Evol Biol (2012) 39:443–446
DOI 10.1007/s11692-012-9204-5
INTRODUCTION
Human EvoDevo
Philipp Mitteroecker • Philipp Gunz
Received: 18 October 2012 / Accepted: 19 October 2012 / Published online: 2 November 2012
Springer Science+Business Media New York 2012
With the realization that any evolutionary change,
apparent in the adult, is the result of some primary
alteration in the processes of growth and development, it seems highly desirable to discover the conditions in which human growth differs from the
growth of non-human primates
A. Schultz 1950:428
Evolutionary developmental biology (EvoDevo) investigates how development influences organismal evolution
and how—as a result—development itself evolves (e.g.,
Hall 1999; Arthur 2002; Müller 2007). EvoDevo has led to
significant insights into both domains of science, evolutionary biology and developmental biology, and became an
important part of an extended body of evolutionary theory
(Pigliucci and Müller 2010).
Already to Darwin ontogenetic development was a
major source of evidence for evolutionary processes, and
early evolutionary biologists such as Ernst Haeckel speculated extensively on how organismal development and
evolution might be intertwined. But despite of a small
number of outstanding pioneers, such as Conrad H.
Waddington and Ivan Schmalhausen, only in the 1980s
EvoDevo formed a distinct discipline, owing partly to
the rapid advancements in molecular and experimental
P. Mitteroecker (&)
Department of Theoretical Biology, University of Vienna,
Althanstrasse 14, 1090 Vienna, Austria
e-mail: [email protected]
P. Gunz
Department of Human Evolution, Max Planck Institute for
Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig,
Germany
developmental biology at that time. The study of human
evolution and development (Human EvoDevo) has played
only a minor role in this research agenda, despite the significant interest in the evolution of our own species (but
see, e.g., Oxnard 1983; Richtsmeier et al. 1993; Shea 1989;
Lovejoy et al. 1999; O’Higgins and Cohn 2000; Hallgrimsson et al. 2002; Minugh-Purvis and McNamara 2002;
Mitteroecker et al. 2004; Held 2009).
Yet it had been recognized early on—actually in
pre-Darwinian times—that the differences in appearance
between modern humans and great apes resemble
changes observable during primate growth. Geoffroy SaintHillaire, for instance, wrote in 1836: ‘‘In the head of the
young orang, we find the childlike and gracious features of
man […] we find the same correspondences of habits, the
same gentleness and sympathetic affection, also some traits
of sulkiness and rebellion in response to contradiction’’
(pp. 94–95, cited after Gould 1977). In 1905, J. Kollmann
expressed this observation more explicitly in his fetalization theory, which became widely known through Bolk’s
1926 book ‘‘Das Problem der Menschwerdung’’. Bolk
explained modern human morphology by two interrelated
phenomena: (1) the physiological retardation of human
development, and (2) the retention of ancestral juvenile
proportions (fetalization). While the first phenomenon has
been confirmed be numerous studies (e.g., Smith et al.
2007; see also the papers by Leigh and by Neubauer and
Hublin in this issue), the second idea has largely been
rejected in modern biology. However, the fetalization
theory had been highly influential for many decades. For
example, Gavin de Beer suggested that: ‘‘[…] modern man
may be related to a neanderthaloid type, if he can be
regarded as descended by neoteny from a juvenile from of
the latter. If the human ancestors were similar to Neanderthal, Pithecanthropus or Australopithecus, modern man
123
444
would have descended from them by retention of features in the juvenile forms of their skulls […]’’ (1951:71).
But at about the same time, from the 1920s to the 1960s, a
school of comparative developmental biology and anatomy, dominated by German and Swiss scholars such as
Franz Weidenreich, Adolph Schultz, Dietrich Starck,
Benno Kummer, and Josef Biegert, argued against the
importance of fetalization in human evolution. In numerous
meticulous empirical studies, these authors emphasized the
striking similarities among primates at early developmental
stages and the divergent growth patterns thereafter—an
observation much better explained by Karl Ernst von
Baer’s model of developmental divergence rather than by
recapitulation and fetalization. Schultz (1950:439) wrote:
‘‘In early embryonic life all primates are morphologically
alike and differences between the various groups and the
many species of primates, including the manifold distinctions of man, appear only gradually during growth.’’
