Friday, January 10, 2020

Age polyethism [temporal division-of-labor] in mammals (General Pattern?) [Clara B. Jones, 1996]

Jones CB (June, 1996) Temporal Division-of-Labor In A Primate: Age-Dependent Foraging Behavior. Neotropical Primates 4(2): 50-53. [with minor edits from the original]

Division of labor based on age or size ["polyethism"] may reflect the reproductive condition of individuals in social groups. In 1967, West proposed the general hypothesis that hierarchical relations may be advantageous to both dominants and subordinates and that individuals of low rank may be inferior reproductives who benefit genetically from associations with and contributions to reproductively superior individuals. Since increasing age or size eventually entails decreasing reproductive value (Vx), several authors have noted that the display of social behavior, such as foraging behavior that benefits all members of a group, especially kin, should increase with age as the benefits from individual (selfish) reproduction decline (e.g., West-Eberhard 1975; Hrdy & Hrdy 1996). As individual reproductive value decreases, benefits (genetic or other) from assisting the reproduction of conspecifics (social behavior [cooperation, altruism as per W.D. Hamilton 1964]) may increase because costs (genetic or other [including, delayed costs or benefits] of social behavior) decrease with decreased benefits from individual reproduction. In order to test this hypothesis, I studied the relationship between adult female age, dominance rank, reproductive value, and social foraging behavior (food search and pursuit) for adult female mantled howler monkeys (Alouatta palliata Gray). [Author's note, 1/20/2020: "Temporal division-of-labor" (TDL) may, also, be termed, "age-polyethism" or "primitive" (totipotent) eusociality or Totipotent Eusociality (TE); see blogpost on General Mammalian Patterns, #28]

Subjects and Methods
During an extended period of study at Hacienda La Pacifica, Canas, Guanacaste, Costa Rica, I studied two marked, aged groups of mantled howler monkeys in two tropical dry forest habitats [Riparian, Group 5, and Deciduous, Group 12: see Jones 1980, Table 1]. For this species [and others of the genus], age and dominance rank are negatively correlated [Jones 1978, Jones 1980].

Social foraging was operationally defined as the behavioral series: feed-rest-move [at least 100 m]-feed, by a unit of more than three adults. These criteria were adopted in order to standardize measurement and to eliminate periods of food search within unusually large patches and by consort pairs. I identified which females in the primary study groups initiated foraging sequences and analyzed these observations by age.

My null hypothesis held that the frequency of foraging by females of any age class would be proportional to the total number of females who foraged in an age class. Two of the 15 [adult] females in one group [both young adults--Riparian Habitat Group 5] were never observed to direct foraging sequences and are excluded from analysis. Three [adult] females were aged on the basis of physical and behavioral traits other than tooth wear, and assignment to age classes for these females was made independent of the present analysis. Two of these females were observed from sub-adult through adult growth and classified as young adults; a third [adult] female, classified as middle-aged, was the mother of a sub-adult and a juvenile offspring, a highly unlikely combination for any other age class [see Glander 1980]. In my analysis of the second group [eight adult females--Deciduous Habitat Group 12], two young adult immigrant females were never observed to forage socially and were excluded from analysis. The pattern of results reported here would remain unaffected by alternative treatments of the raw data.

A monthly foraging rate for each forager was computed by dividing the frequency of foraging by the female's number of months resident in a group, a period of time varying from 10-14 months since some females emigrated during the study. These rates were compared with a female's age class, on the one hand, and dominance rank, on the other, to assess the relationship between the display of social foraging behavior and rank, and reproductive value [Vx, for her age class, (computed from) population data in Malmgren 1979, Table 23; equation after Wilson & Bossert 1971; c.f. Jones 1997] where relative contribution to future generations of an individual of a given age is quantified.

Results and Discussion
Table 1 [below--scroll down] presents the results of my analysis for the first group [Group 5] of foraging frequency as a function of female age, including, expected frequencies, and Chi Square. Computing "goodness of fit" led to an unequivocal rejection of the null hypothesis [P <- 0.001, X2= 107.64, df= 3]. Thus, old age and foraging frequency are significantly related. Young adult females initiate foraging significantly less than expected on the basis of their numbers [in Group 5: P <- 0.001], suggesting that such individuals are relatively "selfish" or are conserving time [T] and energy [E], possibly for reproduction and/or competition. Table 1 also shows that the middle-aged to old female foraged more than expected by chance [P <- 0.01], and this female succeeded the oldest and lowest-ranking female as the most frequent [social] forager when the old female emigrated in 1977 [personal observation*].

Additional observations support the reliability of the above patterns. The oldest female in the second group [Group 12] foraged more frequently than any other adult female [P <- 0.001, X2= 17.29, df= 2; c.f. Jones 1998]. Similarly, the relationship between foraging rate and age class [Fig. 1] yields a significant positive correlation [rs= +0.629, P <- 0.05]. Related to this, the correlation between foraging rate and dominance rank [Fig. 2] is significant but negative [i.e., the higher the foraging rate, the lower the dominance rank, rs= -0.63, P <- 0.05]. Thus, the initiation of [social] foraging is significantly associated with female age and dominance rank.

It was hypothesized above that the expression of social behavior would increase with increasing age since reproductive value [Vx, Fig. 3] decreases with age and with it the benefits from selfish reproduction [i.e., adult females have less to lose and more to gain in fitness as they age]. Figure 3 shows the reproductive value curve for the population of mantled howler monkeys at Hacienda La Pacifica [after Jones 1997]. Comparing Fig. 3 with Figs. 1 and 2, consistent with expectation, a strong negative association appears to exist between reproductive value and rate of foraging. Reproductive value in the four adult age classes is negatively, and significantly correlated with social foraging rate/month [rs= -0.95, P <- 0.02]. These results support the view that increasing age or size eventually entails decreasing reproductive value and that the display of social behavior should increase with age as the benefits from individual [selfish] reproduction decline.

What features of the howlers' environment might favor temporal division-of-labor? On 52 occasions, I was able to record the specific resource upon which foraging sequences terminated. Forty-four [85%] of these sequences terminated on ephemeral food [i.e., fruit, flowers, or new leaves: see Jones 1996], while eight [15%] sequences terminated with feeding on mature leaves [P <- 0.001, X2= 49, df= 1]. Thus, the initiation of social foraging sequences appears to be associated with food, the local distribution of which is temporally uncertain; new leaves, flowers, and fruit. The old female initiated 21 of the 52 [foraging] bouts, 20 of these for ephemeral food [c.f. Jones 1998].

An old female's presumed experience with the mosaic of her home range might enhance her efficiency as a forager so that her foraging activity may yield an energetic and nutritional gain to other group members. Temporal uncertainty of preferred food resources [see Jones 1996] may favor individuals that are the beneficiaries of the foraging activity of others, particularly, kin, when reproductive value is low. Division-of-labor through differential social roles may be a function of relative reproductive value, and behavioral roles may be understood within the context of life history patterns. [------>across Social Mammals** & other Social Vertebrates**? across Social Animals**?].

I appreciate the comments of R.C. Lewontin, E.O. Wilson, M.J. West-Eberhard, I.S. Bernstein, W.C. Dilger, and K.E. Weber on an earlier draft of this note. I thank the W. Hagnauer family for permission to work on their property, Hacienda La Pacifica, and for logistic assistance. My gratitude to Norman J. Scott, Jr. [USFWS], for expert introductions to the conduct of fieldwork and for imparting a variety of skills, is immeasurable. The work was supported by grants from the National Fellowships Fund and the National Research Council.

Clara B. Jones, Institute of Animal Behavior, Rutgers University-Newark, 101 Warren Street, Newark, New Jersey 07102, U.S.A.

