Developmental approaches to human evolution

353 Pages·2015·8.536 MB·English

by  Julia C. Boughner, Campbell Rolian

Developmental Approaches
to Human Evolution
Developmental Approaches
to Human Evolution
Edited by
Julia C. Boughner and Campbell Rolian
Copyright © 2016 by John Wiley & Sons, Inc. All rights reserved
Published by John Wiley & Sons, Inc., Hoboken, New Jersey
Published simultaneously in Canada
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Library of Congress Cataloging‐in‐Publication data applied for
ISBN: 9781118524688
Cover image: Janka Dharmasena © iStock / Getty Images Plus, Ralf Hettler/iStockphoto,
luismmolina/iStockphoto.
10 9 8 7 6 5 4 3 2 1
Contents
Contributors vii
Foreword: Humans from Embryos ix
Günter P. Wagner
1 Introduction to Evo‐Devo‐Anthro 1
Campbell Rolian and Julia C. Boughner
2 Chondrocranial Growth, Developmental Integration and
Evolvability in the Human Skull 17
Neus Martínez‐Abadías, Mireia Esparza, Torstein Sjøvold and
Benedikt Hallgrímsson
3 The Tooth of the Matter: The Evo‐Devo of Coordinated
Phenotypic Change 35
Julia C. Boughner
4 Genetic Regulation of Amelogenesis and Implications for
Hominin Ancestors 61
Rodrigo S. Lacruz
5 Evo‐Devo Sheds Light on Mechanisms of Human Evolution:
Limb Proportions and Penile Spines 77
Philip L. Reno
6 Out on a Limb: Development and the Evolution of the
Human Appendicular Skeleton 101
Nathan M. Young and Terence D. Capellini
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vi Contents
7 Tinkering with Growth Plates: A Developmental Simulation of
Limb Bone Evolution in Hominoids 139
Campbell Rolian
8 Origin, Development, and Evolution of Primate Muscles, with
Notes on Human Anatomical Variations and Anomalies 167
Rui Diogo and Bernard Wood
9 The Evolutionary Biology of Human Neurodevelopment:
Evo‐Neuro‐Devo Comes of Age 205
Bernard Crespi and Emma Leach
10 Evolving the Developing Cortex: Conserved Gradients of
Neurogenesis Scale and Channel New Functions in Primates 231
Christine J. Charvet and Barbara L. Finlay
11 Growing Up Fast, Maturing Slowly: The Evolution of a
Uniquely Modern Human Pattern of Brain Development 261
Philipp Gunz
12 FOXP2 and the Genetic and Developmental Basis of
Human Language 285
Carles Lalueza‐Fox
13 Assembly Instructions Included 297
Kenneth Weiss and Anne Buchanan
Index 317
Contributors
Julia C. Boughner Bernard Crespi
Department of Anatomy and Department of Biological Sciences
Cell Biology Simon Fraser University
College of Medicine Burnaby, BC, Canada
University of Saskatchewan
Rui Diogo
Saskatoon, SK, Canada
Department of Anatomy
Anne Buchanan Howard University College of
Department of Anthropology Medicine
Pennsylvania State University Washington, DC, USA
University Park, PA, USA
Mireia Esparza
Terence D. Capellini Secció d’Antropologia
Department of Human Evolutionary Departament de Biologia
Biology Animal
Harvard University Universitat de Barcelona
Cambridge, MA, USA Barcelona, Spain
Christine J. Charvet Barbara L. Finlay
Behavioral and Evolutionary Behavioral and Evolutionary
Neuroscience Group Neuroscience Group
Department of Psychology Department of Psychology
Cornell University Cornell University
Ithaca, NY, USA Ithaca, NY, USA
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viii Contributors
Philipp Gunz Philip L. Reno
Department of Human Evolution Department of Anthropology
Max‐Planck‐Institute for The Pennsylvania State University
Evolutionary Anthropology University Park, PA, USA
Leipzig, Germany
Campbell Rolian
Benedikt Hallgrímsson Faculty of Veterinary Medicine
McCaig Institute for Bone and Joint University of Calgary
Research Calgary, AB, Canada
Alberta Children’s Hospital
Torstein Sjøvold
Research Institute
Osteologiska Enheten
Department of Cell Biology and
Stockholms Universitet
Anatomy
Stockholm, Sweden
Faculty of Medicine
University of Calgary Kenneth Weiss
Calgary, Canada Departments of Anthropology
and Biology
Rodrigo S. Lacruz
Pennsylvania State University
Department of Basic Science and
University Park, PA, USA
Craniofacial Biology
New York University College of Bernard Wood
Dentistry Center for the Advanced Study of
New York, NY, USA Hominid Paleobiology
Department of Anthropology
Carles Lalueza‐Fox
George Washington University
Institut de Biologia Evolutiva
Washington, DC, USA
CSIC‐Universitat Pompeu Fabra
Barcelona, Spain Nathan M. Young
Department of Orthopaedic Surgery
Emma Leach
University of California
Department of Biological Sciences
San Francisco, CA, USA
Simon Fraser University
Burnaby, BC, Canada
Neus Martínez-Abadías
Centre for Genomic Regulation (CRG)
The Barcelona Institute of Science
and Technology, Dr. Aiguader
Universitat Pompeu Fabra (UPF)
Secció d’Antropologia
Departament de Biologia Animal
Universitat de Barcelona
Barcelona, Spain
Foreword: Humans from Embryos
If there ever have been any large‐scale transformations of the study of evolution,
then there have been two recent ones, both precipitating towards the end of the 20th
century: the first is the establishment of a rigorous framework for phylogenetic and
comparative studies, and the second is the origination of developmental approaches
to evolutionary biology. The latter depended to some extent on the success of the
former, in the sense that developmental inferences about the mechanisms of evolu-
tionary change require one to use phylogenies and the comparative method to con-
