integration of the oral apparatus in early postnatal ontogeny, while other cranial regions show similar levels of integration to that observed in placentals, we suggest that high integration may compound the effects of the functional constraints for continuous suckling to ultimately limit the ontogenetic and adult disparity of the marsupial oral apparatus throughout their evolutionary history.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">27260858</PMID><DateCreated><Year>2016</Year><Month>08</Month><Day>20</Day></DateCreated><DateRevised><Year>2017</Year><Month>02</Month><Day>20</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1557-7023</ISSN><JournalIssue CitedMedium="Internet"><Volume>56</Volume><Issue>3</Issue><PubDate><Year>2016</Year><Month>Sep</Month></PubDate></JournalIssue><Title>Integrative and comparative biology</Title><ISOAbbreviation>Integr. Comp. Biol.</ISOAbbreviation></Journal><ArticleTitle>Do Developmental Constraints and High Integration Limit the Evolution of the Marsupial Oral Apparatus?</ArticleTitle><Pagination><MedlinePgn>404-15</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1093/icb/icw039</ELocationID><Abstract><AbstractText>Developmental constraints can have significant influence on the magnitude and direction of evolutionary change, and many studies have demonstrated that these effects are manifested on macroevolutionary scales. Phenotypic integration, or the strong interactions among traits, has been similarly invoked as a major influence on morphological variation, and many studies have demonstrated that trait integration changes through ontogeny, in many cases decreasing with age. Here, we unify these perspectives in a case study of the ontogeny of the mammalian cranium, focusing on a comparison between marsupials and placentals. Marsupials are born at an extremely altricial state, requiring, in most cases, the use of the forelimbs to climb to the pouch, and, in all cases, an extended period of continuous suckling, during which most of their development occurs. Previous work has shown that marsupials are less disparate in adult cranial form than are placentals, particularly in the oral apparatus, and in forelimb ontogeny and adult morphology, presumably due to functional selection pressures on these two systems during early postnatal development. Using phenotypic trajectory analysis to quantify prenatal and early postnatal cranial ontogeny in 10 species of therian mammals, we demonstrate that this pattern of limited variation is also apparent in the development of the oral apparatus of marsupials, relative to placentals, but not in the skull more generally. Combined with the observation that marsupials show extremely high integration of the oral apparatus in early postnatal ontogeny, while other cranial regions show similar levels of integration to that observed in placentals, we suggest that high integration may compound the effects of the functional constraints for continuous suckling to ultimately limit the ontogenetic and adult disparity of the marsupial oral apparatus throughout their evolutionary history.</AbstractText><CopyrightInformation>© The Author 2016. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Goswami</LastName><ForeName>Anjali</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>*Department of Genetics, Evolution and Environment, University College London, Gower Street, London, WC1E 6BT, UK Department of Earth Sciences, University College London, Gower Street, London, WC1E 6BT, UK a.goswami@ucl.ac.uk.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Randau</LastName><ForeName>Marcela</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>*Department of Genetics, Evolution and Environment, University College London, Gower Street, London, WC1E 6BT, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Polly</LastName><ForeName>P David</ForeName><Initials>PD</Initials><AffiliationInfo><Affiliation>Department of Geological Sciences, 1001 E. 10th Street, Indiana University, Bloomington, IN, 47405, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Weisbecker</LastName><ForeName>Vera</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>School of Biological Sciences, Goddard Building 8, University of Queensland, St. Lucia 4072, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bennett</LastName><ForeName>C Verity</ForeName><Initials>CV</Initials><AffiliationInfo><Affiliation>*Department of Genetics, Evolution and Environment, University College London, Gower Street, London, WC1E 6BT, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hautier</LastName><ForeName>Lionel</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Laboratoire de Paléontologie, Institut des Sciences de l'Èvolution de Montpellier (CNRS, UM, IRD, EPHE), c.c. 064, Université Montpellier 2, Place Eugène Bataillon, F-34095 Montpellier, Cedex 5 , France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sánchez-Villagra</LastName><ForeName>Marcelo R</ForeName><Initials>MR</Initials><AffiliationInfo><Affiliation>Palaeontological Institute and Museum, University of Zürich, Karl-Schmid-Strasse 4, CH-8006, Zürich, Switzerland.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2016</Year><Month>06</Month><Day>02</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Integr Comp Biol</MedlineTA><NlmUniqueID>101152341</NlmUniqueID><ISSNLinking>1540-7063</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><CommentsCorrectionsList><CommentsCorrections RefType="Cites"><RefSource>Dev Dyn. 2006 May;235(5):1181-93</RefSource><PMID Version="1">16408286</PMID></CommentsCorrections><CommentsCorrections 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