Do Developmental Constraints and High Integration Limit the Evolution of the Marsupial Oral Apparatus?
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.
*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.
Anjali
A
Goswami
*Department of Genetics, Evolution and Environment, University College London, Gower Street, London, WC1E 6BT, UK.
Marcela
M
Randau
Department of Geological Sciences, 1001 E. 10th Street, Indiana University, Bloomington, IN, 47405, USA.
P David
PD
Polly
School of Biological Sciences, Goddard Building 8, University of Queensland, St. Lucia 4072, Australia.
Vera
V
Weisbecker
*Department of Genetics, Evolution and Environment, University College London, Gower Street, London, WC1E 6BT, UK.
C Verity
CV
Bennett
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.
Lionel
L
Hautier
Palaeontological Institute and Museum, University of Zürich, Karl-Schmid-Strasse 4, CH-8006, Zürich, Switzerland.
Marcelo R
MR
Sánchez-Villagra
D000818:Animals; D005075:Biological Evolution; D008394:Marsupialia / Q000033:anatomy & histology* / Q000254:growth & development*; D009055:Mouth / Q000033:anatomy & histology* / Q000254:growth & development*