Research Background

1. Introduction

Secure interpretation of the special case of human origins requires comprehensive study of primate evolution from its earliest beginnings. My research strategy has been based on the conviction that only a wide-ranging approach can yield reliable general principles. I have therefore conducted broad comparisons across primates, covering morphology, palaeontology, behaviour/ecology and reproduction, in all cases combined with investigation of size relationships (allometric scaling). In addition to revealing general principles, this synthetic approach has the special advantage that it can reveal otherwise undetectable relationships, such as the connection between brain size and reproductive biology. Only in this way was it possible to infer that maternal energy turnover played a vital part in the evolution of the human brain.

2. History of Research Career
Several continuing themes in my research originated with my PhD project (1964-67) on behaviour and evolution of tree-shrews (Tupaiidae). This was based on research with K. Lorenz and I. Eibl-Eibesfeldt (Max-Planck-Institut, Seewiesen), supervised by N.Tinbergen (University of Oxford). Tree-shrews were then widely thought to be the most primitive living primates and my initial aim was to study their behaviour as a model for inferring adaptations of the earliest primates. While breeding tree-shrews, I discovered a very unusual pattern of maternal behaviour: the infants are kept in a separate nest and the mother suckles them only once every 48 hours during a very brief visit. This finding not only stimulated my long-lasting interest in reproductive biology (particularly maternal behaviour) but also revealed a stark contrast with the intensive infant care that typifies primates, suggesting that tree-shrews are not in fact related to them. This led me to re-examine the evidence (largely morphological) for inclusion of tree-shrews in the order Primates. Data on size and structure of the brain had been very influential and so I initiated comparative studies of the brain that in turn revealed the pervasive importance of allometric scaling. In my PhD thesis, I concluded that tree-shrews are not close relatives of primates. This conclusion has since been reinforced by several other investigations and tree-shrews are now generally relegated to the separate mammalian order Scandentia. In fact, however, the process of excluding tree-shrews from the order Primates brought the key adaptations of real primates into sharper focus, revealing a very early origin for many key features of human biology.

Following my PhD, I decided to study relatively primitive undoubted primates and obtained a NATO postdoctoral grant (1967-69) to work with J.-J. Petter and A. Petter-Rousseaux (Museum National d'Histoire Naturelle, Brunoy). I made detailed studies of reproductive biology on their unique breeding colony of mouse lemurs while continuing my broad-based work on primate morphology. During this postdoctoral period, with support from the Royal Society (London), I also conducted my first behavioural/ecological field study in Madagascar (1968), including original observations on mouse lemurs. Combined field and laboratory observations indicated that mouse lemurs are in fact a good model for the ancestral primate condition and that several key adaptations can be traced to a small nocturnal ancestor in the "fine-branch niche" of tropical and subtropical forests.

My postdoctoral research was followed by my first university post as Lecturer in Biological Anthropology at University College London (1969-74). In this new post, I continued to work on reproduction of mouse lemurs in a newly founded colony, while simultaneously expanding comparative work on morphology of the skull, brain, postcranial skeleton and reproductive system in primates. I also conducted a second field study of mouse lemurs in Madagascar (1970). During this period at UCL, my interest in allometric scaling grew and I focussed in particular on the size of the brain and its parts. My work also expanded to include studies of primate fossils Ð notably early forms such as Adapis Ð including study of endocasts of the cranial cavity.

At this point in my career, I moved to become Senior Research Fellow at the Wellcome Laboratories, Zoological Society of London (1974-78), where I was responsible for coordinating research on mammalian reproduction. The main projects involved breeding colonies of primates: mouse lemurs, owl monkeys and cottontop tamarins. Owl monkeys are the only nocturnal higher primates and were also of major interest for research on human malaria, so a grant was obtained from the Wellcome Trust to conduct, with A.Dixson, the first detailed study of their reproductive biology. In connection with the projects on primate reproduction, I established a laboratory for hormone radioimmunoassay. This opened up possibilities for conducting hormonal studies on easily-collected urine samples and combining these with studies of behaviour unaffected by sample collection. While applying this to gorillas, I initiated a long-standing research connection with the Jersey Wildlife Preservation Trust, becoming Chairman of the Scientific Advisory Committee in 1975 and a Council member in 1978 (both posts held until 2001). My connection with JWPT (now re-named as the Durrell Wildlife Conservation Trust) strengthened a growing interest in primate conservation biology and focussed it on the topic of breeding endangered species in captivity.