Despite the apparent overall retardation of human development relative to the great apes and some instances of
heterochrony (changes in developmental timing), this view
of diverging development among primates still holds today.
Schultz also pointed out that the human life history pattern
is unique among primates (Schultz 1969; see also the
contributions by Kachel and Premo, Leigh, and Low et al.
to this issue).
The measurement and statistical analysis of morphology has always played a crucial role in studies of human
growth and evolution, and also modern geometric morphometrics has received strong inputs from physical
anthropology in the last two decades (e.g., Bookstein 1998;
Slice 2005). Especially in the second half of the twentieth
century, the morphometric concepts of allometric scaling
and heterochrony have been used extensively to explain the
evolution of modern human and primate morphology (e.g.,
Shea 1989), closely reflecting the idea of fetalization. Only
in the new millennium the advanced morphometric
approaches permitted to draw a more differentiated picture:
allometric scaling does play a role in the evolution of
several aspects of modern and fossil human anatomy, but
only together with the divergence of developmental pathways at various age stages, particularly during perinatal
and early postnatal development (e.g., Richtsmeier et al.
1993; Ackermann and Krovitz 2002; Lieberman et al.
2002; Mitteroecker et al. 2004, 2005; Coquerelle et al.
2010; see also the contributions by Gunz, McNulty, and
Singleton to this issue).
Based on early studies of protein and DNA comparison,
King and Wilson concluded in 1975 that ‘‘the molecular
similarity between chimpanzees and humans is extraordinary’’ because ‘‘the genetic distances among species from
different genera are considerably larger than the humanchimpanzee genetic distance’’ (p. 113), whereas at the
123
Evol Biol (2012) 39:443–446
phenotypic level humans are distinct among the great apes.
Today, after both the human and the chimpanzee genomes
have been fully sequenced, we know that the two genomes
differ only 1.23 % in terms of nucleotide substitutions and that
orthologous proteins in human and chimpanzee are extremely
similar. King and Wilson suggested that a small number of
regulatory genes, influencing the timing and activity of the
expression of other genes during development, account for the
pronounced phenotypic differences between humans and
chimpanzees. This idea has stayed attractive until present,
especially as the vastly increasing number of molecular
studies presented little convincing evidence that the differences between humans and chimpanzees can be explained by
mutations of single coding genes (e.g., Carroll 2005).
Empirical studies of human and primate transcriptomes are
still hampered by methodological problems but already generated promising results, including insights into the transcription of genes in the human brain (e.g., Caceres et al. 2003;
Khaitovich et al. 2006, Prabhakar et al. 2008; Somel et al.
2009). However, the study of model systems and theoretical
considerations indicate that morphological differences in
complex anatomical structures such as the primate skull
usually cannot be attributed to allelic variation or variation
in the expression of one single gene, because the complex genetic background ‘‘funnels’’ to a few developmental
processes that ultimately determine adult morphology
(Hallgrimsson and Lieberman 2008; Martı́nez Abadı́as et al.
and Mitteroecker et al. in this issue). The evolution of complex
phenotypes usually involves alterations of many genes, some
of which may compensate the effects of others (Pavlicev and
Wagner 2012). Furthermore, gene expression is significantly
influenced by the individual’s environment and can, to some
degree, even be inherited to its offspring (Low et al. this issue).
This special issue on Human EvoDevo is aimed at
giving an overview of recent progress and ongoing research
in this field. As the historical notes above and the contributions in this issue demonstrate, Human EvoDevo differs
in several ways—mostly methodologically—from other
areas of EvoDevo research. Despite the remarkable distinctiveness of humans regarding their cultural, behavioral,
and locomotor repertoire, the anatomical differences
between modern humans and their closest living and
extinct relatives are small and of quantitative rather than of
qualitative nature. Most approaches to Human EvoDevo
thus have focused on the ontogeny of these small but
potentially decisive anatomical differences, whereas the
majority of classical EvoDevo studies investigate more
large-scale evolutionary processes, such as the evolution of
new body plans or the emergence or loss of entire organs.
