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 1^st 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, 4^th 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

Review of 2 Social Biology books (ISBE Newsletter) (Clara B. Jones)

Sociobiology of Caviomorph Rodents: An Integrative Approach

Luis A. Ebensperger & Loren D. Hayes, Eds.

2016

Wiley Blackwell

Hoboken, NJ, USA

380 pp

$97.03

Cooperative Breeding in Vertebrates: Studies of Ecology, Evolution, and Behavior

Walter D. Koenig & Janis L. Dickinson, Eds.

2016

Cambridge University Press

Cambridge, U.K.

379 pp

$115.67

Reviewed by Clara B. Jones* (foucault03@gmail.com)

In his highly regarded book, Principles of Social Evolution (2011), Andrew Bourke treats the origin of societies as a major evolutionary transition characterized by control of conflict and the appearance of castes (Table 1.3). In this author's system, castes define a society as eusocial, “with an appreciable reproductive division of labour, irreversible or not” (Box 1.1). Eusocial societies with totipotent individuals, are sometimes referred to as “primitively” eusocial (Wilson 1971), and Bourke points out (loc. cit.) that cooperatively breeding vertebrate societies resemble (reversible) eusocial societies “because any level of reproductive division of labor implies a degree of altruism” (loc. cit.). In my own work, I follow Bourke's terminology (Jones 2014), in addition to his use of Hamilton's (1964) schema limiting animal (including, human) behavior to four categories (selfish, cooperative, altruistic, and spite, Table 1 this review). In Hamilton's system, then, “social” behavior is confined to cooperative or altruistic interactions between (usually) conspecifics, measured according to differential reproductive costs or benefits to Actor and Recipient.

In Sociobiology of Caviomorph Rodents, Ebensperger and Hayes have performed a service by summarizing a speciose and diverse group of primarily South American rodents (Patterson & Upham 2014) characterized by twelve families of which ~75% include one or more social species (including, capybaras, tuco-tucos, cavies, maras, viscachas, and chinchillas). Since at least 1998, Ebensperger has advocated for the use of hystricognath rodents as a model of social evolution, and the book under review reinforces that message documented in several chapters devoted to the wide range of caviomorph sociosexual behaviors and structures (Chapters 1, 2, 7-11). Additional chapters review caviomorph neurobiology, genetics, communication, and fitness effects, presenting a comprehensive, “integrative” approach to the group, while, in the final chapter (Chapter 13) the editors synthesize what we know and need to know, in their opinion, about caviomorph sociality.

Sociobiology of Caviomorph Rodents will appeal to specialists wishing to broaden their knowledge of social taxa as well as to students interested in identifying stimulating and important research topics upon which to base a dissertation or a career. Furthermore, the potential for comparative studies is documented by similarities in certain traits between some caviomorph species and voles. Unfortunately, readers will need to be tolerant of the volume's limitations such as the authors' failure to cite more than a few references after 2012, frequent repetitions, some annoying grammatical errors, too many instances of researchers relying upon personal opinion and qualitative statements rather than inferences based on measurements. Also, investigators studying caviomorph social biology seem to have a penchant for attributing group-living in this infraorder to predation pressure, a factor that some specialists consider a common cause of group-formation but not group-maintenance. Likewise, most of the authors in this text use group size as a proxy for social behavior, a problematic assumption seemingly resulting from defining “social” as group-living whereby larger groups would exhibit a greater number of interindividual interactions. As Rubenstein et al. (2016) show, however, the evolution of sociality relative to (female) group size is taxon-specific and rule-governed. Finally, and of significant concern, where Hamilton's general rule is discussed at all, statements appear naïve at best and, in some cases, incorrect (e.g., pages 307 and 311). This text is, nonetheless, recommended as a point of entry to a group of rodents with significant research potential. Indeed, rodents are the largest Order of Mammals; however, our knowledge of their social biology is limited compared to that of primates and carnivores, Orders with a noteworthy proportion of social species.

In Cooperative Breeding in Vertebrates, cooperative breeding is broadly defined as “breeding associations with three or more individuals collectively raising young in a single brood or litter” (Introduction). As a result, the book covers a wide range of taxa, behaviors, and structures. Koenig and Dickinson chose 19 species to illustrate their topic, 15 of these chapters covering birds, 1, fish, and 3 reports on cooperatively-breeding mammals. The final, summary chapter by the Editors is noteworthy because of Figure 20.3 and Table 20.1. In addition to the fact that the descriptive studies are fascinating and informative, they are examples of the high standards which field natural history can attain. Authors, many with international reputations, have not only keenly observed relevant behavioral and structural details of their systems, but, relying, primarily, on verbal, rather than, quantitative, models, interpret their results with an appreciation for hypothesis-testing. For the most part, researchers rely on descriptive statistics to illustrate their subjects and associated traits, though a few studies incorporate genetic analyses as tentative tests of “kin selection” theory.

