Mammal Societies
Tim Clutton-Brock
2016
Wiley-Blackwell (Oxford, UK)
744 pp
ISBN 97811119095323
“The key to the sociobiology of mammals is milk.” E.O. Wilson (1975)
Reviewed by Clara B. Jones (2016; revised 2020)*
Knowledge about group-living mammals may contribute to an understanding of vertebrate social evolution and the evolution of gregariousness in animals with generalized phenotypes [specialization being a signature of high "grades" of social evolution (specialization, reproductive division-of-labor]. Compared to social insects and birds, the social biology of mammals is poorly known with the exception of ungulates, carnivores, and primates (3 of ~25 Orders). Among many similar papers in the mammalian literature on Social Paleontology, in 2011, Ladevèze et al. reported fossil evidence appearing to document mammalian gregariousness and its associated ecology from the basal Tertiary of Bolivia. These findings suggested that extinct, marsupial-like Pucadelphys andinus were group-living, probably exhibiting frequent interactions, strong sexual dimorphism, and male-male competition, as well as, polygyny. Based on the spatial and ecological settings of their specimens, as well as, the climate, in addition to, physical and situational associations and patterning of adult, sub-adult, and juvenile remains in their sample, these authors speculated that the species may have been "social" [gregarious]. In 2012, employing phylogenetic analyses, Briga et al. showed that relatedness and allomaternal¹ care are positively correlated in Class Mammalia. These papers indicate that, though the population dispersion of most extant mammals is sexually segregated (“solitary”) and though fossil remains cannot definitively preserve Behavior, group-living may have a long history in this Class (also see Jones 2014, Table 3.1, pp 19-25).
Tim Clutton-Brock (henceforth, “TC-B”) is a highly-regarded empiricist at the University of Cambridge (UK), recognized, particularly, for his field studies on primates, red deer, and meerkats. He is a prolific scientist with a knack for asking good questions and choosing animal models that have yielded flagship research. The author will be familiar to most animal behaviorists and behavioral ecologists as a specialist of cooperative breeding and evolutionary aspects of reproduction (e.g., female mating strategies, sexual selection). In the book under review, TC-B notes that his undergraduate training was in Anthropology and that he completed his doctorate under Robert Hinde, an animal behaviorist that Psychology typically claims as one of its own. I have been familiar with TC-B's work since the 1970s, and my personal favorites among his copious publications are his 1995 paper with Geoff Parker and the 2003 volume edited with R.M. Sibley & J. Hone. I am pleased to have the opportunity to review Mammal Societies. I have interacted with TC-B on several occasions, once face-to-face, and, more than once, via e-mail. He has always been generous and courteous to me.
Previous books by JH Crook, “Griff” Ewer, J Eisenberg, EO Wilson, R Estes, D MacDonald, CB Jones, and others, have treated mammalian social biology to one degree or another. Mammal Societies, however, is the first attempt to provide a comprehensive literature review of the topic. The publisher's description of the volume states that it is intended for “behavioral ecologists, ecologists, and anthropologists,” and TC-B self-identifies as a “behavioral ecologist.” The book is, to all purposes, a literature review emphasizing publications on Old World taxa [a tradition attributable, in particular, to Primatology]. While the Table of Contents presents a detailed outline of topics of interest to social biologists, the book is not organized using ecological [e.g., JH Crook] or evolutionary models [e.g., the "major transitions"]. To provide context, professors using Mammal Societies as a course textbook or reference work are strongly advised to acquaint their students early on with Wilson's (1975) treatment (pp 456-574) presenting an explicitly articulated conceptual framework for mammalian social biology, including, trends, conventional terminology, general and comparative features in the Class, an extensive glossary, as well as, case studies and summary tables, figures, and diagrams. John Eisenberg's [1981], "mammalian radiations," is, also, an invaluable source of information on mammalian patterns, including, behavior, as well as, mating & group architectures.