The quantification of growth patterns continues to play an
important role in Human EvoDevo (see the contributions
by Gunz, Martı́nez Abadı́as et al., McNulty, Mitteroecker
et al., and Singleton) and other computational approaches,
Evol Biol (2012) 39:443–446
such as finite element analysis, are gaining prominence
(O’Higgins et al. and Toro in this issue). Despite the strong
comparative tradition in the study of human growth and
development, contemporary Human EvoDevo research
also investigates how the developmental system and postnatal growth processes may have driven or constrained
hominid evolution (e.g., contributions by Broek et al.,
Gunz, Hamrick, McNulty, Mitteroecker et al., Singleton,
and Toro). While experimental approaches are common in
contemporary EvoDevo, they are of course impossible in
humans and great apes. Experiments and genetic perturbations therefore have to be made on model systems
(Martı́nez Abadı́as et al. in this issue).
Broek et al. and Low et al. in this issue show that
research in Human EvoDevo has a significant potential to
contribute to the study of human health. Many studies are
focused on the evolution and development of the human
brain (for reviews see the contributions by Leigh and by
Neubauer and Hublin) and some studies even extended the
EvoDevo paradigm to human behavior, life history, and
language (see the contributions by Fitch, Kachel and
Premo, Leigh, and Low et al.).
This special issue results from a workshop on Human
EvoDevo hosted and financed by the Konrad Lorenz
Institute for Evolution and Cognition Research in Altenberg, Austria. We are very grateful to the institute and in
particular to Werner Callebaut, Eva Karner, and Gerd
Müller for their support. We are also indebted to Benedikt
Hallgrimsson and all the authors for making possible this
special issue on Human EvoDevo.
References
Ackermann, R. R., & Krovitz, G. E. (2002). Common pattern of facial
ontogeny in the hominid lineage. The Anatomical Record (New
Anat.), 269, 142–147.
Arthur, W. (2002). The emerging conceptual framework of evolutionary developmental biology. Nature, 415(14), 757–764.
Bolk, L. (1926). Das problem der Menschwerdung. Jena: Gustav
Fischer.
Bookstein, F. (1998). A hundred years of morphometrics. Acta
Zoologica Academiae Scientarium Hungaricae, 44(1–2), 7–59.
Caceres, M., Lachuer, J., Zapala, M. A., Redmond, J. C., Kudo, L.,
Geschwind, D. H., et al. (2003). Elevated gene expression levels
distinguish human from non-human primate brains. Proceedings
of the National Academy of Sciences of the United States of
America, 100(22), 13030–13035.
Carroll, S. B. (2005). Evolution at two levels: On genes and form.
PLoS Biology, 3(7), e245.
Coquerelle, M., Bookstein, F. L., Braga, J., Halazonetis, D. J., &
Weber, G. W. (2010). Fetal and infant growth patterns of the
mandibular symphysis in modern humans and chimpanzees (Pan
troglodytes). Journal of Anatomy, 217(5), 507–520.
De Beer, G. R. (1951). Embryos and ancestors. Oxford: Clarendon
Press.
445
Gould, S. J. (1977). Ontogeny and phylogeny. Cambridge: Harvard
University Press.
Hall, B. K. (1999). Evolutionary developmental biology. Dodrecht:
Kluwer.
Hallgrimsson, B., & Lieberman, D. E. (2008). Mouse models and the
evolutionary developmental biology of the skull. Integrative and
Comparative Biology, 48, 373–384.
Hallgrimsson, B., Willmore, K., & Hall, B. K. (2002). Canalization,
developmental stability, and morphological integration in primate limbs. American Journal of Physical Anthropology, 35,
131–158.
Held, L. I. (2009). Quirks of human anatomy: An evo-devo look at the
human body. Cambridge: Cambridge University Press.