In 1975, I also spent a semester at Yale University as Visiting Professor in the Department of Anthropology. This allowed me to visit several research centres and museums in the USA to study fossil specimens and develop my work on comparative morphology. One significant finding generated by comparative studies of endocasts of fossil and living primates is that brain size has increased over time in all lineages, so humans are in fact distinguished from other primates by an unusually high rate of brain expansion.

In parallel to other studies, I also organised a quantitative radiotelemetric field study of behaviour and ecology of lesser bushbabies in South Africa supported by the Royal Society (1975-77). The fieldwork was mainly conducted by S. Bearder, although I was able to join him for several months in the field. Apart from yielding detailed data on social organization, our observations confirmed my interpretation of the ancestral primate as a small-bodied nocturnal form occupying the fine-branch niche.

From the Zoological Society, I then moved back to University College London for eight years, first as Reader (1978-82) and then as Professor (1982-86) in Biological Anthropology. My primary research became focussed on allometric scaling, particularly concerning the brain. A key development was the inference of a link between metabolic rate and brain size in mammals. The realization that this link must be indirect led to my hypothesis (associating brain size with reproductive biology) that resources provided by the mother have a major influence on the evolution of brain size. This "maternal energy hypothesis" was first published in Nature in 1981 and consolidated in the 1982 James Arthur Lecture on the Evolution of the Human Brain (American Museum of Natural History, New York). It also led to a 3-year project grant (1982-85) from the Medical Research Council (London) to investigate quantitative aspects of brain development and associated reproductive features of primates. In 1983, I spent a semester as Professeur Associe at the Musee de l'Homme, Paris and used this opportunity to study variation in modern human brain size. My interests in fieldwork on primate ecology also continued on a more modest scale during my second period at UCL. Two study visits were made to Brazil with support from the Royal Society (1980) and the British Council (1982-85). In 1981, I was invited to spend 2 months as Senior Visiting Fellow at the Smithsonian Tropical Research Institute, Panama, where I mainly conducted observations on behaviour and ecology of howler monkeys.

In 1986, I moved to take up the post of Director and Professor at the Anthropological Institute in Zurich and built up a range of research activities. The colony of New World monkeys (Callimico, Callithrix, Cebuella) became an important research resource for work on behaviour and reproduction. Major collections of primate specimens are also available for quantitative studies. After moving to Zurich, I finished an advanced textbook, Primate Origins and Evolution (1990), as a synthetic overview arising from my research. Two chapters cover the sense organs and the brain, which played a pivotal r?le in primate evolution. Together with S. Bunney, J.S. Jones and D.R. Pilbeam, I later coedited the award-winning Cambridge Encyclopedia of Human Evolution (1993). For the last eight years of my appointment in Zurich, I was a member of the national committee for biology and medicine of the Swiss National Science Foundation.

In September 2001, I took up my present appointment Ð first as Vice President and then as Provost for Academic Affairs Ð at The Field Museum in Chicago. My responsibilities, with an emphasis on external relationships, are to coordinate research programmes, collections management, contributions to higher education and exhibit-related activities with a team of 40 curators and 60 professional staff in Anthropology, Botany, Geology and Zoology. In parallel to my administrative appointment, I hold the post of Curator in Biological Anthropology.

3. Current Research Interests

A. Allometric Analysis of Brain and Reproduction in Primates
My recent research has concentrated on developing new methods for exploring allometric scaling and using them for comparative study of relations between brain size, reproduction and development. For modern primates, collection and analysis of data on brain size, body size, gestation period, basal metabolic rate and other key factors has been intensified. On the fossil side, the range of specimens covered has been expanded to ensure more effective coverage. Several advances have also been made with respect to methods, including detailed work on potential effects of phylogenetic inertia and development (with A. Barbour and K. Isler) of a novel non-parametric line-fitting technique. Overall, a considerable body of new evidence has been assembled to support the maternal energy hypothesis for brain evolution, with special emphasis on humans. Future work will concentrate on methods of analysis based on exploration of underlying mechanisms in allometric scaling.

B. Inferring Divergence Times in the Primate Tree
In 1985, I suggested that, because time of origin is commonly dated from the earliest-known fossil representative, the very fragmentary nature of the primate fossil record must lead to serious underestimation of divergence times. This suggestion, subsequently backed by initial calculations in an invited review article for Nature (1993), has been challenged by some palaeontologists. A novel statistical approach developed (in collaboration with S. Tavare, O. Will., C. Soligo and C. Marshall), has confirmed and expanded the original conclusions The inference that times of origin in the primate tree are far earlier than commonly believed is supported by recent studies of molecular evidence using divergence dates based on more reliable criteria. This has implications for dating times of origin throughout the primate tree, including hominid origins.