Chapter 1, “Social evolution,” omits definitions of terms the first time they appear in the book (e.g., “aggregation,” “social”, “cooperation”), leading to obfuscation throughout, particularly, since there is no discussion of how to measure social traits (cooperation, altruism) and to discuss their pertinence to reproductive success. In this chapter, the author might have defined “Mammal” and should tell the reader why mammalian social biology is of import. The reader will want to understand possible trajectories to cooperation and altruism from aggregations to group-formation to group-maintenance and how the (spatial and temporal) distribution of limiting resources favor or disfavor the evolution of mammalian sociality. Chapter 1 is, in great part, a selective account of the history of Animal Behavior combined with some mention of theoretical issues (e.g., Darwinism, competition, reciprocity, game theory). However, for rigorous discussions of verbal and quantitative theory in Behavioral Ecology, as well as, overviews of Methods and G x E interactions, readers are referred to Davies et al. (2012) and Westneat & Fox (2010).
Chapters 2-9 address topics related to features of female behavior, particularly, as they pertain to mating, maternal tendencies, and gregariousness. Focusing on females, their strategies, and their energetic requirements as the primary driver of group-living and patterns of male behavior and dispersion is fundamental to an understanding of mammal societies because fertilizable females are a limiting resource for males and, subsequently, an ultimate determinant of male “fitness." Though these and other important concepts are implicit in some of TC-B's discussions, explicit use of many principles inherent to Behavioral Ecology are unclear or lacking (e.g., integration of Hamilton's rule [rb > c] throughout chapters, acknowledgment of the many competing hypotheses in Ecology pertaining to dispersal or multiple-mating by females, use of optimality formulations). As an example from Chapter 5 (“Maternal care”), TC-B's treatment asserts, accurately, that mammalian females invest heavily in current offspring, but theory holds that, after parturition, female resources, above some critical minimum, are channeled into future reproduction and lifetime reproductive success--“fitness.”
Chapters 10-16 pertain to males, especially, mating strategies, relations with females, and paternal care. Characteristic of Mammal Societies as a whole, these chapters are literature reviews of mostly descriptive publications from the Animal Behavior literature. Life history evolution is addressed in this chapter without mentioning the importance of tradeoffs, the distinction between semelparity and iteroparity (“fast” and “slow” life history trajectories, respectively), the importance of life-tables and the role of mortality as a driver of life-history evolution (Stearns 2000). Chapter 17 reviews “Cooperative breeding,” one of TC-B's specializations, and Chapter 18 presents a discussion of “Sex differences." Throughout the book, the author impresses the reader with the centrality of sex, sexual competition, and mating—topics of import in TC-B's career, though one is surprised that more attention is not given to Sexual Selection, per se. Chapters 19 and 20 address hominoids and hominids, including, modern humans, topics often missing or skimmed in other Animal Behavior texts.
TC-B presents at least one controversial formulation in Mammal Societies by asserting, with no supporting evidence or logical arguments, that no mammals are “eusocial”²—that the highest grade of sociality in mammals is “cooperative breeding.” This view is orthogonal to standard practice in Mammalian Social Biology whereby the social mole rats are typically classified as “primitively” eusocial. Technically, according to common usage, “cooperative breeders” might, as well, be classified “primitively” eusocial because of the presence of reproductive division of labor [cooperation between specialists] in the form of totipotent “helpers” (see Jones 2014, p 48-52). Mammal Societies exemplifies the need for practitioners of Natural History, Animal Behavior, and Behavioral Ecology to revisit topics such as standardization of terminology, advancement of the Hamiltonian Project, the roles of quantitative theory and modeling (in particular, agent-based modeling), field experiments, as well as, hypothesis-testing [including, the role of null-hypotheses] based on 1st principles. The text will appeal to professors wanting a Natural History, mostly, non-quantitative, review allowing supplementary reading to be incorporated into a syllabus. Future syntheses of Mammalian Social Biology will rely on mainstream schemas from Ecology & Evolution, in particular, employing a Major Transitions Approach (cf. West et al. 2015), in addition to, Population Ecology, of which Behavioral Ecology is a sub-field.
¹Care of offspring by conspecifics other than the mother
²”The evolution of eusociality, here defined as the emergence of societies with reproductive division of labour and cooperative brood care, has occurred under specific ecological, genetic, and life history conditions. Although sophisticated levels of cooperation have evolved in the largest and more complex societies, conflicts among individuals are still common because, in contrast to cells of an organism, they are not genetically identical,”--i.e., not "clones" (Keller & Chapuisat, 2010)
References
Bradbury JW (1981) The evolution of leks. In Natural selection and social behavior. (RD Alexander, DW Tinkle, eds). Chiron Press, New York, pp 138-169.