Glander KE [1980] Reproduction and population growth in free-ranging mantled howling monkeys. Am J Phys Anthropol 53: 25-36.
Hamilton WD [1964] The genetical theory of social behavior. J Theor Biol 7: 1-52.
Hrdy SB, Hrdy DB [1976] Hierarchical relations mong female hanuman langurs (Primates: Colobinae, Presbytis entellus]. Science 197: 913-915.
Jones CB [1978] Aspects of reproduction in the mantled howler monkey, Alouatta palliata Gray. Ph.D. Dissertation, Cornell University, Ithaca, NY.
Jones CB [1980] The functions of status in the mantled howler monkey, Alouatta palliata Gray: intraspecific competition for group membershi in a folivorous Neotropical primate. Primates 21: 389-405.
Jones CB [December, 1996] Predictability of plant food resources for mantled howler monkeys at Hacienda La Pacifica, Costa Rica: Glander's dissertation revisited. Neotropical Primates 4(4): 147-149.
Jones CB [1997] Life history patterns of howler monkeys in a time-varying environment. Bol. Primatol. Lat. 6(1): 1-8.
Jones CB [March-Dec, 1998] A broad-band contact call by female mantled howler monkeys: implications for heterogeneous conditions. Neotropical Primates 6(2): 38-40.
Malmgren LA [1979] Empirical population genetics of golden mantled howling monkeys (Alouatta palliata) in relation to population structure, social dynamics, and evolution. Ph.D. Dissertation, University of Connecticut, Storrs.
West MJ [1967] Foundress associations in polistine wasps: dominance hierarchies and the evolution of social behavior. Science 157: 1584-1585.
West-Eberhard MJ [1975] The evolution of social behavior by kin selection. Quart Rev Biol 50: 1-33.
Wilson EO, Bossert WH [1971] A primer of population biology. Sinauer Assoc., Stanford, CN.

*  The last time I saw Group 5's D4 female, she was seated alone and immobile on a tree limb; her face impaled with quills of the prehensile-tailed porcupine [or, coendou: Coendou]. I never encountered this female again.
**EO Wilson's 2019 book, Genesis, advances the idea that many Mammals, including, humans, may be "eusocial." Where "temporal division-of-labor" is demonstrated, taxa can be classified, "primitively eusocial;" this classification would apply, also, to any other Vertebrates or, indeed, to any other Animals, where "age polyethism" is identified. If "tradeoffs" [e.g., energetic, reproductive, survivval] are most likely to be observed in "poor" conditions [e.g., heterogeneous regimes where "fitness" is compromised; recurrent drought, unpredictable food or water supply], "age polyethism" may evolve to minimize energetic costs in time and space. While females are expected to be most sensitive to energetic effects, males, also, may benefit, under some conditions, from age-dependent responses. Furthermore, there  may be energetic [reproductive] benefits in coordinating many maturational [age-dependent] and developmental [age-dependent] milestones or markers with one another as genetic and physiological energy-savings tactics and strategies.
Table 1. Age class, estimated age in years, number of females in each age class (N), observed (O), and expected (E) frequencies of social foraging, and chi square (X2) for a test of the null hypothesis. In “Age Class” column, YA= Young Adult; M-a= Middle-aged Adult; M-a-O= Middle-age to Old Adult; O= Old Adult.
Age Class N O E (O-E)2/E (X2)
YA (5-7) 5 15 42.4 17.71
M-a (7-10) 5 35 42.4 1.29
M-a-O (10-15) 1 18 8.1 12.11
O (15+) 1 33 8.1 76.54
Total 12 101 101 107.65

Thursday, September 19, 2019

My comments on Eisenberg JF (1981)...Mammal "radiations" (Clara B. Jones)

My comments on Eisenberg JF (1981)...Mammal "radiations"...

The mammalogist, John F. Eisenberg's, oeuvre remains one of the most highly respected and important in his field. Because most of his research investigated Neotropical mammals, rather than mammals of the Old World, his is not a household name. Because of my own specializations, in this brief review, I limit my comments to Eisenberg's treatments of mammal Behavior and Social Organization [group-living, interindividual interactions, cooperation, and altruism]. With E.O. Wilson's 1975 important chapter on patterns of sociality in Class: Mammalia ["The secret to the evolution of sociality in mammals is milk."], Eisenberg's "radiations" is the first attempt to identify PATTERNS of Behavior & Social Biology across all group-living mammals for which there was data by 1981. No subsequent treatment has attempted successfully to summarize the social biology of mammals comparable to Wilson's 1971 treatment of Social Insects [necessary reading for Behavioral Ecologists & Social Biologists] or Holldobler & Wilson's 1990 treatment of the Ants. Though Tim Clutton-Brock recently published a book [2016]  titled Mammal Societies [sic], it stands as a highly selective literature review, rather than a synthesis. The limited and highly selective chapter by Smith et al. in Rubenstein & Abbott's 2017 Comparative Social Evolution omits Primates and posits bats as the Order needing research as a model for the evolution of sociality in mammals [a view, possibly, derived from Wilson, 1975's discussion of bats]. To the contrary, bats are a highly derived group not suited for a model of general patterns. Rodents are the taxon of choice, including large-bodied and small-bodied groups, sexually-segregated ["solitary"] to highly social species [including the social mole-rats], and taxa with generalized as well as specialized phenotypes--living across virtually all ecotones, and with a commensal relation to humans--that will be most helpful in the early phases of identifying common features across mammals, as well, possibly, across vertebrates. Additionally, critical to any scientific treatment, and as Eisenberg points out in "radiations," the marsupials are the only group of mammals that can serve as a "control group" for tests of hypotheses and apparent patterns [see comments on this idea in Wilson '75]. My 2014 book, The evolution of mammalian sociality in an ecological perspective, is synthetic, emphasizes Ecology, but is brief. The Class is sorely in need of a synthesis across taxa for which data are available; unfortunately, behavior & sociality of rodents are not well known [but, see, Wolff & Sherman's 2007 volume, Rodent Societies]. Wilson, 1971, 1975, are critical for the standardization of terminology, as well as, factors critical to the study of Social Biology and patterns of group life [e.g., the evolution of Communication, "polyethism"], and Robert Trivers', Social Evolution, as well as, James Costs's, The other social insects, should be consulted. Critically, as a few mammalogists have pointed out [e.g., Bob Selander], initial attempts to synthesize patterns across group-living mammals should begin with analyses that study large and small mammals separately. Finally, we want to assess the observation that the structure of mammal [vertebrate?] groups results from the tendency of females to select rich patches of food and that of males to select the largest relative aggregation[s] of females. Other patterns are identifiable in existing literature. Since the time of John Hurrell Crook [Behavior Monograph X], we know that patterns of group organization depend upon the distribution and abundance [dispersion]  of limiting resources [e.g,, food, mates, sleeping sites]. Also, related to this overview, females are, cet. par., "energy maximizers;" males, "time-minimizers."

General Mammalian Patterns, esp., Social Patterns [compiled by Clara B. Jones]

General Mammalian Patterns [?--in no particular order] with an emphasis on Social Biology & Behavioral Ecology--also see Twitter @cbjones1943 

1. For analysis, and where data permit, we will separate comments for large & small mammals--as suggested in literature, e.g.,

2. Several authors have claimed that large mammals have, cet. par., generalized phenotypes, presumably, related to evolution in heterogeneous regimes ["environmental grain" theory proposed by Richard Levins]. Is this related to the evolution of phenotypic flexibility [temporary change] and phenotypic plasticity [permanent change"]? Wilson '75 posits that phenotypic flexibility/plasticity is a general feature of social evolution of large mammals [n.b., the evolution of "learning" should be discussed here, including, the evolution of "social" learning requisite to Culture]. For all of the topics in #2, you might want to take a look at my 2012 Springer Brief. Furthermore, to the extent that mammals exhibit generalized phenotypes, this trait would be expected to inhibit evolution of specialized morphologies, such as, morphologically distinct castes. See sections on generalized phenotypes in Eisenberg (1981).

