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American Journal of Physical Anthropology 165.4 (2018): 834-854

DOI: http://doi.org/10.1002/ajpa.23357

Copyright: © 2018 Wiley Periodicals

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Page 1 of 61 American Journal of Physical Anthropology
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3 Human life course biology: A Centennial Perspective of scholarship on the human
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5 pattern of growth and capacity for culture.
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8 Barry Bogin1, Carlos Varea2, Michael Hermanussen3, Christiane Scheffler4
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11 1 School of Sport, Exercise & Health Sciences, Loughborough University LE11 3TU
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UK [email protected] TEL: [phone]
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16 2 Physical Anthropology Group, Department of Biology, Universidad Autónoma de
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Madrid, Madrid, Spain [email protected]
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3 Aschauhof 3, 24340 Altenhof, Germany, [email protected]
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4 Universität Potsdam, Institut für Biochemie und Biologie, Maulbeerallee 1, 14469
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27 Potsdam [email protected]
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30 Corresponding author: Barry Bogin
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33 Number of text pages – 32
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35 Figures – 4
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Tables – 4
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Key Words: Life History, Childhood, Adolescence, Menopause, Senescence
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44 Word count, main text: 9,629
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American Journal of Physical Anthropology Page 2 of 61
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3 The great lesson that comes from thinking of organisms as life cycles is that it is the
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5 life cycle, not just the adult, that evolves (Bonner, 1993, p. 93).
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8 We structure our Centennial Perspective on human life course biology in the
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following manner: 1) the discovery of the interplay between evolutionary processes
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with physical growth and development; 2) the recognition of novel features of human
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15 growth and development, and several ways these may be organized into a
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17 continuum of ontogenetic events; 3) evidence that the human life course biology
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19 establishes the foundation for the capacity for human culture and biocultural
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reproduction; 4) the interactive nature of human life course biology with the social,
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economic, and political environment. Our essay is not an exhaustive review, rather it
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26 highlights critical research and scholarship, emphasizes articles published in the
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28 AJPA and the Yearbook of Physical Anthropology, and mentions research by the
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authors where appropriate (‘all is vanity’ Ecclesiastes 1:2).
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Part 1: The interplay between evolutionary processes with physical growth and
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development
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38 Evolution and growth
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40 Ever since Darwin (Gould, 1977) we know natural selection is one of the mechanisms
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shaping biology. Ever since Dobzhansky we know that, “Nothing in biology makes
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sense except in the light of evolution” (Dobzhansky, 1973). The pattern of human
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growth makes sense when illuminated by evolution, especially the twin engines of
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49 natural selection – differential fertility and mortality. Other mechanisms of evolution,
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51 mutation, migration, genetic drift, epigenetic assimilation (Waddington, 1957;
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Hallgrimsson et al., 2002; Fuentes, 2010; Bogin, 2013), and sexual selection (Gray,
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2013), also play their roles. Today we study human growth in the context of life
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58 history theory -- the study of the evolution and function of life stages and of behaviors
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Page 3 of 61 American Journal of Physical Anthropology
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3 related to these stages (Bogin and Smith, 1996, 2012; Kaplan et al., 2000; Varea and
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5 Bernis, 2013). The life history of a species may be defined as, “Ithe evolutionary
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adaptations used to allocate limited resources and energy toward growth,
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maintenance, reproduction, raising offspring to independence, and avoiding death”
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12 (Bogin, 1999, p.154). Life history patterns of species are often a series of trade-offs
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14 between growth versus reproduction, quantity versus quality of offspring, death
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16 sooner or later after reproduction and other biological possibilities given the limited
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time and resources available to all living things (Stearns, 1992; Charnov and
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Berrigan, 1993).
