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

2015

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, though "inclusive-fitness maximizing" and sexual selection are fundamental to Robert's writings, his body of work fails to reflect the importance of Evolutionary Ecology, particularly, life-history evolution (e.g., Stearns 1976), as well as, 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 is aware of Population Genetics and G x E interactions, an operation receiving limited treatment 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?). As important as his neglect of evolution in heterogeneous regimes [Population Ecology] & of life-history evolution, Robert, in addition, fails to address Behavioral Ecology, especially, the fundamental & "classic" work of John Hurrell Crook (1964: group structure in response to limiting resource dispersion [distribution and abundance] in Time & Space). All of these concerns relate to the "condition-dependence"/"situation-dependence" of organismic responses & adaptation, or, lack thereof, in the context of "local adaptation."

On the other hand, Robert's “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. Of particular import, is that, regardless of having produced seminal papers in his early career, as well as, an interesting book on sociality (Trivers 1985), Robert has shown little interest in the EVOLUTION of sociality [as, Major Transitions Approach: West et al. 2015], per se, as per transitions from solitary breeding, to breeding in groups [including, group formation & group maintenance], to Presocial state, to Subsocial state, to Cooperation [as per Hamilton '64], & to Complex Sociality (reproductive division-of-labor; specialization as per Eusociality variously defined); see, Wilson 1971's schema]. Furthermore, treatment of social evolution in comparative perspective [within & between genera, families, orders, classes] is lacking in Robert's oeuvre.

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.

References

Crook JH (1964) The evolution of social organization and visual communication in the weaver birds (Ploceinae). Behaviour Supplement #10: 1-201.

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,

Stearns SC (1976) Life-history tactics: a review of the ideas. Quart Rev Biol 51: 3-47.

Trivers RL (1985) Social evolution. Benjamin-Cummings.

West SA, Fisher RM, Gardner RA, Kiels ET (2015) Major evolutionary transitions in individuality. PNAS 112(33): 10112-10119.

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

*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 (foucault03@gmail.com)

Asheville, NC, USA (now, Silver Spring, MD, USA)

February, 2016 In International Society of Behavioral Ecology Newsletter

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

Genesis: the deep origin of societies.

Edward O. Wilson

2019

Liveright Pub. Co. (W.W. Norton & Co.)

153 pp

$15.88

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:

 https://www.youtube.com/watch?v=rQUsApf3RHs ].

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.

References

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.

https://www.environment.gov.au/science/abrs/publications/thrips

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, 2^nd 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, amazon.com] 

http://vertebratesocialbehavior.blogspot.com/2019/04/review-of-robert-l-trivers-memoir-wild.html

----, 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.]. Trivers' canon is about mechanisms, not, about causes. His 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). 

When to exhibit Social Behavior [Cooperation, Altruism]? Clara B. Jones [Graph, Legend]

Fig. 1. When should an Actor or a Recipient exhibit Social* Behavior [Cooperation, Altruism]? Clara B. Jones, 3/13/2019

