Pedomorphosis in the ancestry of marsupial mammals

Heather E White; Abigail S Tucker; Vincent Fernandez; Roberto Portela Miguez; Lionel Hautier; Anthony Herrel; Daniel J Urban; Karen E Sears; Anjali Goswami

doi:10.1016/j.cub.2023.04.009

Pedomorphosis in the ancestry of marsupial mammals

Curr Biol. 2023 Jun 5;33(11):2136-2150.e4. doi: 10.1016/j.cub.2023.04.009. Epub 2023 Apr 28.

Authors

Heather E White¹, Abigail S Tucker², Vincent Fernandez³, Roberto Portela Miguez⁴, Lionel Hautier⁵, Anthony Herrel⁶, Daniel J Urban⁷, Karen E Sears⁸, Anjali Goswami⁹

Affiliations

¹ Science Department, Natural History Museum, Cromwell Road, London SW7 5BD, UK; Centre for Craniofacial and Regenerative Biology, King's College London, Great Maze Pond, London SE1 9RT, UK; Division of Biosciences, University College London, Gower Street, London WC1E 6DE, UK. Electronic address: h.white@nhm.ac.uk.
² Centre for Craniofacial and Regenerative Biology, King's College London, Great Maze Pond, London SE1 9RT, UK.
³ European Synchrotron Radiation Facility, 71 rue des Martyrs, 38000 Grenoble, France.
⁴ Science Department, Natural History Museum, Cromwell Road, London SW7 5BD, UK.
⁵ Science Department, Natural History Museum, Cromwell Road, London SW7 5BD, UK; Institut des Sciences de l'Evolution, Université de Montpellier, CNRS, IRD, EPHE, Montpellier 34095, France.
⁶ UMR 7179, Centre National de la Recherche Scientifique/Muséum National d'Histoire Naturelle, Département Adaptations du Vivant, 55 rue Buffon, 75005 Paris, France.
⁷ Institute of Genomic Biology, University of Illinois, Urbana, IL 61801, USA.
⁸ Department of Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, CA 90095, USA.
⁹ Science Department, Natural History Museum, Cromwell Road, London SW7 5BD, UK; Division of Biosciences, University College London, Gower Street, London WC1E 6DE, UK.

PMID: 37119816
DOI: 10.1016/j.cub.2023.04.009

Abstract

Within mammals, different reproductive strategies (e.g., egg laying, live birth of extremely underdeveloped young, and live birth of well-developed young) have been linked to divergent evolutionary histories. How and when developmental variation across mammals arose is unclear. While egg laying is unquestionably considered the ancestral state for all mammals, many long-standing biases treat the extreme underdeveloped state of marsupial young as the ancestral state for therian mammals (clade including both marsupials and placentals), with the well-developed young of placentals often considered the derived mode of development. Here, we quantify mammalian cranial morphological development and estimate ancestral patterns of cranial shape development using geometric morphometric analysis of the largest comparative ontogenetic dataset of mammals to date (165 specimens, 22 species). We identify a conserved region of cranial morphospace for fetal specimens, after which cranial morphology diversified through ontogeny in a cone-shaped pattern. This cone-shaped pattern of development distinctively reflected the upper half of the developmental hourglass model. Moreover, cranial morphological variation was found to be significantly associated with the level of development (position on the altricial-precocial spectrum) exhibited at birth. Estimation of ancestral state allometry (size-related shape change) reconstructs marsupials as pedomorphic relative to the ancestral therian mammal. In contrast, the estimated allometries for the ancestral placental and ancestral therian were indistinguishable. Thus, from our results, we hypothesize that placental mammal cranial development most closely reflects that of the ancestral therian mammal, while marsupial cranial development represents a more derived mode of mammalian development, in stark contrast to many interpretations of mammalian evolution.

Keywords: cranial; development; evolution; heterochrony; mammal; morphometrics; ontogeny; paedomorphosis; shape; skull.

Publication types

Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Biological Evolution
Female
Mammals / anatomy & histology
Mammals / genetics
Marsupialia* / anatomy & histology
Marsupialia* / genetics
Placenta
Pregnancy
Skull / anatomy & histology

Grants and funding

BB/ M009513/1/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom