Thursday, January 3, 2019

Review of Mammal Societies by Tim Clutton-Brock (Clara B. Jones)


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)

Knowledge about group-living mammals may contribute to an understanding of vertebrate social evolution and the evolution of gregariousness in animals with generalized phenotypes. 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). In 2011, Ladevèze et al. reported fossil evidence documenting 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, these authors speculated that the species may have been cooperative breeders. In 2012, based on a phylogenetic analysis, 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”), group-living has a long history in these animals.

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, and, as a point of information, admit to having no “bones to pick” with its author. 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. In this review, I do not intend to deconstruct, to question the book's authority, or to impose my biases. Instead, I hope to provide a context for its readers, particularly, mammalian social biologists, to decide on their own its scope and utility.

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 of selected Natural History reports emphasizing publications by his own laboratory, by primatologists, and from the Old World. Of an estimated 5,300 references cited in the book under review, only 64 [THIS NUMBER IS INCORRECT--corrected in next issue of ISBE Newsletter] derive from mainstream journals in Ecology and Evolutionary Biology (N= 15 journals, including, Trends In Ecology and Evolution, American Naturalist, Journal of Theoretical Biology, Journal of Evolutionary Biology). While the Table of Contents presents a detailed outline of topics of interest to social biologists, there is little integration of technical reports with ecology and evolution. Furthermore, the sheer number of topics covered is so large that little space is devoted to most of them. 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 of the same topic (pp 456-574) presenting an explicitly articulated conceptual framework for mammalian social biology, including, trends, general and comparative features, an extensive glossary, as well as, case studies and summary tables, figures, and diagrams.

Chapter 1, “Social evolution,” omits definitions of terms (e.g., “aggregation,” “social”, “cooperation”), leading to obfuscation throughout the book, 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 and groups 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 fertilizeable females are usually a limiting resource for males and, subsequently, an ultimate determinant of male “fitness optima.” 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 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 “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 familiar Natural History papers and book chapters from the Animal Behavior literature, and few of the reports classifiable as Behavioral Ecology meet the standards of, say, Bradbury 1981. 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), 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” (without discussing classic theory). 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. 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 in the form of totipotent “helpers” (see Jones 2014). Mammal Societies highlights 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 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 more heavily on mainstream reports from Population Ecology (e.g., Oikos, Functional Ecology, Journal of Animal 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.” (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, 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.

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.

Westneat D, Fox C (eds) (2010) Evolutionary behavioral ecology. Oxford University Press, Oxford University Press, UK.

Wilson EO (1975) Sociobiology: the new synthesis. Belknap (Harvard), Cambridge, MA.


*Originally published in International Society for Behavioral Ecology Newsletter, 2016

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