3. Selander & others [see paper linked in #1 above] argue that large mammals have higher tolerance for genetic monomorphism. x

4. The basis for Social Evolution in mammals is milk. (EO Wilson 1975, Sociobiology, Belknap: HUP) n.b. a number of authors claim that the basis for Social Evolution in mammals is the primitively [non-cooperative, non-altruistic] communal female group. The basis of Wilson's point, however, is that Mammal females are obligate caretakers of young, predisposing them to certain life-history trajectories, including, probably, receiving help, all limited by energetics. Recall the litany that females are "energy-maximizers," males, "time-minimizers." x

5. The four "pinnacles" of social evolution: the colonial invertebrates [e.g., corals, bryozoans], the social insects, the non-human mammals, & humans]...Wilson '75 p 379 x

6. Traits of the non-human mammals: aggressiveness & discord carried further in vertebrate, including, mammal, societies than in social insects...selfishness rules interindividual sterile castes [though reproduction may be suppressed chemically or by "choice"]...acts of altruism infrequent and usually directed toward kin, especially, offspring...cooperation usually rudimentary; though inequity & hierarchy virtually ubiquitous [wherever there is division of labor there will be inequity] human standards, some acts "butal" [e.g., treatment of infirm & dying]...mostly after Wilson '75, p 380

7. Human social traits: humans remain "essentially vertebrate" in their social structure, but more "complex," not by reduction of selfishness but by evolution of intelligence and language [relate to phenotypic plasticity; learning, including, social learning (cultural mechanism); social parasitism; persuasion; manipulation; exploitation, etc]...elaboration of kin relations [cost-benefit]...human societies "approach" levels of cooperation in insect societies & far exceed social insect societies in communication...mostly after Wilson '75, p 380

8. Most "interesting" mammal orders: rodents, artiodactyls, primates, marsupials--"control group" for Class after Wilson '75 & Eisenberg '81 [social biology of largest mammal orders--bats, rodents--virtually unknown as of 1975]...mostly after Wilson '75, p 468 x

9. Traits labile [e.g., mode of intrasexual cooperation, degree of cohesion, openness of societies (c.f. "open" vs. "closed" groups)]. Many forms of interaction change seasonally, & patterns differ at species level. [after Wilson '75]

10. Phylogenetically, more primitive living marsupials and insectivores tend to be solitary. Species that forage nocturnally or underground are, also, mainly solitary.

11. As a rule, the most complex social systems within each Order occur in the physically largest numbers...true of marsupials, rodents, ungulates, carnivores, and primates [Why? maybe because diurnal and because of large brains (intelligence?)? Wilson '75 Also, refer to J.H. Crook's work with weaver birds and other work in Behavioral Ecology: need to evaluate dispersion (distribution and abundance in time and space) of limiting resources relative to behavior & social biology].

12. Species adapted to life in open environments more likely to be social. Rodents known to form coteries of mixed sexes are all inhabitants of grasslands. Ungulates--great herds predominantly found i n grasslands and on savannas, though herds mostly loosely structured--but see, horses, mountain sheep, elephants, and a few others [zebras?] Wilson '75

13. The structure of mammal [vertebrate?] groups is thought to result from the tendency of females to select rich patches of food and that of males to select large aggregations of females. Because patch richness and the consequent number [and quality] of females [female group size] is expected to vary, the relative reproductive success [RRS] of females may, also, vary over time and space. See the following paper, for example:

Also, see:

Jones, CB (March, 1996) Relative reproductive success [RRS] in the mantled howler monkey: implications for conservation. Neotropical Primates 4(1), pp 21-23.

14. Chapters on Mammals in Rubenstein & Abbott (2017), not useful for treatments of general patterns of Social Biology in Mammals; however, see stimulating final, summary chapter in this ambitious edited volume.

15. IMO, the chapters in Wilson (1975) on non-human primates and on humans are not very useful for identifying patterns in the Primates, in Homo sapiens, across Mammals [or, across vertebrates].

16. Tim Clutton-Brock's text, Mammal Societies, not very useful for identifying general patterns of Social Biology in Mammals. This book is a highly selective literature review. See, however, the useful table of contents & #generateideas.

17. Neotropical social mammals require thorough treatment, review, and integration into the broader literature on mammals which is dominated by research in the Paleotropics. In South America, see, especially, caviomorph rodents [infraorder, Caviomorpha], uniting all So. American hystricognaths. n.b. all or most of these spp. are small-bodied, & they are related to Old World [hystricognath] social mole rats.

18. General Patterns...Gene Evolution...Convergence...Gene E. Robinson Lab [see Jenny Tung's preliminary, though, cutting-edge, work on mammals]:

19. Temporal division of labor [age (-graded) polyethism: Wilson 1971] is ubiquitous in social insects; how common is it in Mammals & other vertebrates? See [especially, tables]: Jones CB (June, 1996) Temporal division of labor in a primate: age-dependent foraging behavior. Neotropical Primates 4(2): 50-53.

also, Wilson EO (1971) The Insect Societies. Belknap [HUP], Cambridge, MA.

20. The following book by Bernie Crespi discusses correlates of sociality [p 66, pp 73-74]...note, especially, significance of "high value" of limiting resources [abode, mates, food, etc.]...again, shows need to study limiting resource dispersion [distribution & abundance in time & space]...

Crespi BJ, Morris DC, Mound LA (2004) Evolution of ecological and behavioural diversity: Australian Acacia thrips as model organisms. Australian Biological Resources Study, Canberra.

21. How much of the variation in mammal behavior & social biology is explained by body size?

22. Nursing [mammary glands] predisposes mammal females to caretaking, dependency, subordinate [e.g., "helper"] status, & favoritism of kin &/or other females. But how are these adaptations affected by evolution in suboptimal ["poor"] conditions or conditions of intense competition [for limiting resources], or, say, drought or collapse of prey population?

23. See Part 4 of Eisenberg [1981] for discussion [also, tables] of mammalian behavior, including mating systems & social biology--see, especially, Chapters 31-33.. Eisenberg [1981] classifies mammal "mating systems" into 10 categories, reduced to 3 basic types: polygyny [1 male, >1 females]; polyandry [multiple-male : multiple female], in which females mate with >1 male [not necessarily "promiscuous", i.e., females may demonstrate selectivity or preferences; also, there may be "favoritism" in which an adult female & an adult male are likely to mate exclusively or commonly with each other]; monogamy [uncommon] 

See Eisenberg's outdated but still interesting and classic paper, Eisenberg JF (1966) The social organizations of mammals, Handbuch der Zoologie, Band 8. Lieferung 39: 10(7): 1-92.

24. Feldhamer GA, Drickamer LC, Vessey SH, Merritt JF, Krajewski C (2007) Mammalogy. Johns Hopkins UP, MD: "typical mammalian pattern of preferring unrelated distant kin as mates;" Emlen's "ecological constraints" model + Trivers' reciprocity [+ "pay to stay"?] explain "helping" in mammals?--especially, patterns in social mole rats [do naked mole rats have castes since there is a specialized "disperser form" in this species?]...see Jarman [1974] for classification of mammalian social organization x feeding selectivity: least selective most gregarious, large, polygamous, & sexually dimorphic--Jarmon PJ [1974] The social organization of antelope in relation to their ecology. Behaviour 48: 215-267...need to integrate Jarmon's findings with those of Crook [1964, Behaviour Monograph X] on weaver birds, i.e. relationship between food dispersion [distribution & abundance] and social structure/organization...

25. Ricklefs RE, Miller GL [2000] Ecology, 4th Edition. W.H. Freeman & Co., NY: Part 4, Population Ecology, Section 4.2, The dispersion of individuals reflects habitat heterogeneity and social interactions--"The dispersion of individuals within a population describes their spacing with respect to one another."--clumped [aggregation (maybe poor choice of word)]--clumped [limiting] resources may be most common determinant of these patterns, also, tendency of offspring to remain in natal group --see #13 above; spaced [even spacing= hyperdispersion]; random ["In the absence of social antagonism, which results in a spaced dispersion pattern or mutual attraction, which leads to clumping, individuals may distribute themselves at random" Can use Poisson methods to evaluate dispersion patterns...also, see Index of Dispersion [Clark & Evans, 1954]...also, can evaluate "nearest-neighbor distance"--"interindividual distance" [IID] in primatology literature...again, see Crook, 1964, Behavior Monograph X...

26. When discussing patterns of grouping or "social" organization [in populations], I have the strong impression that Mammalogists tend to attribute the patterns to phylogeny, philopatry [patterns of dispersal x sex], and/or predation...a Crookian [Behavioral Ecology] framework seems not to influenced Mammalogy very much where a "Crookian framework" would entail the mapping of animals in a population on to the dispersion of limiting resources [distribution and abundance of limiting resources in time and space--ceteris paribus & on average relative to differential engergetics x sex--males, at least, adult males, expected to be "time-minimizers," females, at least, adult females, "energy-maximizers"]...

27. The (2007) edited volume on Rodents by Wolff & Sherman [link] should be read in association with John F. Eisenberg's 1981 book on mammalian "radiations" [op. cit.]...Eisenberg provides broad context for many topics [e.g., parental behavior, scent marking, infanticide]...

