Tribute to Percy Milton Butler 1912–2015

Percy Butler could be regarded as the champion of the study of mammalian teeth. In fact in his very long scientific career, he published many papers not only on modern and fossil mammalian dentitions, including those of humans, but also on the cranial and postcranial regions of extinct mammals. Moreover, his works also included the study of modern ecology, especially of insects, a field for which he is less well known, at least among palaeontologists. He always regarded himself as a zoologist, rather than as a palaeontologist, although his contributions to the field of mammalian palaeontology are recognized by palaeomammalogists to have been immense. He duly received Honorary Membership (1994) and the prestigious lifetime achievement award, the Romer-Simpson Medal (1996), from the Society of Vertebrate Paleontology. Dentists likewise appreciated his human tooth studies. Thus, he received the Certificate of Appreciation from the Zoller Memorial Dental Clinic, University of Chicago (1966); Membre d’Honneur (certificate and medal) of the Groupement International pour la Recherche Scientifique en Stomatologie (1971); and La Médaille de la Ville de Paris (1986). Very early in his career (1937), he was awarded Membership of the Society of Sigma Xi, devoted to the Promotion of Research in Science.

I first met Percy in the late 1960s on one of his many study visits (which he told me began in 1933) to the Natural History Museum, London (then British Museum (Natural History)), where I had recently begun employment in the junior post of Scientific Assistant in the Fossil Mammal Section. I found him more ready than most of his contemporaries, whom I hosted, to discuss his work with me on an equal basis. He did not react negatively to my wild ideas, but offered sound advice. I first became interested in early perissodactyls and I was stimulated especially by his papers on occlusion and premolar molarization in the group (Butler 1952a, 1952b). What I learned from him has fuelled and influenced much of my research ever since.

He gained a BA degree at Pembroke College, Cambridge and a B.Sc. in Zoology at London University (external), both in 1933. In 1936, he visited the U.S.A., having received a Commonwealth Fund Fellowship at Columbia University, to study fossil mammal teeth in various museums. While in the country, he collected some fossil mammals, including a molar of the large Late Eocene brontothere Megacerops. He gained his Ph.D. in 1939 at the University of Cambridge under the supervision of Clive Forster Cooper. During the Second World War, he applied his knowledge of insects in the Infestation Division of the Ministry of Food, where the work involved entomological inspection of ships and examinations of a wide variety of food storage and manufacturing premises in Northern Ireland. An account was published joint with A.F. O’Farrell in 1948. He then lectured at Exeter and Manchester Universities before joining Royal Holloway College in Egham, Surrey, (now part of the University of London) in 1956 as Reader and Head of the Department of Zoology. After retiring in 1972, he retained his position at Royal Holloway as Emeritus Professor in the Department of Biology for the next 43 years (Figure 1).

Figure 1. Percy speaking on the occasion of his 100th birthday party at Royal Holloway, University of London, 19 July 2012. Source: Photo courtesy of Christopher Dean.

In the 1930s, Percy was at the forefront of research into understanding how mammalian teeth evolved, in particular their character development, cusp homology and dietary function. For twenty-first Century palaeomammalogists, it is hard to appreciate that the developmental relationships between milk teeth, premolars and molars, primary cusp identification and knowledge of the process of mastication through observation of wear facets had not at that time been firmly established. These are all phenomena that we accept today and rely upon to build more elaborate hypotheses and apply to phylogeny and ancient dietary reconstruction. A series of observationally meticulous and clearly argued papers in the late 1930s to early 1950s pioneered these studies. Detailed comparison of the morphology of adjacent teeth led him to propose his field theory, which regarded a mammalian dentition as a metamerically arranged organ, like the vertebral column (Butler 1937, 1939a). Together with physiological, embryological and genetic arguments, he showed the unlikelihood of teeth evolving individually and independently of one another, as frequently held in the nineteenth and early twentieth Centuries (e.g. Cope 1885; Gregory 1934). He used this to justify the homologizing of cusps in adjacent teeth ‘provided that the transition from tooth to tooth is sufficiently gradual to make comparison possible’ (Butler 1937, 127–128). He recognized that simplification of structure occurred both anteriorly and posteriorly of the most complex tooth in the row, which he called the ‘anticlinal tooth’ (usually in the range DP4-M2: Butler [1937, 130]). Thus, a gradation of form could be observed along a tooth row, responding in embryonic development to the presence of morphogenetic fields (Butler 1939a). In 2001, he had lived long enough to publish a review of the theories that had been proposed subsequently, through embryological and genetic research, on the causes of differentiation of the dentition as described by his field theory (Butler 2001a).

Percy’s mammal tooth work began with what was then known as the placental order Insectivora, as their molars appeared the least modified and therefore suitable for studying dental evolution. In 1948 he published a comprehensive paper on the teeth and skulls of modern and fossil hedgehogs. It is a sound, important work still regularly cited today. As time went on it became clear to him that insectivorans were not just primitive and that they included quite differently specialized types. They were a ‘wastebasket’ group that today we categorize as paraphyletic and polyphyletic. He played an important role in splitting them up into their component natural monophyletic groupings. Thus, we now recognize, amongst others, elephant-shrews (order Macroscelidea), which he named (Butler 1956c), and tree-shrews (Scandentia), to which he gave ordinal status (Butler 1972a). These groups are no longer considered close relatives of hedgehogs, moles and shrews (core insectivorans in the order Lipotyphla), and are as phylogenetically remote from one another as monkeys and elephants. He also took on the task of describing mainly the smaller mammals (insectivorans and bats) that were being collected from Neogene rocks in East Africa by Louis Leakey in the 1950s and 1960s, at times co-authoring with Marjorie Greenwood and Arthur Tindell Hopwood.

