246 Evolutionary Anthropology

BOOK REVIEWS

umes, as well as what one finds in the simple idea that changes in the rate Whither the journals, falls within four major cate- and/or timing of specific developmen- gories, none of which is entirely inde- tal processes can cause many pheno- of Human pendent. First are studies of hetero- typic changes. has been chrony, how changes in the rate and both a boon and a curse ever since it Growth and timing of developmental processes was revived because it is so easily op- lead to evolutionary change. Hetero- erationalized and because it potentially Development? chrony research has a long history in explains how simple mechanisms can paleoanthropology. As is evident from account for large evolutionary shifts. Development, Growth and Evolution: Human Evolution through Develop- According to this framework, descen- Implications for the Study of the mental Change, which is mostly de- dants can differ from their ancestors by Hominid Skeleton Edited by P O’Higgins and M Cohn, voted to this subject, enthusiasm for altering the rate at which specific fea- (2000) Academic Press. 271 p. $79.95 studying heterochrony shows little tures grow, the length of time that they (cloth). ISBN 0-12-524965-9. sign of abating. Second, there has grow, or both. For example, many dif- been a recent interest in heterotopy, ferences cranial shape between humans Human Evolution through the study of evolutionary changes in and chimpanzees arise during ontog- Developmental Change spatial patterning. Heterotopy offers eny because the human brain grows Edited by N Minugh-Purvis and KJ McNamara (Eds) (2002) The Johns an interesting and important alterna- more rapidly and for longer than does Hopkins University Press. 508 p. $59.95 tive to heterochrony, but has barely the chimpanzee brain. Such cases of (cloth). ISBN 0-8018-6372-0. been considered in studies of human more development of a particular fea- evolution. Zelditch’s Beyond Hetero- ture during in a descendant Beyond Heterochrony: The Evolution chrony includes many papers that test than in an ancestor are termed per- of Development heterotopy hypotheses, but none even amorphosis (or hypermorphosis). The Edited by ML Zelditch (ed) (2001) Wiley-Liss. 371 p. $99.95. ISBN 0-471- mentions human evolution, let alone opposite pattern, less development dur- 37973-5. primates. Third, and most prominent ing ontogeny in a descendant than in an of late, is evolutionary-developmental ancestor, is termed pedomorphosis (or These three recent volumes offer an biology, often called “evo-devo,” hypomorphosis). Peramorphosis and opportunity to evaluate current re- which is a partial focus of O’Higgins pedomorphosis are divided into further search in this field, especially in rela- and Cohn’s Development, Growth and subcategories, the most famous of tion to human evolution. After years Evolution. Evo-devo defies a simple which is , a type of pedomor- in which comparisons of adult skele- definition, but mostly concerns the phosis in which the juvenile form of an tal morphology dominated most re- study of the genetic bases for pheno- ancestor is retained in the adult stage of search on hominid systematics and typic shifts. Evo-devo is one of the the descendant. functional morphology, more and fastest growing and most prominent There is no question that hetero- more paleoanthropologists are turn- new fields of biology, largely because chrony is a powerful and often elegant ing to the study of growth and devel- of successes in explaining the regula- way of testing hypotheses about evo- opment to test their hypotheses. A tory bases for the origin of new body lutionary change. Human Evolution large proportion, though not all of this plans (bauplane). It is not surprising through Developmental Change con- research, is driven by the logic that that a number of researchers have at- tains excellent reviews of the assump- phenotypic shifts occur through alter- tempted to apply evo-devo studies tions and mathematical bases that un- ations of processes of growth and de- and, on occasion, approaches to phe- derlie heterochony analyses by D. velopment. It follows that to test hy- notypic shifts in human evolution. Fi- Alba, G. Eble, R. German and S. Stew- potheses about the nature and causes nally, a few researchers, myself in- art, B.K. Hall, K. McNamara, S. Rice, of evolutionary events it is necessary cluded, have been focusing on what and B. Shea. There are also a few good to test hypotheses about the shifts in one might call intermediate mecha- case studies (all of which have been processes of growth and development nistic processes, which lie somewhere published elsewhere in more detail). that generate novel . Put between genetic studies and analyses Perhaps the most interesting is Mc- simply, the goal is to understand the of heterochrony. These approaches, Kinney’s work on the evolution of the processes that underlie the patterns along with papers on methodological brain. McKinney argues that the hu- we observe. issues, are also represented in Devel- man brain, as compared to that of The research presented in these vol- opment, Growth and Evolution. apes, evolved through two major per- So how are we doing? Let us start amorphotic changes. First, more cells with heterochrony, first formulated are allotted to the human brain early explicitly by Haeckel in 1866, and re- in development. Second, human vived almost single-handedly by the growth is characterized by a series of Evolutionary Anthropology 11:246–248 (2002) late Steven Jay Gould’s landmark sequential delays (called sequential DOI 10.1002/evan.10037 1 Published online in Wiley InterScience book, Ontogeny and Phylogeny. Het- hypermorphosis) in general somatic (www.interscience.wiley.com). erochrony analyses are based on the and neural mitosis. These delays gen- BOOK REVIEWS Evolutionary Anthropology 247