28. General patterns in Social Mammals [Social Vertebrates? Social Animals?]: EO Wilson [Insect Societies, Belknap (Harvard), 1971] discussed "age polyethism" ["temporal division-of-labor": TDL; "primitive" (totipotent) eusociality] in social insects as a feature of eusociality, particularly, "primitive" eusociality [taxa displaying "totipotency," the capacity to switch from a reproductive to a non-reproductive state & vice versa, as opposed to "advanced" eusociality, taxa characterized by sterile castes]...this article* provides the first empirical evidence of temporal division-of-labor in a mammal [1996], the mantled howler monkey, Alouatta palliata Gray, studied by the present author in Canas, Guanacaste, Costa Rica. Temporal division-of-labor ["age polyethism," "primitive" (totipotent) eusociality] may occur widely among social mammals, social vertebrates, and, possibly, all social animals, where Cooperation and/or Altruism [including, reciprocity] have evolved in group-structured populations...i would speculate that TDL ["age polyethism;" "primitive" (totipotent) eusociality] is more energetically efficient than more opportunistic, and, perhaps, more flexible or plastic, modes of [social] behavioral expression & might be expected to evolve/occur in contexts favoring conservation of energy [e.g., in heterogeneous regimes]...since females are expected to be "energy maximizers" [metabolically, reproductively], TDL may be more likely to be observed in females compared to males ["time-minimizers"]...TDL is expected to be developmentally programmed [within some (statistically normal) species-typical, population-typical, range (x sex)], & conscious & aware processes may not be required for its ////?, Jones reported age-dependent expressions of conflict-resolution among adult males of the same Alouatta species in the same location & group; these results require intense investigation, lab & field experiments, & modeling, including, for is important to investigate those conditions under which different energy-conservation strategies evolve x sex...since males are expected to be more robust under energy constraints, it seems likely that thresholds will be identified differentially x sex for the same endogenous and exogenous, including, social, stimuli/factors/conditions.

EO Wilson's 2019 book, Genesis, advances the idea that many [social] Mammals, including, humans [ see**], may be "eusocial." Where "temporal division-of-labor" ["age polyethism"] is demonstrated, taxa can be classified, "primitively eusocial" and/or Totipotent Eusocial [TE] this classification would apply, also, to any other Social Vertebrates or, indeed, to any other Social Animals, where "age polyethism" [TDL; "primitive" eusocial; TE] is identified. If "tradeoffs" [e.g., energetic, reproductive, survival] are most likely to be observed in "poor" conditions [e.g., heterogeneous regimes where "fitness" is compromised; recurrent drought, unpredictable food or water supply], "age polyethism" may evolve to minimize energetic costs in time and space. While females are expected to be most sensitive to energetic effects, males, also, may benefit, under some conditions, from age-dependent responses. Furthermore, there  may be energetic [reproductive, survival] benefits in coordinating many maturational [age-dependent] and developmental [age-dependent] milestones or markers with one another as genetic and physiological energy-savings tactics and strategies.

29. Wolff & Sherman (2007, link) includes some interesting & useful chapters, though, terminology is not standardized [& is often confusing (e.g., "single-breeding," "multiple-breeding"--particularly, as they are discussed in relation to philopatry...see, for example, Chapter 21 by Lacey & Sherman, who needed to make Emlen's work on Ecological Constraints fundamental to their discussion of "philopatry")], and "species" is often employed where "population" is, rather, the correct term. Each chapter in this book has a Summary at the end that can be read before digging into the whole chapter. Some chapters in Sections, "Introduction," "Social Behavior," & "Comparative Sociality" are of particular interest to students of Behavioral Ecology & Social Biology. There are many allusions to the importance of environmental [exogenous] factors, including, dispersion of resources; however, there is no explicit integration of [John Hurrel] Crookian socioecology [Behavior Monograph X] nor is there integration of Emlen's Ecological Constraints model which is fundamental when combined with Crookian socioecology. For context & references (especially, Emlen, Crespi), see blogpost, this blog, of EO Wilson's, Genesis.

Wolff & Sherman [2007],

EO Wilson Genesis review [blogpost, this blog]:***

30. Fundamental questions in Behavioral Ecology pertain to Population Structure relative to dispersion [distribution & abundance of limiting resources in T(ime) & S(pace)], also to Population Structure relative to Basic Laws of Ecology--Acquisition, Consumption, Allocation. Ultimately, we should be able to reduce "fundamental questions" to Thermal Biology [all Biology reduces to Heat], & all material phenomena reduceable to Physics----->expressible in mathematical terms.

31. Towards general principles [GUTs] via studies of Biological Assembly...for group-living---->sociality, see literature in Physics on "queuing"...




Tuesday, June 25, 2019

Research questions based on Ratnieks et al. 2006 (Clara B. Jones)

Research questions for group-living vertebrates based on Ratnieks et al. 2006*, **


Inclusive fitness theory explanations for both cooperation and conflict

What do we mean by conflict resolution?
1. "Potential conflict is any difference in the reproductive optima of individuals or groups within a society."
2. Individuals have three be workers, reproductives, or dependents (e.g., "social parasites") or some combination of these serially or concurrently. Categories can be analyzed by class or rank, by sex, by age, by race or ethnicity, etc.
3. For vertebrates, including, humans, how do we estimate "fitness optima?"

Kinship, coercion, and constraint
"...low relatedness makes wasteful conflicts more likely because the cost of conflict falls upon more distant kin."

Sex allocation
...differential investment in males and/or females & differential costs/benefits...

1. "Coercion and constraint may help to resolve conflict if one party has complete power over sex allocation." ...etc., e.g., over access to limiting resources...
2. "Mixed power seems likely in many but not all situations." ...e.g., "division of task"..."division of labor"...n.b. DoL more efficient than DoT; also note, male & female interests may not coincide since males are expected to be time-minimizers, females, energy-maximizers...
3. Under some conditions, is it more beneficial for an individual to assume the costs of conflict rather than to resolve conflict? ...i.e., When are costs of conflict [over reproduction &/or limiting resources (convertible to offspring] tolerated or preferred relative to benefits of conflict-resolution?
4. Importance of information, especially, competition for information [see EO Wilson 1971 on "communication" in societies]...Humans: language, who shares information with whom, etc...
5. Investigate "policing"*** as a form of conflict-resolution [mitigation of selfishness], mitigation of conflict [e.g., force, coercion, constraint, persuasion, etc. (see French & Raven's "bases of power")]...
6. What factors lower incentives for individual selfishness [& subsequent "tragedy of the commons"]
7. High "r" lowers the proportion of reproductives in a population...
See "reproductive skew" literature, e.g., R Hager & CB Jones 2009 CUP...

Conflicts among totipotent individuals
1. "Totipotency greatly increases the potential for conflict...."
2. If optimal family and/or group size can be estimated, excess individuals are likely to increase potential for conflict...

Discussion & Conclusions
1. Class conflicts relatively easy to resolve [because dominants "police" subordinates?]...
2. Conflict easily resolved when one party "powerless"...
3. Should the incorporation of steriles or other non-reproductives in groups reduce conflict?...relative to what [e.g., "r"]...
4. How do humans escape control in groups? [see French & Raven's "bases of power"]
5. What role does genetics play in conflict-resolution [e.g., genetic conflict]...

*Ratnieks FIW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu. Rev. Entomol. 51: 581-608.****
**Sentences in quotation marks are quotations from paper; other statements, comments, or questions are my interpolations relative to group-living vertebrates, including, humans.
***New paper: "'Enforcement' is central to evolution of cooperation"...i.e., &, also, to evolution of repression of selfishness...