His meticulous examination of teeth led him to realize that they did not function as pestles and mortars as many of his early contemporaries thought, but, especially in the case of premolars and molars, had complex patterns of mastication. Thus, he began studying dental occlusion and the wear facets produced by dietary wear (Butler 1952a, 1961, 1972b). He noted (Butler 1961, 117):

It is possible to trace homologous wear-facets through a variety of molar teeth, just as it is possible to trace homologous cusps. In fact, wear facets and cusps are intimately related: a cusp can be identified from the wear facets on its surfaces.

He also numbered the wear facets (Butler 1952a). His work began with fossil members of the order Perissodactyla and he subsequently applied it to many different groups, including rodents, primates and extinct Mesozoic orders.

Insectivorans led Percy on to studying the earliest mammals of the Mesozoic Era, in a quest to understand the first stages of mammalian evolution. His earliest studies of modern insectivorans involved the tenrecs of Madagascar, which have a particularly simple molar structure known as zalambdodont. He realized that zalambdodonty and many other types of molar structure had evolved independently multiple times. He was particularly impressed by the amount of evolutionary convergence of form that existed in nature, especially as demonstrated by the fossil record. This made him rather suspicious of cladistic methodology, which had its biggest impact in the scientific community relatively late in his career. He felt that there was too much convergence for successful phylogenetic resolution through cladistic analysis. At the height of the cladistics controversy period in the 1970s, in response to a question on his talk at a scientific meeting, he once joked that multituberculates were ‘another subgroup of the Chelonia’. This reflected the initially rather coarse codings of characters used by cladists, early in the development of the field, leading to a proposed relationship between dicynodonts and turtles. Nevertheless, he did use non-computerized cladistic-style analysis of the insectivores in 1988 (Butler 1988a). In any case, what is most important in modern phylogenetic analysis is the reliance on derived characters, which early on he saw as key to classifying the Insectivora. Thus, he realized that they were an unnatural group based on primitive characters and recognized the need to split them into several individual orders (Lipotyphla, Scandentia, Macroscelidea) based on derived characters (Butler 1972a).

He continued to pursue his Mesozoic studies, including co-authoring with his late colleague Zofia Kielan-Jaworowska. Early in his career, Mesozoic mammals were exceptionally poorly known, the best being jaws and teeth from the U.K. middle Jurassic and early Cretaceous, the North American late Cretaceous and some cranial material from the late Cretaceous of Mongolia. Since those early years, the rate of new finds of Mesozoic mammals and their quality rose exponentially from all parts of the world and he kept abreast of such developments, modifying his ideas accordingly.

Significant predictions made by Percy have been shown subsequently to be correct. In 1973, he and Zofia (Butler & Kielan-Jaworowska 1973) suggested that a Cretaceous supposed placental insectivoran from Mongolia, called Deltatheridium, based on rather poorly preserved material, might instead be a marsupial. A quarter of a century later, much more complete and better-preserved specimens showed that this animal was indeed a stem marsupial (Rougier et al. 1998). In 1978, he concluded that another Cretaceous supposed placental from Texas, called Pappotherium, and known from little more than a few isolated teeth, was also a marsupial. He based this on the recognition that there were four different upper molar morphologies, indicating the marsupial number (primitively) of four molars rather than the three expected in a placental. The metatherian (i.e. stem marsupial) nature of Pappotherium has also been corroborated by more recent work (Davis & Cifelli 2011). A group of very early mammals, mainly from the late Triassic and early Jurassic, called haramiyids, had been enigmatic since their discovery in the early nineteenth Century, as they consisted only of isolated molariform teeth that were unlike those of any modern mammal. Thus, it was unclear which were upper and which lower teeth, and also which was front versus back and which were from left versus right sides. In a joint paper with Giles MacIntyre in 1994, Percy worked out how the teeth functioned during chewing by looking at the wear facets and thereby reconstructed the dentition. Three years later, haramiyid jaws with teeth were discovered in Greenland (Jenkins et al. 1997), which showed Percy’s reconstruction to be fully accurate, which pleased him no end.

Percy published more than 100 papers and book chapters and co-edited one book in his long publishing career. His first paper was in 1935, co-authoring on the ecology of Bardsey Island in Wales. His publications currently span a remarkable 82 years, the last posthumous one being on Bathonian triconodonts in 2016 joint with Denise Sigogneau-Russell. There is also still one co-authored manuscript in preparation. The impact of Percy’s work on the way we study teeth today has been immense. He was an unassuming person, but with a sharp wit, friendly and ready to share his ideas and listen to the ideas of others. In 1986 he told me he attributed long life to drinking tea and smoking a pipe. It feels like the end of an era.

Disclosure statement

No potential conflict of interest was reported by the author.

Acknowledgements

I thank Graham Twigg and David Polly for providing important information, Gregg Gunnell for helpful comments and Chris Dean for the photograph.