Briga M, Pen I, Wright J (2012) Care for kin: within-group relatedness and allomaternal care are positively correlated and conserved throughout the mammalian phylogeny. Biology Letters: p.rsbl20120159
Clutton-Brock TH (2021) Social evolution in mammals. Science 373(6561): doi:10.1126/science.abc9699.
Clutton-Brock TH, Parker GA (1995) Punishment in animal societies. Nature 373: 209-216.
Davies NB, Krebs JR, West SA (2012) Introduction to behavioral ecology. Wiley-Blackwell, 4th edition. Oxford, UK.
Eisenberg JF (1981) Mammalian radiations. U Chicago Press.
Jones CB (2014) Evolution of mammalian sociality in an ecological perspective. Springer, New York.
Keller L, Chapuisat M (2010) Eusociality and cooperation. In Encyclopedia of life sciences. Macmillan, published online: DOI: 10.1002/9780470015902.a0003670.pub
Ladevèze S, de Muizon C, Beck RMD, Germain D, Cespedes-Paz R (2011) Earliest evidence of mammalian social behaviour in the basal Tertiary of Bolivia. Nature 474: 83-86.
Sibley RM, Hone J, Clutton-Brock TH (eds) (2003) Wildlife population growth rates. The Royal Society: Cambridge University Press, Cambridge University Press, UK.
Stearns SC (2000) Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87: 476-486.
West SA, Fisher RM, Gardner RA, Kiels ET (2015) Major evolutionary transitions in individuality. PNAS 112(33): 10112-10119.
Westneat D, Fox C (eds) (2010) Evolutionary behavioral ecology. Oxford University Press, Oxford University Press, UK.
Wilson EO (1971) The insect societies. Belknap (Harvard), Cambridge, MA.
Wilson EO (1975) Sociobiology: the new synthesis. Belknap (Harvard), Cambridge, MA.
*Originally published in International Society for Behavioral Ecology Newsletter, 2016.
Addendum: I want to apologize to Tim Clutton-Brock for this review which expresses, as much as anything else, my disappointment in his text--of which I had great expectations. My expectations were so high--I expected a synthetic masterpiece in the context of evolution and the Major Transitions Approach--something on the order of EO Wilson's, The Insect Societies (1971), but, for Mammals. Even a book like JF Eisenberg's, mammalian "radiations" (1981), but about mammalian social evolution--extending Eisenberg's relevant chapters--would have been a major advance for the field. Instead, Clutton-Brock's book, whose title is a misnomer, is little more than a review of many highly selected publications without a conceptual framework [e.g., The Hamiltonian Project (the General Law of Social Evolution); Major Transitions, including, Sociality (Cooperation, after Hamilton 11964), as well as, Complex Sociality: SPECIALIZATION: division-of-labor (Cooperation between specialists); reproductive DoL, task, role, &/or morphological specialization] without any treatment of general patterns, without standardization of terminology, with only a nod to, systematic, quantitative theory--including, Hamilton's rule, and all in the context of a colonial historical-academic framework [e.g., every photograph of people of African descent is of primitive groups save one, and that one of an African guide, apparently, on a hunting safari with white male tourists. Unless I am mistaken, only a very few women are highlighted. Surely, TC-B might have provided a nod to changing worldviews by highlighting one or more of his African & female colleagues who must exist since TC-B has been conducting research in Africa for decades; if TC-B has not had African collaborators, volumes are silently spoken [admittedly, I know nothing about his personal or academic or research affiliations or his views on race, ethnicity, class or gender; and, I "get" it--the "greats" in Animal Behavior are, mostly, white men--even, until recently, in Anthropology, & I defer to the historical record ... nonetheless, it would have been generous to include, say, "Griff" Ewer, as deserving of recognition, for example--if only for the sake of appearances, but, then, my own biases are showing; in the final event, it would not detract from C-B's legacy for him to have been more generous in his historical acknowledgements].In short, as one who has admired TC-B's exhaustively rendered empirical work for decades, my expectations and anticipations, as well as, intellectual curiosity, were totally deflated by the long literature review treated herein. A synthesis of mammalian Ecology & Evolutionary Biology, in other words, a text on Mammal Societies, awaits future treatment. John F. Eisenberg's 1981 book, "radiations," is the closest thing we have so far to a synthesis of mammalian social biology. 5/9/2020; slight edit, 12/30/2023 ...