****Topics/questions based on titles of literature cited:
--evolution of male and female traits
--causes & consequences of informational constraint
--conflict over class/SES determination
--status-allocation to offspring
--Does it "pay' kin to favor relatives who are "losers" or inferior reproductives and/or competitors?
--n.b. Charnov EL (1978) Evolution of eusocial behavior: offspring choice or parental parasitism? JTB 75: 451-465.
--n.b. Crespi BJ, Ragsdale JE (2000) A skew model for the evolution of sociality via manipulation: why it is better to be feared than loved. Proc R. Soc. London B Biol. Sci. 267: 821-828.
--facultative policing
--conflict over paternity [n.b. causes & consequences of multiple-mating by females]
--n.b. Keller L (1997) Indiscriminate altruism: unduly nice parents and siblings. TREE 12: 99-103.
--genes regulating complex social behavior
--ancestral states of complex sociality
--sex-ratio determination in groups & populations [e.g., conflict over sex-ratio determination]
--causes & consequences of sexual deception [e.g., in some mammal species, males are indistinguishable from adult females for some time before expressing secondary sexual characteristics (see, e.g., mantled howler monkeys, Alouatta palliata)]
--selfish tactics & strategies that promote sociality [e.g., "social cohesion"]
--implications: "heirs & spares"
--mechanisms of conflict-management & conflict-resolution in eusocial taxa
--n.b. Ratnieks FLW, Wenseleers T (2005) Policing in insect societies. Science 307: 54-56.
--alternative reproductive strategies and conflict-resolution/conflict-management
--n.b. Sachs JL, Mueller UG, Wilcox TP, Bull JJ (2004) The evolution of cooperation. Q. Rev. Biol. 79: 135-160.
--policing x age, sex, class/SES, race, etc.
--Is multiple-mating by females rare in vertebrates?
--causes & effects of totipotency; ubiquitous in vertebrates?
--genetic basis of sterility
--mechanisms of kin discrimination
--What traits differentiate members of classes [within & between]?
--relevance of behavioral flexibility & phenotypic plasticity to conflict-management & conflict-resolution [also, flexibility of group structures]

Thursday, April 11, 2019

Review of Tim Clutton-Brock's, Mammal Societies (by Clara B. Jones, 2016)

Mammal Societies*
Tim Clutton-Brock**
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; corrected and revised 4/11/2019]

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, as well as, the climate, as well as, 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 of a higher social grade than "communal." 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”), group-living has a long history in these animals (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, 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. 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 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 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 (many important "behavior" papers that would classify as Ecology are missing, (e.g., 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, p 48-52). 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., OikosFunctional EcologyJournal 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)


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/

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

**This text is a literature review rather than a synthesis. By titling his book, Mammal Societies, Clutton-Brock boldly suggests that he intends the volume to be compared to E.O. Wilson's, Insect Societies [Belknap/Harvard, 1971]. By implication, Clutton-Brock indicates that he intends to be compared to E.O. Wilson. Behavioral Ecologists, Functional Trait Ecologists, and Population Ecologists will, ultimately, determine how to classify Clutton-Brock's review. To date, no synthetic treatment of group-living mammals has been written comparable to Wilson's 1971 treatment of social insects. [ review]

Review of Robert L. Trivers' Memoir, Wild Life (by Clara B. Jones, 2016)

Wild Life: Adventures of an Evolutionary Biologist
Robert L. Trivers
Biosocial Research
New Brunswick, NJ
225 pages
$9.58 (Paperback and Kindle)

Reviewed by Clara B. Jones, Asheville, NC, USA (February, 2016; slightly revised, 4/11/2019)

To dispense with preliminaries, I have interacted with Robert L. “Bob” Trivers intermittently since I was in graduate school but have never been in his “inner circle.” I requested a complimentary copy of Wild Life from Robert, telling him that I intended to review it for a journal that was, at the time, undetermined. Robert was enthusiastic about the idea and sent the memoir. I have reviewed a number of books for ISBE Newsletter so it was logical for me to consider it as the venue for publication, particularly, since I speculated that many readers would be interested. I appreciate Andreas Svensson for giving me this opportunity.

In addition to several other biologists (e.g., Louise Emmons, Dan Janzen, Russ Lande, Nancy Moran, Steve Stearns, Mary Jane West-Eberhard, Don E. Wilson, EO Wilson), I consider Trivers to be a National Treasure. Against numerous odds, he has risen to the top of his field, having published papers that are fundamental contributions to Social Biology, generators of immeasurable bodies of systematic and informal research and publications, as well as, continuing streams of productive thought—among his peers, other scientists, educators, students, journalists, and the general public. Many persons in and outside the scientific community will purchase a copy of Wild Life hoping, even, expecting, to find inside their names or mention of one of their vivid memories with Robert. Most of these men and women will be crushed, and I can think of four or five who will never recover. Robert's new book should have included a detailed index, not only for reference purposes, but, also, to prevent time wasted by some who would otherwise rifle through the book in search of evidence that Trivers considers them worthy of mention.

In the literary world, a memoir belongs to the genre, Creative Nonfiction. Wild Life, however, for the most part, appears to be uncontrived, a convincing example of a brilliant, though, controversial, figure telling it as he truly sees it. As the saying goes, “What you see is what you get.”, though Robert is clear to point out that he is unable to measure the full extent to which deception and self-deception influenced this project. After reading Wild Life, I was left with several messages, one being that its author has written a memoir hoping to determine the arc of his legacy. With the exception of Chapters 14 and 15, he crafts his story, as he has presented all of his ideas, with clinical, even, scapular, precision. There is a sense in which the dominant theme of the book can be summarized by a single observation expressed on page 186 when speaking of W.D. Hamilton: “I thought of Bill as perhaps the greatest evolutionary theorist since Darwin. Certainly, where social theory based on natural selection is concerned, he was our deepest and most original thinker.” Many would place E.O. Wilson in second place. However, in Wild Life, as well as, elsewhere, Robert seems of the opinion that Wilson is greatly overrated (an opinion with which I disagree). Though he does not say so explicitly, Trivers likely considers himself to hold second rank after Hamilton, a self-assessment that many would challenge if only because of the author's non-normative record of behavior. Nonetheless, as Robert told a reporter at Rutgers University in 2014, “I don’t want to sound immodest, but I am one of the greatest social theorists in evolutionary biology alive, period.”

Wild Life, dedicated to Robert's teacher, William H. Drury, Jr., comprises fifteen chapters, seven of which, in addition to numerous additional remembrances, concern his life and research in Jamaica. He reports, with obvious pride, that all of his five children are “American/Jamaican,” referring to himself as an “out-breeder” created by his peripatetic experiences as the son of a career diplomat. For decades, I was an obsessive reader of the print-version of The New York Times. One day in 1987, scanning the obituary page, I noticed the name, Howard Trivers [sic, no middle initial], and, because, at that time, I had received second-hand reports of Robert's life from one of his close friends, I determined from relevant details that the deceased was the evolutionary biologist's father. Among other prominent roles in the U.S. Department of State, Howard Trivers had been Director of its Office of Research and Analysis. It was impossible not to note that the diplomat's obituary included no personal information—no mention of parents, a wife, or other family members. I had been told that Robert had a very contentious relationship with his father, in part, because of the latter's profession. Robert has only mentioned his father to me once, in passing; thus, I was not totally surprised to find virtually no reference to his family, including his mother, in Wild Life. For this reason, combined with the, sometimes shocking, even, disturbing, particulars of his life, Robert would provide a Freudian scholar with copious material and room for speculation (e.g., Oedipal failure?). In addition to passing mention of his “family of origin” and his children, the Preface expresses the author's opinions about the conventional lives of scientists (“This kind of life never appealed to me.”), and the remaining few paragraphs introduce the reader to themes that follow.

Chapter 1 is revealing to all students of Trivers' work. He documents his early precocity in mathematics, particularly, The Calculus. I consider myself an amateur student of the thinking strategies of famous scientists. Many population ecologists, for example, think like physicists, characterizing genes and other events as mass flowing in space and time. Ecosystem ecologists, on the other hand, are likely to think, not only spatially, but at multiple scales at once. Robert's mind is that of a quantitative modeler expertly identifying and manipulating decision rules. A limitation but, even, more, a strength, of his mostly verbal theories is that they bypass complexity to identify fundamental principles of natural selection for mechanisms and functions of general import. Trivers reveals that Drury taught him to begin with interesting questions about human behavior, and Robert has exhibited a remarkable ability to choose topics basic to non-human, as well as, human, Social Biology, always cognizant of intra- and inter-individual conflict (-of-interest) and of genetics operating at the level of individuals, constrained by Hamilton's Rule. While I imagine there is intuition and art involved in Trivers' generative processes, I think his successes can be attributed, primarily, to his cogent choice of topics and his ability to write with laser clarity, as close as verbal models can come to mathematical ones. In my humble opinion, Robert is a better verbal modeler than Charles Darwin.