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23 Humans share some life history characteristics with other relatively large and long-
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25 living mammals. Other such species, weighing more than 30 kg and known to have
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lived 50 or more years in the wild or captivity, are elephants, whales, Baikal and
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Caspian seals, dugongs, orangutans, gorillas, and chimpanzees, bonobos and the
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32 light weight exception (<4 kg), the white-throated capuchin monkey
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34 (http://www.earthlife.net/mammals/age.html). Notable characteristics of species with
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36 longevity potentials of 50+ years is that they live in social groups, most are known to
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use tools (not reported for seals, bats or dugongs), and have relatively large brains.
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They also have slow life histories, taking a relatively long time (years vs. months) to
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43 grow from birth to reproductive maturity. These features and life history traits are the
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45 result of biological selection for age-related and sex-specific trade-offs in adaptations
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to habitats and ecological niches (see Table 1 for a list of life history biology traits and
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trade-offs).
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52 Table 1 about here
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54 Humans have one additional adaptive trait - culture. We define human culture as
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56 having three equally important components: 1) technology, 2) sociology, 3) ideology,
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a trilogy of terms from Leslie White (1949), but with the needed modifications in
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American Journal of Physical Anthropology Page 4 of 61
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3 meaning and biological rigor as provided by Henrich and Henrich (2007), Boyd and
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5 Richerson (2009), and other contemporary theorists of culture. Medium- and long-
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lived mammalian species may have elements of technology (tool use, tool
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manufacture), sociology (live in social groups, cooperate in feeding or offspring care),
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12 or both. Only the human species, so far as we are aware, has ideology, which
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14 includes symbolic language, religion, marriage and formal kinship systems, with kin
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16 terminology and its associated behavioral obligations. We do not debate here when
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and where human culture appeared in the 6-7 million years of evolutionary history
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since hominins diverged from other primate lineages. Rather, our purpose is to
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23 demonstrate a few of the ways in which the human capacity for culture is inextricably
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25 linked with the human species-specific pattern of life course biology.
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The inseparable biocultural nature of the human species is its primary evolutionary
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engine. Dobzhansky, once again, stated this most clearly, “Iit is precisely because
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32 we know that [humankind] changes so greatly culturally that we can be so confident
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34 that it changes to some extent also geneticallyI The potentialities for rapid evolution
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36 of the human species have not been depleted, since the environment continues to
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change and the genetic variance remains plentiful. [Humankind] assuredly continues
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to evolve, both culturally and biologically (Dobzhansky, 1963, p. 147, ‘humankind’
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43 substituted for the original ‘mankind’).
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Growth and evolution
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The study of biological growth in relation to evolution has a venerable history. D’arcy
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52 Thompson (1860-1948) used mathematics and principles of mechanics to show in a
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54 formal and scientific manner the physical and geometrical constraints on
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56 developmental biology (Thompson, 1917). Thompson took issue with natural
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selection as the only force of evolution and as the primary ’lathe of evolution’, that is,
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Page 5 of 61 American Journal of Physical Anthropology
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3 the process that shapes biological form to any functional adaptation. Instead, some
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5 biological forms derive from simple mechanical rules. The hexagonal shape of
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honeycomb chambers of the bee hive, for example, is the shape that minimizes
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surface area to volume ratio. Charles Darwin (1809-1882) thought that the
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12 honeycomb is the product of natural selection operating on the genetic basis of the
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14 bees’ behavior, but Thompson showed that the shape results simply from the
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16 process of individual bees putting globe-shaped cells together. The hexagon shape
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results from the minimization of the forces of compression and strain on each cell
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(Hales, 1999). There is no selection on the bee’s genetic basis of behaviour for
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23 hexagon construction; highly similar boundary shapes are created in a field of soap
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25 bubbles. Thompson further supported his mechanical explanation by noting that
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queen honey cells, which are constructed singly, are irregular in shape with no
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evidence of efficiency.