Because the species described in this text range from delayed dispersal with no cooperative care (Siberian jays), to “marginal” cooperative breeders (western bluebirds), to simple conformations with single-pair breeders (superb fairy wrens) and their “helpers,” to complex societies incorporating plural breeders (superb starlings), the book can be read in a way that reveals patterns related to the evolution of cooperative breeding and possible causal factors (e.g., distribution and abundance of limiting resources, environmental heterogeneity, group size and composition, population demography, predation). Finally, throughout the text, promising topics for investigation are indicated, such as, Why does “helping” by males appear to be common (e.g., superb fairy wrens, chestnut-crowned babblers, bell miners, banded mongooses), and are its causal factors different than those for female “helpers”? Also, one is curious about “kidnapping” behavior in banded mongooses and whether it might be induced by social parasitism or, perhaps, is a precursor to “slavemaking” as is the case in some social insects?

Apparently, none of the research programs in either of the books under review utilizes multivariate analyses in an attempt to assess causality or agent-based modeling to conduct quantitative tests of hypotheses (but, see Chapters 3 and 18); thus, for the most part, inferences remain speculative. Furthermore, it is not clear from the discussion of methods in most chapters whether animals were marked, whether focal-animal observational procedures were employed (preferably with a randomized baseline), and in what ways field experiments were conducted. Virtually every chapter in both books under review end their reports by calling for more research to document variability of target phenomena, implying that it is premature to search for general principles within and between taxa, even though some of these studies have proceeded for decades. As the paper by Rubenstein et al. (2016) demonstrates, however, analyses based on central tendencies can expose straightforward rules upon which complex phenomena depend. Weinrich et al. (2006) demonstrated that there exists a limited number of solutions to any evolutionary question which would include the problems inherent to Social Biology. Sociobiology of Caviomorph Rodents and Cooperative Breeding in Vertebrates deserve serious inspection by students of sociality,, animal behavior, and behavioral ecology. However, conventional Natural History might benefit from the incorporation of more rigorous methods and the application of quantitative procedures.

References

Bourke AFG (2011) Principles of social evolution. Oxford University Press, Oxford.

Ebensperger LA (1998) Sociality in rodents: the New World fossorial hystricognaths as study models. Revista Chilena de Historia Natural 71: 65-77.

Hamilton WD (1964) The genetical theory of social behavior. J Theor Biol 7: 1-52.

Jones CB (2014) The evolution of mammalian sociality in an ecological perspective. Springer, New York.

Patterson BD, Upham NS (2014) A study in contrasts: two extensive Neotropical radiations. Frontiers in Ecology and Evolution 2: 1-2.

Rubenstein DR, Botero CA, Lacey EA (2016) Discrete but variable structure of animal societies leads to the false perception of a social continuum. R. Soc. open sci. 3: 160147. http://dx.doi.org/10.1098//rsos.160147

Weinreich DM, Delaney NF, DePristo MA, Hartl DL (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312: 111-114.

Wilson EO (1971) The insect societies. Harvard, Cambridge, MA.

*Originally published in ISBE Newsletter, 2016

Table 1. This table presents Hamilton's schema depicting hypothetical outcomes of interactions 

between two (usually conspecific) individuals (a “dyad”), including, predicted reproductive tradeoffs 

(often measured as # offspring). A “selfish” state is presumed to be original and fundamental since 

selection acts on individual genotypes and since assisting ego’s own reproduction should benefit an 

individual more than benefiting another individual's reproduction (an individual is always related to 

itself by 1.00). It follows that “cooperation” and “altruism” have evolved where a “selfish” strategy 

cannot do its best. By definition, “cooperation” and “altruism” require Actor (“ego”) to restrain or 

compromise some measure of its “fitness budget” by donating some measure of reproduction to a 

Recipient. In the case of “spite,” both Actor and Recipient lose reproductive benefits as a result of 

one or more interactions.

	BENEFITS OR COSTS TO ACTOR	BENEFITS OR COSTS TO RECIPIENT
SELFISH	+	-
COOPERATIVE	+	+
ALTRUISTIC	_	+
SPITEFUL	_	-

Social Biology (or Bound By Dulosis) (for E.O. Wilson) by Clara B. Jones

Social Biology (or Bound By Dulosis)

ISBN-10: 0674454901

“The mind makes the world in which it lives.” E.O. Wilson (1971)

Starting at fifteen,

adopting a priestly life

from fieldwork to fame.

Fondness for ants in amber

in fide scientiam.