Chapters 2 and 3 describe early experiences conducting fieldwork and the impact of Drury and Ernst Mayr, respectively, on the development of the memoirist's early thinking, publications, and career. Robert convincingly communicates the extent to which he honors these men, and he shares with candor the pivotal role they played in the formation of some of his most important ideas. Trivers has reason to be confident that his acknowledgments of others' inputs will not reduce his reputation and that, though some critics may attempt to diminish his project, particularly, posthumously, Robert's theories are not subject to claims that they are derivative. Chapter 4 is titled, “I Become a Lizard Man in Jamaica,” describing how he became “a green lizard freak” after accompanying Ernest Williams there as a research assistant. Some readers will be offended by both men's evaluation of primatologists and, by implication, Anthropology as a field (but, see Chapter 6). In another chapter he denigrates Psychology, and it is clear throughout the memoir that Robert's opinion about what constitutes a Science is a narrow one.

Wild Life is peppered with interesting facts about lizards and other animals, as well as, snapshots of geography and human nature. Chapters 5, 7, 8, 9, and 10 recount a variety of experiences in Jamaica, some of them life-threatening, as well as, significant friendships, mostly with men. The only women who receive a lingering nod in the memoir are “mother-in-law,” “Miss Nini,” and her daughter, Robert's “wife,” Lorna, mother of four of his children. Even though these chapters, and a few other accounts, document Robert's capacity for deep, sincere, and reciprocated feelings, he sometimes refers to friends using clinical, seemingly detached, language.

Chapter 11 is an interesting one in which the author reminisces about his relationship to Huey Newton and the Black Panther Party, and Chapter 12 continues descriptions of his entanglements with intra-specific conflict, including, incarceration. Robert seems not to have learned a litany from Behavioral Ecology that the costs of aggression (or, spite) usually outweigh its benefits (see the self-analysis in Chapter 15, and Parker 1974). Chapter 13, titled, “Vignettes of Famous Evolutionary Biologists,” suggests that, in addition to Drury, Mayr, and Williams, Richard Dawkins and W.D. Hamilton, effectively, complete Trivers' list of illustrious figures in the field who have influenced him and his ideas, and in this chapter, Robert includes a few sarcastic paragraphs about Stephen J. Gould that I consider gratuitous and unnecessary.

The final two chapters are intimate in nature, Chapter 14 is titled, “Ambivalence About Jamaica,” describing the unsettling and increasing rates of violence there. Some readers will find the final chapter haunting since Robert candidly assesses personal failings and outlines his burial plans. I was surprised that he had nothing to say about politics or the state of the world (e.g., climate change, income inequality, racism, biodiversity loss, terrorism), if only to inform the reader about how his opinions and values might have changed since his Black Panther days (“One man's terrorist is another man's freedom fighter.”, as the CIA used to say). His life is not as dark as it may appear, however, since Robert has recently outlined several proposals for future research, specifically, speciation processes (with Koos Boomsma); evolutionary heterogamety; natural selection of honor killings; evolutionary dynamics of homosexuality; and, human evolutionary genetics.

It would be remiss and unrealistic not to provide some academic critique of Trivers' work, and I consider it appropriate to suggest a couple of limitations*. Since I was introduced to his publications in the 1970s by Behavioral Ecologists at Cornell, it has concerned me that Robert's research fails to reflect the importance of Evolutionary Ecology, particularly, evolution in changing environments about which there is a significant literature pre-dating Robert's first publication (e.g., Levins 1968, Lewontin 1957). Though Evolutionary Ecology is relatively recent as a systematic discipline, Robert has a terrific grasp of Population Genetics and G x E interactions, an operation receiving limited treatment, at best, in his publications (e.g., How do “selfish” genes and social traits behave when conditions vary or along gradients? When and under what conditions is social behavior situation-dependent? ...flexible?). Furthermore, his “feel” for statistical thinking is that of an expert, and I would expect more treatment of variation and deviations from central tendencies in his canon.

On the other hand, one way that Trivers' work achieves elegance, is by simplifying complex phenomena; thus, environmentally-focused, realistic theories might not have been as successful, productive, or fundamental. In a sense, the author's insights are primitive in the deep, honorific sense that the word is employed to describe some treatments in pure mathematics. Nonetheless, all theoretical work of import is subject to vetting by subsequent theory, models, experiments and other empirical tests. Already, a few researchers have modified certain details of Trivers' theory of sex ratio selection, and his ideas about parental investment and sexual selection have been challenged by some feminist biologists. Related to any discussion of Robert's legacy, in Wild Life, the memoirist states how important the appreciation of conflict (genetic and whole organism, intra- and inter-individual) has been to his success. In my opinion, this observation confirms Trivers' understanding that asymmetries produce differential “fitness optima” and that differential (asymmetric) phenotypes are exposed to environments upon which selection may act. I strongly recommend Wild Life to all who are interested in Ecology and Evolutionary Biology, not only, for its explication of “wild” experiences, but, also, for insights into how a stunning mind works.


Levins R (1968) Evolution in changing environments: some theoretical explorations (No. 2). Princeton University Press.

Lewontin RC (1957) The adaptation of populations to varying environments. Cold Spring Harbor Symp Quant Biol 22: 395-408.

Parker GA (1974) Assessment strategy and the evolution of fighting behaviour. J Theor Biol 224: 115-126,

*First, no American social biologist can compete with Wilson's expertise as a student of a single social group, ants, in Wilson's case. Second, IMO, The Insect Societies (1971) is the greatest book ever written in Social Biology, indeed, in Animal Behavior and Ethology as a whole.

Third, unlike E.O. Wilson, Trivers is not a synthesizer, though his most heralded papers have general import. Trivers has not communicated much interest in a search for general patterns--within, between, and across taxa. Also, again, in contrast to E.O. Wilson, Trivers' canon pays scant attention to Genotype<----->Phenotype<----->Environment<-----> causes and effects. One seeks, for the most part, in vain, to locate Ecology--abiotic & biotic Environments [however conceptualized]--in Trivers' writings. Furthermore, to my knowledge, Trivers has not emphasized the topics--group-formation, group maintenance, and the environmental conditions facilitating the emergence of sociality [which may or may not follow group-formation]. Especially pertaining to the latter are the topics, competition and differential access to limiting resources, as well as, limiting resource dispersion [distribution and abundance in time and space].

Trivers may be one of the last remaining extreme genetic thinkers. He typically asks a question, then, considers what consequences would obtain given alternate, pairwise combinations of related individuals [parents, full sibs: 1/2; first cousins: .1/8, etc.]. This approach has yielded several fundamental papers; however, Trivers' work does not satisfactorily address variations in inter-individual interactions nor evolution in heterogeneous regimes nor phenotypic plasticity nor the principle that behavior is condition-dependent. In other words, an actor & a recipient, whatever their "r" [coefficient of relationship], will respond relative to "b" [benefits to recipient] and "c" [costs to actor ("donor"--of reproductive units)], rather than, strictly, "r" [Hamilton's Rule: rb - c >0].

Trivers' literal logic based, apparently, on "r" alone, may reveal one unfortunate consequence of the term, "kin selection" that leads many to assume that it is always in ego's favor to exhibit social behavior towards kin. The latter assumption may be an assumption behind Trivers' [very successful and justifiably heralded] publications. Furthermore, as I [and several others before me (thanks to James Marshall and Andrew Bourke for making me aware of this literature)] have suggested, it may be useful to consider the role of competition influencing behavior between actor [donor] and recipient and to question whether Hamilton's Rule adequately incorporates the consequences for actor and recipient and for the expression or non-expression of cooperation or altruism [i.e., "social behavior"] of interindividual competition [for limiting resources, e.g., food, mates, space].

Thus, sometimes, kin may be ego's "worst enemy," a litany of Behavioral Ecology [it may not be beneficial for ego to assist the reproduction of kin; it may be in the interest of ego to assist the reproduction--depending upon environmental regime] where predation is non-random by genotype [where cooperation or altruism toward a relative would increase ego's chances of becoming prey]. But, complicating the matter, in certain conditions, death, however, defined [e.g., self-induced, other-induced], can benefit kin. Clearly, systematic empirical and theoretical studies, in addition to modeling, are needed.

In the final analysis, however, the impressive success of Trivers' verbal models based on "r" may demonstrate the power of Hamilton's Rule to predict a very broad array of the social acts [cooperation, altruism] observed in Nature, including, Human Nature. However, we should not only ask, "What is "r"?, but, also (or rather?), "'r' relative to what?" According to Hamilton's Rule, the effects of "r" are expected to be constrained by the components that comprise "b" & "c".

