Mammalian skull heterochrony reveals modular evolution and a link between cranial development and brain size.
The multiple skeletal components of the skull originate asynchronously and their developmental schedule varies across amniotes. Here we present the embryonic ossification sequence of 134 species, covering all major groups of mammals and their close relatives. This comprehensive data set allows reconstruction of the heterochronic and modular evolution of the skull and the condition of the last common ancestor of mammals. We show that the mode of ossification (dermal or endochondral) unites bones into integrated evolutionary modules of heterochronic changes and imposes evolutionary constraints on cranial heterochrony. However, some skull-roof bones, such as the supraoccipital, exhibit evolutionary degrees of freedom in these constraints. Ossification timing of the neurocranium was considerably accelerated during the origin of mammals. Furthermore, association between developmental timing of the supraoccipital and brain size was identified among amniotes. We argue that cranial heterochrony in mammals has occurred in concert with encephalization but within a conserved modular organization.
1] Palaeontological Institute and Museum, University of Zürich, Karl Schmid-Strasse 4, Zürich 8006, Switzerland [2] The University Museum, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-0033, Japan.
Daisuke
D
Koyabu
Palaeontological Institute and Museum, University of Zürich, Karl Schmid-Strasse 4, Zürich 8006, Switzerland.
Ingmar
I
Werneburg
Anthropological Institute and Museum, University of Zürich, Winterthurerstrasse 190, Zürich 8057, Switzerland.
Naoki
N
Morimoto
Anthropological Institute and Museum, University of Zürich, Winterthurerstrasse 190, Zürich 8057, Switzerland.
Christoph P E
CP
Zollikofer
1] Palaeontological Institute and Museum, University of Zürich, Karl Schmid-Strasse 4, Zürich 8006, Switzerland [2] Ianigla, CCT-Mendoza, CONICET, Avda. Ruiz Leal s/n, Mendoza 5500, Argentina.
Analia M
AM
Forasiepi
The University Museum, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-0033, Japan.
Hideki
H
Endo
Department of Anatomy and Cell Biology, College of Veterinary Medicine, Seoul National University, Seoul 151-742, Korea.
Junpei
J
Kimura
Institute of Low Temperature Science, Hokkaido University, Kita-19 Nishi-8, Kita-ku, Sapporo 060-0819, Japan.
Satoshi D
SD
Ohdachi
Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet Street, Hanoi 10000, Vietnam.
Nguyen
N
Truong Son
Palaeontological Institute and Museum, University of Zürich, Karl Schmid-Strasse 4, Zürich 8006, Switzerland.
Marcelo R
MR
Sánchez-Villagra
D000818:Animals; D005075:Biological Evolution; D001921:Brain / Q000033:anatomy & histology* / Q000254:growth & development; D006801:Humans; D008322:Mammals; D010012:Osteogenesis; D012886:Skull / Q000033:anatomy & histology*