Did you remain cloistered in your rooms

like an ascetic finding pleasure in restraint

a Lucretius of Sociobiology

investigating the way things were

as well as the way things are

not separate but connected

as solitary is connected to eusocial

and Polistes to Polybia

and Euclid to Mirzakhani?

You a storyteller not a mythmaker

a cenobite in scientific guise

aged by the ergonomic business of grants

and research and writing and papers or books

riving colleagues into separate classes or castes

with you and Hölldobler on top of them all

secure that your own kind honors patriarchy

above the societies of your ants always active

never able to afford contemplation

or forays beyond the local regime.

What codes prompted you to specialize on hexapod labor

divided like a Frau specializing on shopping or cleaning

while Herr divides his time between the laboratory and the gym

both places of commerce whether in Cologne or Cambridge

both places driven by testosterone's tendency to dominate the other type

dominating in some societies alien to altruism in the insect mode

as females form the nest and all its roles

succeeding in stunning contrast to their coevals with chaulky spines

separate domains

neither sex coexisting peacefully as matriarch or patriarch

since conflict releases ego from its boundaries.

I belong to a caste of workers acting for their own type

and types like them

wearing men's boots and gold hoop earrings

complement to the hues of their shoulders

strong as workers hauling detritus from their nests

as I cleansed my synapses of him, a task requiring months, no, years

memories persisting in some disarray, out of order

as you seemed to summon Hecate

rejecting, or, appearing to reject, Hamilton's c,

b being less of a loss in any formulation.

You know the gold ring encircles a formula

even though empiricists are the true heroes

the fact-checkers keeping Theory on the path to confidence

or, if not confidence, clarity of motive and function

an Atta foray on a clear night.

“You would make a worthy parasite.

May I be your host?”

a couplet spoken to too many consorts

iterations of manic emotions

nearly similar guises

on continents as different as South and West

and cities as alien as Letícia and Salzburg

but only one of you was called, “Patrón”

the one never forgotten

like the hostage-taker constantly on the other's mind.

Using energy that might succor herself

a contract that our kind calls “Love”

though insects know only slaves

as acervorum serves sublaevis in Germany

caring for the parasite's young

a task reserved for Patrón's other host

in another city, in another country

his supercolony extending across thousands of miles

connected by airplanes and radio towers

not limited by tiny legs moving in single file behind a leader.

I stayed exhausted, but, then, I was a caste of one, a man's host.

It might be easier to work with sisters and to serve one's own type.

Ant workers must have the best of all possible worlds.

Human families are polydomous

scattered yet still connected

across scales too massive for pheromones to span

though my senses recall him close to me in our humble cabina

lying parallel or not

anything but humble

our families nested thousands of miles away

secure that we were not a family

and never would be yoked through a new generation

or through some other holy contract

preventing us from gamboling serious contests with the highest stakes

and from morphing from pedestrian to universal

but, then, I could not sit at the High Table with him

though some reflect upon a negress wanting to

predisposed instead by ancient contracts advancing dulosis

and the fate of chance encounters

over the predictability of domestic life.

Once I saw a video of New York during rush hour

a high-speed moving picture of humans striding, or, running

in apparently random walk

ants scurrying in, out, around a perturbed nest

expending energy proportional to size

as humans do when not projected ahead in time

both types bound by Kleiber's Law and temperature

confounded by a constant

related to that other rule that you've rejected

where b and c expressed in terms of reproduction

will be defined as functions of Brown's theory

advancing our claims on the Unification Project

treating Solitary, Quasisocial, Semisocial, Eusocial

as states subsuming minimal and maximal rates

with each ergonomic component making its contribution

summation of energy-producing genotypes and phenotypes

conserved and reprogrammed from ants to man.

A robo-bee guided by my circuitry

semi-autonomous since that night in San José

a humanoid sitting opposite him at dinner

my fingers awkwardly grasping a fork

skewering chunks of brothy bass

both bitter and sweet with lemongrass and honey

made by bees near Bagaces

my hand steered remotely

powered by signals pulsing from his optic nerve

striking my programmed hand

avoiding an angle that might unveil my face

expressionless but wondering how I would return

to Cañas from Alajuela at 3 a.m.

My brain detached from self-induced intention

sensing that I was “winging it”

as scientists do while waiting for the next data point

humanoids as tethered to society

as an Apis flying alone to a blossom.

If not an individual, what?

If social behavior is a subterfuge

then selfish behavior is a hungry lion looking me in the eyes

calculating her odds with Hebbian precision

knowing in some connectome of her cortex that

without a good algorithm and a share of luck

potential for success may be as costly as failure.

A female lion and a worker ant are not alone

encumbered instead

by the energy of others in a pride or a colony

like other mammals or insects dominating terrestrial landscapes

or like ants fixed in amber

superior in ancient regimes arid or wet.