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32 A human example of biological development which requires no natural selection is
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34 the growth in size and pattern of gyrification (folding) of the human fetal brain. The
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36 human brain is relatively large for total body mass and is already so at birth (Varea
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and Bernis, 2013; Bogin and Varea, 2017). The surface of the fetal brain is initially
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smooth and then folds as it grows. This is mechanically efficient as a folded structure
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43 can occupy a smaller space than if that same structure were flat or smooth. Much
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45 research focuses on the genetic and molecular determinants of growth in size and
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the pattern of gyrification of the human brain. A recent article, however, shows that
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pattern of gyri formation of the human fetal brain, “Iis an inevitable mechanical
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52 consequence of constrained cortical expansionI” (Tallinen et al., 2016, p. 591). The
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54 authors built a layered 3D-printed gel mimic of a pre-folded human fetal brain based
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56 on magnetic resonance images of real brains. The mimic was immersed in a solvent
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American Journal of Physical Anthropology Page 6 of 61
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3 that caused outer layer to swell relative to the inner layer, replicating the actual
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5 process of cortical brain growth. The relative expansion of the ‘cortical’ layer induced
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mechanical compression and led to the formation of sulci and gyri like those in actual
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fetal brains. This process was repeated via numerical simulations and the results
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12 were essentially identical. The authors do not rule out a role for natural selection to
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14 influence the functional coordination of brain regions that are in close physical
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16 proximity, but they conclude that, “Ithe size, shape, placement and orientation of the
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folds arise through iterations and variations of an elementary mechanical instability
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modulated by early fetal brain geometry” (p. 588) – in other words, this is the way that
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23 brain tissue bends when squashed against the inside of the skull. In his book On
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25 Growth and Form, Thompson provided similar examples of purely mechanical folding
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in biology and in pastry cooking (pellets of dough, 1917, p. 84).
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Thompson also demonstrated that differences in body shape and size between
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32 adults of various closely related species may be due to differences in growth rates
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34 from an initially highly similar embryonic or newborn form. For this he used the
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36 system of Cartesian transformational grids. Thompson included examples of primate
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growth and perhaps the most well-known is his transformational grid illustration of
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age changes in the chimpanzee and human skull from between birth and adulthood
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43 (Figure 1).
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45 FIGURE 1 ABOUT HERE
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In these cases, Thompson visualized the force of natural selection to bring about new
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patterns of growth and development. Per Figure 1, selection was for large canine
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52 teeth for the chimpanzee versus selection for a larger brain for the human. Thompson
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54 anticipated the powerful impact of data visualization, which became more readily
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56 available to science with the advent of digital computers. The publication of On
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Growth and Form celebrated its own centennial in 2017
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3 (https://www.ongrowthandform.org/news/). The book remains in print and continues
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5 to inspire biologists, mathematicians and philosophers.
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One inspired scholar is John Tyler Bonner (1920- ), whose 1965 book Size and Cycle
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was an homage to Thompson’s early 20th century work on growth and form. The
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12 book also synthesized the evolution of growth in size and shape with life cycle
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14 biology. Bonner’s essential observation was that, “Evolution [is] the alteration of life
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16 cycles through timeI” (Bonner, 1965, p. 3). Biologists may define species by the
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adult (reproductive) morphology, such as the anatomy of an adult dog, chimpanzee,
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or oak tree. But, each species is distinct from the moment of fertilization, through its
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23 life cycle and even after death as a carcass of fallen tree. The ‘dog’, ‘chimpanzee’, or
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25 ‘oak tree’ are, in fact, the entire life cycle of the organism. Bonner understood that the
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life cycle of each species is part of its adaption to the physical and biological
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environment, or more accurately the ecological niche, which is composed of nonliving
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32 objects as well as other life cycles. The life cycle of the human species is both
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34 adapted to the human niche and, due to our biocultural nature, allows people to
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36 modify the niche to enhance adaptiveness, measured in fertility, longevity, material or
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social complexity, and ideological productivity.
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The human life cycle is derived from mammalian, especially primate, ancestors. This
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43 ancestry places some Thompson-like constraints on how much natural selection can
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45 modify ancient patterns of growth and development. The transformational grids of
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Figure 1 are an example of constraint under selection, that is, retention of nearly
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identical skeletal-dental components in adulthood, despite change in size and shape,
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52 due to the shared ancestry of chimpanzees and humans.