other taxa. Fascinating examples are presented in many chapters in the Zelditch volume, including those by Webster and coworkers, Zelditch and colleagues, Guralnik and Kurpius, Roopnarine, and Shapiro and Carl. These and other studies show that het- erotypy is also an important engine of change, even among such closely re- lated species as piranha fish. It will be fun to see such analyses extended more broadly to problems in human evolution, such as the chin. Chins de- Figure 1. Two examples of different ontogenetic vectors in shape space expected between velop, in part, from resorption fields ancestor (black) and descendant species. Left, paedomorphosis (hypomorphosis) versus on the upper alveolar surface of the paeramorphosis (hypermorphosis); Right, heterotopy. mandibular symphysis.3,4 Nonhuman primates lack this growth field, mak- erate longer durations of all develop- is the thorny problem of homology. ing the chin an excellent candidate for mental stages, a larger brain, and a Heterochrony analyses often homolo- heterotopy. larger body mass. In other words, a gize ontogenetic stages, but this can Another especially important devel- few ontogenetically early shifts that be theoretically or methodologically opment, and one that is of major inter- alter many aspects of and problematic, as is evident from analy- est to many biological anthropologists, life history can explain in one fell ses of the age of fossils such as Nari- is the application of three-dimensional swoop many of the differences be- okotome.2 Heterochrony studies also landmark coordinate data and geomet- tween humans (big-brained, big-bod- require the assumption that the mor- ric morphometrics to test alternative ied, and slow-growing) and both phological features one measures are hypotheses of evolutionary change. In chimpanzees and australopithecines homologous, independent units. This (small-brained, small-bodied, and fast assumption has bedeviled many stud- Development, Growth and Evolution, growing). Other interesting reviews of ies, which have failed to dissociate chapters by Spoor and colleagues and the application of heterochrony to hu- heterochronies between integrated re- by O’Higgins provide especially clear man evolution include chapters by C. gions. As Shea points out in Human and useful reviews of three-dimen- Berge and by L’Engle Williams and Evolution through Developmental sional imaging technology and the use colleagues. Change, studies of whether the human of three-dimensional data in geometric The advantages of heterochrony as a skull is globally neotenous are point- morphometrics. While geometric mor- methodology are also potential weak- less because the human skull com- phometric analyses of three-dimen- nesses. Heterochrony research is easy prises several regions that probably sional data are becoming increasingly to do, and if one accepts its assump- have quite different heterochronies. prevalent in the study of human evolu- tions uncritically, then one can always Our brains are obviously peramor- tion, they are not always used in the do analyses that yield results that are photic, but our faces may well be pe- context of explicit hypotheses about interpretable within a heterochrony domorphotic. A consequence of this growth and development. Yet, as Figure framework. All one needs to do is phenomenon is that analyses of inte- 1 shows, ontogenetic vectors from rela- measure some features in individuals grated morphologies can unwittingly tive warp analyses may be used to dis- of ancestor and descendant species of conflate dissociated heterochronies tinguish between heterotopy and het- different ages. (It is best if one knows as, for example, Lieberman shows for erochrony, and even to distinguish the real age and can avoid using size the brow ridge in Development, between some, but not all, of the sub- as a proxy for age). With a little data Growth and Evolution. categories of heterochrony. Applying entry and a smattering of computer A final problem is that while hetero- such a framework to recent geometric time, one can quickly calculate regres- chrony is clearly common, not all evo- morphometric studies in human evo- sion lines for two or more species hav- lutionary change is heterochronic. As lution will be interesting. For exam- ing slopes and lengths that allow one our understanding of developmental ple, the differences in cranial growth to discriminate between peramorpho- processes improves, it is becoming ev- vectors between humans and Nean- sis and pedomorphosis and among ident that other mechanisms, includ- derthals by Ponce de Leon and Zol- their various subtypes. But the devil ing heterotopy (change in place) and likofer5 are most likely explained by lies in several key details and assump- heterotypy (change in type), merit fur- hypomorphosis. tions, which are nicely outlined and ther study. An old-fashioned analysis It is clear that future research on tested in most of the papers in designed to test hypotheses of hetero- growth and development must con- Zelditch’s Beyond Heterochrony. First, chrony will not reveal these other sider alternatives to heterochrony as is one really comparing ancestor and mechanisms. Examples such as part of the normal suite of analytic descendant species? That is not actu- changes in number and identity of approaches. Fortunately, we are en- ally true, for example, in comparisons vertebrae abound in human evolu- tering an era in which we can now of chimps and humans. Second, there tion, but have mostly been studied in frame and test hypotheses about the 248 Evolutionary Anthropology BOOK REVIEWS molecular mechanisms that underlie where,8 have been most explicit about metric morphometrics, is creating the specific heterochronic and hetero- how