textualize the mechanistic results from different species. Given the experimental bent
of the study of developmental evolution, it is not surprising that, for much of its
history, devo‐evo was a largely zoological and botanical enterprise, focusing on
Drosophila wing pigmentation, Nematode vulva development, and the origin of
limbs and flowers, among other “model characters.” Human evolution was not a
natural proving ground for devo‐evo due to the ethical and practical strictures on
any work with humans and other primates. But a determined cadre of biological
anthropologists worked towards changing that, making human evolution an impor-
tant application of developmental evolutionary thinking and research. How then is
it possible to learn about human and primate developmental evolution without
executing on primate species breeding experiments, transgenic techniques, and inter-
fering with primate embryonic development? The answer is given here in the exciting
collection of chapters on “Developmental Approaches to Human Evolution.”
Surveying the contributions to this volume, it seems there are two principal work-
arounds to overcome the lack of opportunity for direct experimentation in primates.
One could be called homology‐based mechanistic inferences. The idea is to take
advantage of mechanistic knowledge obtained from model organisms, mostly “the”
model mammal, mouse. The assumption is that homologous developmental mecha-
nisms are also relevant in primates, and thus evolutionary changes in the orthologous
genes in the human lineage are taken as evidence for a corresponding developmental
evolutionary change in human evolution. These inferences are often scaffolded with
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x Foreword
comparative genomic data showing that relevant genes or cis regulatory elements,
related to the trait of interest, have changed in the human lineage. The other approach
could be called theoretical or computational morphology. It combines phenotypic and
variational studies with theoretical models. These models can be abstract genetic
ideas about the structure of the genotype‐phenotype map or specific mechanistic
models of developmental processes. These approaches are surprisingly powerful in
generating overarching explanations of patterns of morphological and even paleon-
tological disparity.
Neither of these approaches will suffice to make anthropology a source of novel
insights into the principles and mechanisms of developmental evolution per se in the
same way as experimental systems can. But nevertheless, the inclusion of evolu-
tionary developmental data and principles will continue to lead and already has led
to a deeper and richer understanding of how the human species arose and how our
human uniqueness resulted from the same material substrate as the rest of biological
diversity. As illustrated in this volume, one area where evolutionary developmental
anthropology has a leg up over most model organism research is its relevance and
access to issues of cognitive evolutionary change. It is an exciting time to be a
biological anthropologist!
Günter P. Wagner
Yale University
Chapter 1
Introduction to Evo‐Devo‐Anthro
Campbell Rolian1 and Julia C. Boughner2
1 Faculty of Veterinary Medicine, University of Calgary, Calgary, AB, Canada
2 Department of Anatomy and Cell Biology, College of Medicine, University of Saskatchewan,
Saskatoon, SK, Canada
Evolutionary developmental biology, or evo‐devo, is a relatively young branch of
biology concerned with how and why organismal development matters to evolution.
Evo‐devo encompasses a range of unified research questions and empirical
approaches that can be grouped into two complementary research areas (Laublicher
2007). The first area concerns the process of organismal development. This research
uses molecular tools such as studies of gene and protein expression patterns to
understand how processes of organismal development have evolved and produced
phenotypic diversification at macroevolutionary scales. The second approach focuses
on the role that process plays in structuring the pattern of heritable phenotypic vari-
ation among individuals. This approach relies on quantitative genetic theory and
morphometric tools to measure developmentally determined patterns of phenotypic
variation, typically at the level of populations, and to understand how these patterns
have biased or constrained the rate and direction of evolutionary change within and
between species (Raff 2000).
In the past couple of decades, the types of research questions that evo‐devo
addresses have also become of great interest to biological anthropologists. The
discipline is gaining traction among researchers interested in the role(s) played by
organismal development in the evolution of uniquely human, and non‐human
primate, traits. This volume aims to provide an overview of past and ongoing research
in evo‐devo specifically as it applies to the study of human and primate evolution –
Evolutionary Developmental Anthropology (EDA, or Evo‐Devo‐Anthro). In this
Developmental Approaches to Human Evolution, First Edition. Edited by
Julia C. Boughner and Campbell Rolian.
© 2016 John Wiley & Sons, Inc. Published 2016 by John Wiley & Sons, Inc.
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