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54 Primate growth and evolution
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known from the 19th century, but the systematic study of primate growth and
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American Journal of Physical Anthropology Page 8 of 61
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3 development in relation to human evolution began with the work of Adolph Schultz
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5 (1891-1976). Schultz (1924) published in the AJPA the article ‘Growth studies in
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primates bearing upon man’s evolution.’ A year earlier, Schultz published in the AJPA
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a detailed analysis of human fetal growth (Schultz, 1923) and two year later
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12 expanded this topic to include non-human primates (Schultz, 1926). These articles
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14 are primarily a descriptive mix of Schultz’s quantitative and qualitative assessments
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16 of primate ontogeny, based on careful measurement and dissection of cadavers of
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fetuses, neonates, immatures, and adults. Schultz does not cite On Growth and Form
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in these articles, but he summarizes his analysis with the Thompsonian statement
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23 that, “Ithere will remain the forcible conclusion that the many striking resemblances
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25 between man, ape, and, monkey in early development, and their frequently closely
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corresponding growth changes can only be explained by one common origin, from
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which they all inherited the tendency for the same ontogenetic processesI” (p. 163).
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32 In later publications in the AJPA and elsewhere Schultz (Schultz,1935, 1960, 1969)
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34 pioneered the analysis of dental maturation and tooth eruption timing as life history
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36 markers. Before Schultz, there are publications by Wilton M Krogman (1903-1987) on
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the eruption of teeth in Old World monkeys and apes (Krogman, 1930). He reported
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that the first permanent molar (M1) is always the first of the permanent teeth to erupt
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43 in all the primates studied. Krogman also discovered that humans take about three
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45 times longer than non-human primates to progress from M1 to M3 eruption.
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Anecdotal evidence had led Arthur Keith (1866-1955) and Solly Zuckerman (1904-
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1993) to incorrectly report that apes and humans were nearly identical in the timing of
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52 dental eruption. Finally, Krogman also seems to be the first anthropologist to report
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54 that the correlation between, “Iepiphyseal union with tooth eruption indicates that
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completed in shorter time” (1930, p. 312). Krogman’s discovery of: 1) the primacy of
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3 M1 eruption in all primates, 2) the significant human delay in molar eruption
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5 sequence, and 3) the overall delay in skeletal maturation of humans were major
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findings that became the basis of all life history research with living and extinct
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primate species (Smith, 1991).
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12 By 1924, in the AJPA, Schultz was using the words embryonic, fetus, newborn,
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14 infant, juvenile, and adult as names for distinct stages or phases of primate growth
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16 and development. He used the words ‘child’ and ‘children’ to denote human pre-
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adults of any age. The word ‘adolescence’ is mentioned one time in 1926 (Schultz,
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1926). Schultz does not define clearly any of these stages of development, rather the
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23 words are used as if the reader understands the meaning. He does state (1935) that
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25 eruption of the first permanent teeth, most often the M1, indicates the end of the
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infantile period and, presumably, the start of the juvenile period.
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The use of these names for developmental stages became more formally associated
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32 with the timing of permanent molar eruption when Schultz published his well-known
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34 illustration of comparative primate life history (Schultz, 1960). In this figure, Schultz
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36 defines the Infantile Period from birth, “Ito the first permanent teeth”, the Juvenile
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Period, “Ito last permanent teeth”, and the Adult Period, “Ito end of mean
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longevity”. More detailed technical definitions of mammalian life course stages were
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43 published in the 1960s and we discuss these later in this article. Schultz’s 1960 figure
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45 is widely copied (Lovejoy, 1981; Smith, 1992; Bogin, 1999; Leigh, 2001). The original
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included a speculative column on the life periods of ‘Early Man’ and is so doing firmly
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established the use of molar eruption sequence in the study of the evolution of
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52 human life course biology.
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