Khaitovich, P., Enard, W., Lachmann, M., & Paabo, S. (2006).
Evolution of primate gene expression. Nature Reviews Genetics,
7(9), 693–702.
King, M. C., & Wilson, A. C. (1975). Evolution at two levels in
humans and chimpanzees. Their macromolecules are so alike
that regulatory mutations may account for their biological
differences. Science, 188(4184), 107–116.
Kollmann, J. (1905). Neue Gedanken über das alte Problem von der
Abstammung des Menschen. Correspondenzbl. Deutsch. Ges.
Anthrop. Ethnol. Urges., 36, 9–20.
Lieberman, D. E., McBratney, B. M., & Krovitz, G. E. (2002). The
evolution and development of cranial form in Homo sapiens.
Proceedings of the National Academy of Sciences, 99(3),
1134–1139.
Lovejoy, C. O., Cohn, M. J., & White, T. D. (1999). Morphological
analysis of the mammalian postcranium: A developmental
perspective. Proceedings of the National Academy of Sciences
of the United States of America, 96(23), 13247–13252.
Minugh-Purvis, N., & McNamara, K. J. (Eds.). (2002). Human
evolution through developmental change. Baltimore: Johns
Hopkins University Press.
Mitteroecker, P., Gunz, P., Bernhard, M., Schaefer, K., & Bookstein,
F. L. (2004). Comparison of cranial ontogenetic trajectories
among great apes and humans. Journal of Human Evolution,
46(6), 679–697.
Mitteroecker, P., Gunz, P., & Bookstein, F. L. (2005). Heterochrony
and geometric morphometrics: A comparison of cranial growth
in Pan paniscus versus Pan troglodytes. Evolution & Development, 7(3), 244–258.
Müller, G. B. (2007). Evo-devo: Extending the evolutionary synthesis. Nature Reviews Genetics, 8(12), 943–949.
O’Higgins, P., & Cohn, M. (2000). Development, growth and
evolution: Implications for the study of the hominid skeleton.
London: Academic Press.
Oxnard, C. E. (1983). The order of man: A biomathematical anatomy
of the primates. Hong Kong: Hong Kong University Press.
Pavlicev, M., & Wagner, G. P. (2012). A model of developmental
evolution: Selection, pleiotropy and compensation. Trends in
Ecology & Evolution, 27(6), 316–322.
Pigliucci, M., & Müller, G. B. (Eds.). (2010). Evolution—The
extended synthesis. Cambridge: MIT Press.
Prabhakar, S., Visel, A., Akiyama, J. A., Shoukry, M., Lewis, K. D.,
Holt, A., et al. (2008). Human-specific gain of function in a
developmental enhancer. Science, 321(5894), 1346–1350.
Richtsmeier, J. T., Corner, B. D., Grausz, H. M., Chevrud, J. M., &
Danahey, S. E. (1993). The role of post natal growth in the
production of facial morphology. Systematic Biology, 42,
307–330.
Schultz, A. H. (1950). The physical distinctions of man. Proceedings
of the American Philosophical Society, 94(5), 428–449.
Schultz, A. H. (1969). The life of primates. New York: Universe
Books.
123
446
Shea, B. T. (1989). Heterochrony in human evolution: The case of
neoteny reconsidered. Yearbook of Physical Anthropology, 32,
69–101.
Slice, D. E. (Ed.). (2005). Modern morphometrics in physical
anthropology. New York: Kluwer Press.
Smith, T. M., Tafforeau, P., Reid, D. J., Grun, R., Eggins, S.,
Boutakiout, M., et al. (2007). Earliest evidence of modern human
123
Evol Biol (2012) 39:443–446
life history in North African early Homo sapiens. Proceedings of
the National Academy of Sciences of the United States of
America, 104(15), 6128–6133.
Somel, M., Franz, H., Yan, Z., Lorenc, A., Guo, S., Giger, T., et al.
(2009). Transcriptional neoteny in the human brain. Proceedings
of the National Academy of Sciences of the United States of
America, 106(14), 5743–5748.