Clara B. Jones (
Asheville, NC, USA (now, Silver Spring, MD, USA)
February, 2016 In International Society of Behavioral Ecology Newsletter

Wednesday, April 10, 2019

Review of E.O. Wilson's new book, Genesis (Clara B. Jones, 2019)

Genesis: the deep origin of societies.
Edward O. Wilson
Liveright Pub. Co. (W.W. Norton & Co.)
153 pp

Reviewed by Clara B. Jones, Ph.D. (2019)

"The key to the sociobiology of mammals is milk." EO Wilson (1975)

Social evolution is an important topic of investigation by behavioral ecologists and evolutionary biologists. The two categories of sociality, cooperation and altruism (Hamilton 1964), have arisen infrequently across vertebrate taxa because, in propitious environmental regimes, group-level coordination and control is usually derailed by “cheaters” who fail to comply with group norms. As Wilson pointed out in 1971, groups of cooperators and altruists characterize the most “successful” (i.e., widely distributed) extant terrestrial taxa—social insects and humans. In his new book, Genesis [sic], the entomologist, E.O. Wilson, winner of the Crafoord Prize in 1990 and America's premier social biologist*, assesses the emergence of eusociality, the highest social “grade” (Wilson 1971). 

Perhaps the primary contribution of this brief book is that Wilson classifies humans as eusocial, a system characterized by overlap of generations, cooperative brood-care, and non-reproductive "helpers." If Wilson is correct, humans would be classified, "primitively" eusocial (Wilson, 1971) or Totipotent Eusocial [TE; see "General Mammalian Patterns" blogpost, this blog, #28, 9/19/19], since most human "helpers" (except post-menopausal females or other sterile persons) are expected to be "totipotent"—"helpers" capable of independent reproduction, able to reverse their non-reproductive status [TE]. Members of permanently sterile “castes,” are labeled, “advanced” eusocial (Wilson, 1971), and Wilson's treatments in this book suggest to me that he might be inclined to label permanently non-reproductive human groups as “caste”-like, associations that should be investigated, as well, for the possible presence of "temporal division-of-labor" ("age polyethism": see Wilson, 1971)..

The first five chapters of Genesis include limited explications of some topics (e.g., “multi-level” selection, “phenotypic plasticity”). Wilson clearly explains that the conceptual frameworks of Genesis are Maynard Smith & Szathmáry's (1995) classic treatment of “major transitions of evolution,” as well as, “multi-level” and “group selection,” terms used interchangeably. In Chapter 6, Wilson appears to be primarily interested in proffering a defense for Charles Darwin's explanation for the evolution of sterile castes—an argument based on group selection which Wilson defines as follows: "...within groups, selfish individuals win against altruists, but groups of altruists beat groups of selfish individuals" [attributed to David Sloan Wilson]. Among impediments to "proofs" of "group selection," defenders need to show how "cheaters" are controlled within groups, demonstrations that will require empirical studies.

Here and throughout the book, Wilson fails to incorporate the ecological literature showing, for example, that intragroup competition is generally stronger than intergroup competition or that behavioral ecologists have, since the early 1980s, advanced general criteria for the evolution of cooperative groups (e.g., Emlen 1982) and of eusociality (e.g., Crespi 1994; also see, Choe & Crespi 1997, Crespi et al. 2004 [see, especially, p 66 & pp 73-74], Bourke & Franks 1995, Bourke 2011); West-Eberhard 1975 on p 169, col. 3, par. 2 in Queller & Strassmann 1998 pp 169-170). More specifically, Wilson fails to cite other researchers who have advanced the idea that humans are eusocial (e.g., Foster & Ratnieks 2005, Jones 2011, Crespi 2014).

Nonetheless, combined with related studies (e.g., Emlen 1982, Emlen 1984, Hrdy 2011), there seems to be an expanding literature justifying systematic and quantitative investigation of eusociality in humans, in particular, and in vertebrates, broadly, including, standardization of terminology, experiments, and modeling (e.g., “agent-based” modeling). For an early, published paper that might generate ideas for these future projects, Lotka (1928) is suggested.

The final chapter (7), titled, “The human story,” reviews “transitions” to eusociality across apes, from chimpanzees (Pan troglodytes), as well as, bonobos (P. paniscus) continuing to Australopithecus and the Homo line. Unlike other chapters, this one emphasizes the importance of ecological factors (habitat) for the evolution of social mechanisms among hominids and their ancestors, and Wilson endorses the “social brain hypothesis” as well as the importance of fire for the “rapid evolution” of large brains and the facilitation of group-life, respectively—as well as, their consequent adaptations. Interestingly, in this chapter (p 114), the author compares human eusociality to other social mammals, in particular, African wild dogs, demonstrating that he is prepared to classify “other mammal species,” eusocial, in addition to the social mole rats (see Jones 2014, pp 48-52)****. For another interesting example, see Dwarf Mongoose.

Wilson does not dismiss “kin selection;” but, he holds that “multi-level” or “group” selection is the primary driver of the route to eusociality, behind which kin effects may follow [he may be right; see this lecture, "Ecology Of Societies," by Simon Levin of Princeton: ].

Most social biologists are certain to be surprised to read Wilson's claims that "Hamilton's Rule" suffers "fatal weaknesses" and is no longer "useful (see Bourke 2011, Bourke & Franks 1995)." Wilson does not support these flippant statements with mainstream literature about which there is wide consensus in favor of Hamilton's Rule, and nowhere in his text does he assess assumptions underlying considerations of differential benefits to recipients of social behavior (cooperation or altruism) or differential costs to "donors," terms subsumed in Hamilton's Rule (see, for example, Bourke 2011, Marshall 2015). Related to this, Wilson all but completely avoids optimality [cost-benefit] thinking, and social biologists will, I think, find his explication of group selection obfuscating when applied to genetics, including the assertion that population geneticists have shown the verity of group selection.

Nonetheless, researchers, including, evolutionary psychologists, human biologists, and anthropologists, will derive many testable hypotheses from Wilson's claims, among the more provocative of them, the statement that division of labor by human professional categories is evidence of eusociality and group selection (that they are "caste-like)." I am led to wonder if some human guilds might be characterized by high r (coefficient of relationship), a possibility that would be easy to test. Likewise, guilds, and other formal human groups (e.g., fraternities and sororities, political groups, and the like), should be investigated for evidence of "temporal division-of-labor" ('age polyethism": see Wilson, 1971).

In service to economy, organization, and clarity, Genesis might have been more wisely presented as a "tight" technical paper rather than a manifesto in book form, though Wilson deserves to be applauded for advancing bold ideas, for insisting that human social behavior be subjected to the same analyses that we apply to non-human animals, and that, ultimately, evolutionary explanations will need to be "gene-centered," a long-standing hallmark of Wilson's approach (e.g., Wilson 1975) and that of the heralded evolutionary biologist, Robert Trivers (see, e.g., Trivers 1985 and the remarkable Trivers & Hare, 1976**; also see citations by Bernie Crespi). I recommend this creative and controversial text to specialists, students, and the general audience. It will raise many questions, stimulate thought, and, hopefully, generate conversations*** and research** about variations in human socio-sexual units, as well as, the origins and evolution, the causes and consequences, of group life across all vertebrates.

Bourke AFG (2011) Principles of social evolution. Oxford University Press, Oxford.
----, Franks NR (1995) Social evolution in ants. Princeton [NJ] University Press.
Choe JC, Crespi BJ (1997) The evolution of social behavior in insects and arachnids. Cambridge University Press, London.
Crespi BJ (1994) Three conditions for the evolution of eusociality: are they sufficient? Insectes Sociaux 41(4): 395-400.
Crespi BJ (2014) The insectan apes. Human Nature 25(1): 6-27.
Crespi BJ, Morris DC, Mound LA (2004) Evolution of ecological and behavioural diversity: Australian Acacia thrips as model organisms. Australian Biological Resources Study, Canberra.