C. Reproductive Biology and Evolutionary Relationships of New World Monkeys
Goeldi's monkey (Callimico) occupies a special place in New World monkey evolution, showing features of both main families (Cebidae, Callitrichidae). I therefore initiated a long-term research project on its behaviour, reproduction, physiology and endocrinology. Fundamental work on reproduction (with C.R. Pryce, M. Jurke, A. Dettling) was supported by a grant from the Swiss National Science Foundation (1990-95), permitting detailed behavioural/endocrinological characterization of the female cycle, mating, pregnancy and development. Re-analysis of the relationship between Callimico and other New World monkeys revealed that it is closer to Callitrichidae than to Cebidae. In fact, later analysis of mitochondrial DNA sequences and other molecular data (with J. Pastorini, M. Forstner, D. Melnick) revealed that Callimico is probably nested within the Callitrichidae and not a basal offshoot as had originally been concluded. Just recently, the basal metabolic rate of Callimico was measured for the first time (with M. Genoud, G. Anzenberger, N. K?lin), showing that it is relatively low as in other callitrichids.

D. Conservation Genetics of Barbary Macaques
The Barbary macaque (Macaca sylvanus) is a valuable test case for primate conservation biology because the wild population is small and fragmented and because it is relatively easy to sample all existing wild and captive populations. A detailed study of behaviour and ecology of this species was conducted in Algeria by A. Gautier-Hion and N. M?nard (University of Rennes) and in 1990 a team from the Anthropological Institute (W. Scheffrahn, F. von Segesser, J. Pastorini and myself) was invited to initiate genetic work. This progressed from protein electrophoresis through multilocus DNA fingerprints to microsatellites and the range of samples was gradually expanded to include Morocco and captive colonies. We also set up our own project with the isolated colony of macaques on Gibraltar, including studies of behaviour and ecology as well as genetics. Work using microsatellites and mitochondrial DNA to investigate the complete set of samples was funded by a grant from the Swiss National Science Foundation (1993-2001). Interim results have already thrown new light on reduction of genetic variability through habitat fragmentation. In a recent development, the Gibraltar Barbary Macaque Project was formally established as a programme of collaboration between the Gibraltar Ornithological and Natural History Society, the Gibraltar Veterinary Clinic, the German Primate Centre (G?ttingen) and The Field Museum.

E. Field Studies of Behaviour and Ecology of Madagascar Lemurs
Over an eight-year period, several long-term studies of behaviour and ecology of five different lemur species were conducted in Madagascar by investigators from the Anthropological Institute in Z?rich. Projects covered the mongoose lemur (PhD, D. Curtis), the Alaotran gentle lemur (PhD, T. Mutschler), the thick-tailed dwarf lemur (PhD, A. M?ller), a comparative study of the sportive lemur and the woolly lemur (postdoctoral study, U. Thalman) and an overall, multi-level analysis of phylogenetic relationships among lemurs using mitochondrial DNA sequence data (PhD, J. Pastorini). Although I guided and coordinated these studies, the primary impulse came from a highly motivated group of students. The overall strategy was to focus on previously little-known lemur species showing particular features that are of theoretical importance. The mongoose lemur and the Alaotran gentle lemur, in common with a few other lemur species, show an unusual pattern of activity including both diurnal and nocturnal episodes (cathemerality). The long-term data collected show that in both species the pattern of cathemerality varies seasonally and that existing hypotheses do not explain it. The thick-tailed dwarf lemur is of special interest among primates because it hibernates for up to seven months, while comparison between the sportive lemur and the woolly lemur is particularly instructive because these two species are folivores of similar size yet show marked differences in ranging and social behaviour. Social organization is of interest for all five species, especially because three of them (mongoose lemur, thick-tailed dwarf lemur, woolly lemur) have now definitely been shown to be monogamous, thus throwing valuable new light on this social pattern.

4. Conclusion: From Primate Ancestry to Human Origins
Homo sapiens is one of some 350 living primate species and the evolution of this entire group provides the general context for the special developments in human origins. Wide-ranging comparative studies of many species and characters generate valid general principles and yield a sound foundation on which to base specific interpretations of human origins and evolution. At the same time, it has become clear that urgent action is needed to conserve our primate relatives.

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