to do this, and have even, by us- potential to test many fundamental topic shifts. Studies of the relation- ing a scaling function in Adobe Pho- hypotheses and the processes that un- ship between phenotype and genotype toshop, hypothesized the existence of derlie perceived patterns in human in a few model animals (mostly fruit- a that could transform a chim- evolution. But our approaches to flies, zebra fish, and mice) are provid- panzee pelvis into a human pelvis. growth and development need to be as ing an increasingly detailed picture of They may be correct about the pelvis, diverse as the pathways by which the genetic toolkit that animals em- although their hypothesis needs test- growth and development occur. And ploy during development. Three chap- ing. However, their view that pheno- we need to be canny in integrating ters in Development, Growth and Evo- typic evolution is driven almost en- experimental and comparative work lution briefly review the development tirely by selection on genetically because it is almost impossible to of the vertebrate skull (by Schilling determined positional information via study growth and development in the and Thorogood), dentition (Fergusen highly conserved pathways is too re- fossil record. With the exception of and coworkers), and limbs (Cohn and ductionist. As outlined in several teeth, which preserve their own devel- Bright) (see also Shapiro and Carl’s chapters in Development, Growth and opmental history, and a barely tolera- chapter in Beyond Heterochrony). Evolution, most notably those by ble cross-sectional sample of Nean- Readers who are interested in more Skerry and Lieberman, development derthals, students of human growth detail will need to delve further. Per- is not all patterned directly by , and developmental have almost no haps the best of many recent books on but occurs through multiple complex primary data with which to test basic the subject is that by Carroll, Grenier, processes of integration in which nu- hypotheses. Such deficiencies leave and Weatherbee,6 which provides the merous epigenetic interactions occur room for considerable creativity. clearest, most succinct, and lavishly at various hierarchical levels of devel- illustrated introduction to the evolu- opment. A likely result of these com- tion of animal development. plex pathways is that many shifts in Evo-devo is exciting. But it is also phenotype may result from all sorts of REFERENCES true that, for two reasons, the insights interactions between genes or from it has provided about primate and hu- subtle shifts in norms of reaction.9 To 1 Gould SJ. 1977. Ontogeny and phylogeny. man evolution have so far been mod- study these processes, we need to look Cambridge: Harvard University Press. 2 Dean MC, Leakey MG, Reid D, Schrenk F, est. First, most evo-devo research has not only at early embryogenesis, but Schwartz GT, Stringer C, Walker A. 2002. been on a broad evolutionary scale to also at intermediate processes of Growth processes in teeth distinguish modern examine the origin of new body plans. growth throughout ontogeny, the humans from Homo erectus and earlier homi- nins. Nature 414:628–631. Evolution within primates in general fourth of the categories listed earlier. 3 Enlow DH. 1990. Facial growth, 3rd ed. Phila- and within the human lineage in par- These studies should include descrip- delphia: W.B. Saunders. ticular is mostly on the micro-evolu- tions of cellular growth fields and the 4 Lieberman DE. 1999. Homology and hominid tionary scale. We have essentially the effects of mechanical loading on the phylogeny: problems and potential solutions. same basic bauplan as a chimpanzee. skeleton. Perhaps the most exciting of Evol Anthropol 7:142–151. 5 Ponce de Leo´n MS, Zollikofer CP. 2001. Nean- Indeed, it is probably fair to charac- these is the study of dental histology, derthal cranial ontogeny and its implications for terize the subtle regulatory shifts nec- which preserves a spectacular wealth late hominid diversity. Nature 412:534–538. essary to turn a chimpanzee into a of detail about tooth development and 6 Carroll SB, Grenier JK, Weatherbee SD. 2001. From DNA to diversity: molecular genetics and human as tinkering. So far, we know life history (reviewed by Schwartz and the evolution of animal design. Oxford: Blackwell very little about developmental tinker- Dean in Development, Growth and Science. ing in most aspects of phenotype (for Evolution and by Ramirez Rozzi in 7 Jernvall J. 2000. Linking development with exceptions, see Carroll, Grenier, and Human Evolution through Develop- generation of novelty in mammalian teeth. Proc Natl Acad Sci 97:2641–2645. 6 Weatherbee’s chapter 7, and Jern- mental Change). Ultimately, such data 8 Lovejoy CO, Cohn MJ, White TD. Morphologi- vall7). The second problem is that we will help us learn where to focus our cal analysis of the mammalian postcranium: a still know very little about the genetic hunt for key genes. developmental perspective. Proc Natl Acad Sci 96:13247–13252. bases for most phenotypes. Thus, an Research on the evolution of growth 9 Schlichting CD, Pigliucci M. 1998. Phenotypic exciting challenge is to figure out how and development has a come a long evolution. Sunderland, MA: Sinnauer. to apply insights from evo-devo to hu- way since Gould1 inspired massive in- man evolutionary history when we terest in heterochrony. While the de- Daniel E. Lieberman don’t yet know the genes responsible bate over human neoteny gave many Peabody Museum for the morphologies in question. of us a case of “heterochrony fatigue,” Harvard University Cambridge, MA 02138 Lovejoy and colleagues, in Develop- the explosion of new fields and tech- E-mail: [email protected] ment, Growth and Evolution and else- niques, particularly evo-devo and geo- © 2002 Wiley-Liss, Inc.