Emlen ST (1982) The evolution of helping I: an ecological constraints model. American Naturalist 119: 29-39.
Emlen ST (1984) Cooperative breeding in birds and mammals. Pp 305-339 in Behavioral ecology an evolutionary approach, 2nd ed. (JR Krebs, NB Davies, eds.). Sinauer, Sunderland, MA.
Emlen ST, Oring L (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197: 215-223.
Foster KR, Ratnieks FLW (2005) A new eusocial vertebrate? Trends in Ecology and Evolution 20(7): 363-364.
Frank SA (1995) Mutual policing and repression of competition in the evolution of cooperative groups. Nature 377: 520-522.
----(2003) Repression of competition and the evolution of competition. Evolution 57(4): 693-705.
Hamilton WD (1964) The genetical evolution of social behavior. Journal of Theoretical Biology 7: 1-52.
Holldobler B, Wilson EO (1990) The ants. Belknap (HUP). Cambridge.
Hrdy SB (2011) Mothers and others. Belknap-Harvard.
Jones CB (2011). Are humans cooperative breeders? A call for research. Archives of Sexual Behavior 40(3): 479-481.
----(2014) The evolution of mammalian sociality in an ecological perspective. Springer, NY.
Lotka AJ (1928) Sterility in American marriages. PNAS 14(1): 99-108.
Marshall JAR (2015) Social evolution and inclusive fitness theory: an introduction. Princeton University Press, Princeton, NJ.
Maynard Smith J, Szathmáry E (1995) The major transitions of evolution. W.H. Freeman Spektrum, New York.
Queller DC, Strassmann JE (1998) Kin selection and social insects. BioScience 48(3): 165-175.
Trivers RL (1985) Social evolution. Benjamin-Cummings Pub. Co., San Francisco.
Trivers RL (2015) Wild Life. Biosocial Research. New Brunswick, NJ. [& e-book,]

----, Hare H (1976) Haplodiploidy and the evolution of the social insects. Science 191(4224): 249-263.
West-Eberhard MJ (1975) The evolution of social behavior by kin selection. Quarterly Review of Biology 50: 1-33.
Wilson EO (1971) The insect societies. Belknap/Harvard, Cambridge, MA.
----(1975) Sociobiology. Belknap/Harvard, Cambridge, MA.
Wittenberger JF (1980) Group size and polygamy in social mammals. Am. Nat. 115: 197-222.
Yamamura N, Higashi M (1992) An evolutionary theory of conflict resolution between relatives: altruism, manipulation, compromise. Evolution 46: 1236-1239.

*First, no American social biologist can compete with Wilson's expertise as a student of a single social group, ants, in Wilson's case. Second, IMO, The Insect Societies (1971) is the greatest technical book ever written to date (and The Ants [Holldobler & Wilson, 1990] the greatest popular book ever written to date) in Animal Behavior and Ethology.

Third, unlike E.O. Wilson, Robert L. Trivers, also a renowned social biologist, winner of the Crafoord Prize in 2007, is not a synthesizer, though Trivers' most heralded papers have broad import. Trivers has not communicated much interest in a search for general patterns--within, between, and across taxa. Also, again, in contrast to E.O. Wilson, Trivers' canon pays scant attention to Genotype<----->Phenotype<----->Environment<-----> causes and effects. One seeks, for the most part, in vain, to locate Ecology--abiotic & biotic Environments (however conceptualized)--in Trivers' writings. Furthermore, to my knowledge,

Trivers has not emphasized the topics--group-formation, group maintenance, and the environmental conditions facilitating the emergence of sociality (which may or may not follow group-formation). Especially pertaining to the latter are the topics, competition and differential access to limiting resources, as well as, limiting resource dispersion (distribution and abundance in time and space). A litany of Behavioral Ecology is that, in some environmental regimes, kin may be ego's worst enemy. Such conditions may occur, for example, where there is intense local competition for limiting resources [above some critical threshold of decreasing reproductive gains].

Trivers may be one of the last remaining extreme genetic thinkers among living social biologists (see my review of his memoir, Wild Life [2015] linked above). He typically asks a question, then, considers what consequences would obtain given alternate, pairwise combinations of related individuals [parents, full sibs: 1/2; first cousins: 1/8, etc.]. This approach has yielded several fundamental papers; however, Trivers' work does not satisfactorily address variations in inter-individual interactions nor evolution in heterogeneous regimes nor phenotypic plasticity nor the principle that behavior is condition-dependent nor the litany of Behavioral Ecology that patterns of  group-living will "map" onto dispersion [distribution and abundance in time & space and abiotic phenomena (e.g., climate)] of limiting resources nor the ideas that females are energy maximizers--males, time minimizers. Trivers does not seem to be sensitive to Hamilton's "b" & "c" whereby an actor & a recipient, whatever their "r" [coefficient of relationship], will respond relative to "b" [benefits to recipient] and "c" [costs to actor ("donor"--of reproductive units)], rather than, strictly, "r" [Hamilton's Rule: rb - c >0].

Trivers' literal logic based, apparently, on "r" alone, may reveal one unfortunate consequence of the term, "kin selection" that leads many to assume that it is always in ego's favor to exhibit social behavior towards kin. The latter assumption may be an assumption behind Trivers' (very successful and justifiably heralded) publications. Furthermore, as I [and several others before me (thanks to James Marshall and Andrew Bourke for making me aware of this literature)] have suggested, it may be useful to consider the role of competition influencing behavior between actor [donor] and recipient (see Yamamura & Higashi, 1992)  and to question whether Hamilton's Rule adequately incorporates the consequences for actor and recipient and for the expression or non-expression of cooperation or altruism (i.e., "social behavior") of interindividual competition for limiting resources (e.g., food, mates, space, etc.).

Thus, sometimes, kin may be ego's "worst enemy" [it may not be beneficial for ego to assist the reproduction of kin; it may be in the interest of ego to assist the reproduction--depending upon environmental regime] where predation is non-random by genotype [where cooperation or altruism toward a relative would increase ego's chances of becoming prey]. But, complicating the matter, in certain conditions, death, however, defined [e.g., self-induced, other-induced], can benefit kin. Clearly, systematic empirical and theoretical studies, in addition to modeling, are needed.

In the final analysis, however, the impressive success of Trivers' verbal models based on "r" may demonstrate the power of Hamilton's Rule to predict a very broad array of the social acts (cooperation, altruism) observed in Nature, including, Human Nature. However, we should not only ask, "What is "r"?, but, also (or rather?), "'r' relative to what?" According to Hamilton's Rule, the effects of "r" are expected to be constrained by the factors comprising "b" & "c". For example, when and under what conditions are kin, enemies?

**See comments on this paper in Holldobler & Wilson (1990, p 184)

***For example, cooperation and altruism might occur by way of "mutual policing," coercion, force, or persuasion, in addition to, "self-restraint" (see, especially, Steve Frank's work, in particular. 1995 and 2003).

****Addendum 4/26/2019: Regarding the ideas that humans are "cooperative brreeders" (e.g., Hrdy 2011) and that "cooperatively-breeding" mammals should be classified, "eusocial" (Jones 2014), I am going to go out on a limb to suggest that, based upon my reading to date on mammal, including, human, group-living patterns, mammalian "cooperative breeding" evolved from groups of communal females, and their offspring, that may or may not, then, evolve to share "economic" tasks, including care of young [see epigraph]...since females, ceteris paribus, are expected to be "energy-maximizers," thermal efficiency, broadly defined, will be paramount as a selective factor and in determining optimal "inclusive fitness maximizing" (see Jones 2014, Chapter 3). Anthropologists specializing in human "cooperative breeding" hold that the system evolved via monogamy, as it is thought to have done in insects and birds. However, mammalian sociosexual systems generally exhibit "sexual segregation" ("solitary" dispersion between the sexes) and, in mammals, monogamy is derived. Related, Mammal sociosexual systems and group structure are thought to result from the tendency of females to select rich patches of [limiting] food and that of males to select the largest possible number, sometimes, an aggregation, of females (Wittenberger 1980, Emlen & Oring 1977).

In summary, it seems to me that the more likely "route" to eusociaity in humans would have been via communally nesting mammalian ancestors, particularly, since monogamy is "derived," mammals are very likely to exhibit a "sexually-segregated" ["solitary"] socio-sexual organization, monogamy is relatively rare, and, in humans, at least, monogamy is often imposed by some authority. Routes to eusociality that might be applied to humans have, also, been proposed by West-Eberhard (1975) and by Queller & Strassmann (1998: "fortress defenders" and "life insurers") [see Queller & Strassmann (1998) for a brief summary of these ideas on pp 169-170]. These issues need to be unpacked.

Clara B. Jones is a retired behavioral ecologist living in Silver Spring, MD (USA).