1. This [idealized] graph**** depicts & predicts when an [idealized] organism--an Actor or a Recipient--should give/exhibit Cooperation or Altruism, defined, formally, as those interactions during which the Recipient benefits [in relative reproductive units].
2. X-axis: Time [T], Energy [E] investment in Social Behavior [reflects organism's T/E budget for a given interaction].
3. Y-axis: Costs [C, in reproductive units to Actor or Recipient] or Benefits [B, in reproductive units to Actor or Recipient] to Inclusive Fitness** [IF= selfish reproductive units (usually, & clasically,  offspring, though, offspring might be delayed, such as when transaction in wealth or other goods--see "Altruism" below) + reproductive units of kin]. r, coefficient of relatedness, is incorporated in measure/estimate of IF [how to measure?].
4. C rise or reach asymptote over T. Costs, for Actor or Recipient, or both, may prevent Cooperation or Altruism between kin when, for example, Cooperation or Altruism increases Competition [for limiting resources such as food, mates, burrows], increasing [for ego or ego's offspring] likelihoods of  dispersal, "competitive exclusion" [demand for ~identical limiting resources], death, etc. Cooperation and Altruism are expected, by definition, to be responses for the avoidance or neutralization of Competition.
5. B rise, then decrease over T.
6. "x" represents the optimal point at which an Actor or a Recipient should exhibit Cooperation [both Actor and Recipient gain reproductive units] or Altruism. [Actor loses, Recipient gains reproductive units]. "x" is the extension to the X-axis of the vertical, black line connecting the points with the greatest separation between the C and B curves--where B > C. "x" is the idealized point maximizing inclusive fitness benefits.
7. The shaded area represents the zone around "x" for which Actor's benefits from Social Behavior are highest. Ideally, the broken vertical lines extend vertically & downward from those points on either side of "x" on the B curve at which the B curve first begins to descend. The shaded area represents the zone of maximal benefit to Inclusive Fitness of A or B, in this case, maximum benefit from an act of Cooperation or Altruism ["IF maximizing"].
8. Actor & Recipient curves and values will usually be asymmetric, by definition [possibly, even, for clones (e.g., identical twins)]. In other words, zones of maximal benefit from social behavior should differ for Actor and Recipient. Overlaying Actor's & Recipient's curves will determine whether there is overlap between Actor & Recipient zones of greatest benefit to ego from Cooperation or Altruism. If there is overlap, the zone of mutual benefit is defined, so that Actor & Recipient should exhibit Cooperation [+, +] within these parameters [of T, E]. If there is no overlap, then conflict arises [between Actor and Recipient &, possibly, kin of one or both].
9. Similarly, an Actor should exhibit Altruism [-, +] to a Recipient when the long-term B of such action[s] outweigh the short-term C [determined by hard-wired Hamiltonian algorithm?].
10. If B from Social Behavior are minimal or non-existent [e.g., low T/E "budget;" little or no overlap between Actor-Recipient zones of greatest benefit], then interactants should adopt an alternate behavior [Alternative Reproductive Behavior--tactic or strategy], such as fight***, avoidance, flight, force, coercion, persuasion, manipulation, exploitation, coexistence--or some combination of these.
11. Group-living organisms experience relatively ongoing "decisions" about how to behave relative to conspecifics; however, it is important to keep in mind that "fitness budgets" change over T and that behavior is condition- [context-] dependent.
12. Ceteris paribus, and on average, curves, B & C, as well as, shapes of zones of maximum benefits for Males [time-minimizers] and Females [energy-maximizers] should differ. Curves, also, are expected to be Age-, Class-, & Role-dependent.

*After Hamilton (1964), "Social Behavior" is defined as Cooperation [both Actor and Recipient gain reproductive units] or Altruism [Actor forfeits reproductive units; Recipient gains reproductive units]
**The term "inclusive fitness" can be confusing since, technically, "fitness" is the frequency of an allele in a population averaged across the reproductive success of all individuals in the population bearing the allele, leading one to inquire how important it is to measure individual variation of traits [since individual variation will be subsumed in the measure of an allele's "fitness"].
***As pointed out by Geoff Parker [1974], aggression should not usually be a first resort because the C of damaging behavior generally outweigh the B.
****The same graphical/conceptual framework could be used for Coexistence if axes modified so that X-axis= savings in T, E to Mean fitness of allele 1 [or 2]; Y-axis= B, C from T, E savings to fitness [Mean frequency] of allele 1 [or 2] in a population. In the case of Coexistence, a Community Ecology process, the population would be escaping Competitive Exclusion. [See, also, my 2014 Springer Brief, Ch 2, for discussion of Coexistence in relation to Hamilton's Rule.]

Acknowledgments: Thanks to my son, Luke [M. Luke Jones] for stimulating discussion and for drawing the figure. Further, via e-mail, I asked Andrew Bourke [Univ. of E. Anglia] to comment on this blogpost. On 4/11/2019, I received the following reply [n.b.: my original blogpost above, including, the graph, have NOT been revised subsequent to Bourke's comments]:

1.     Perhaps the X axis needs clarifying a little – after all, time and energy seem to have most relevance in this context insofar as they are proxies for fitness, so then there would be some relationship between the metrics on the X axis and on the Y axis, and how these interact might then require consideration.

2.     It would be good to have concrete, empirical examples of when the scheme in the figure needs invoking, i.e. showing how considering the time/energy investment dimension in the manner advocated in the figure enlarges our understanding of the occurrence of social behaviours.  Personally I find it hard to think of things in the abstract all the time, so even some hypothetical biological examples/applications might be useful.

3.     I think your footnote 8 makes a good point, i.e. that actor and recipient interests need not overlap even for altruistic and cooperative interactions.  This point was explored theoretically in a fairly old paper by Yamamura and Higashi (1992)*****.  Their work does not seem to have been followed up empirically to any great extent, perhaps because the usual assumption that one of the parties has most control over the interaction (in which case conflict is minimised – e.g. an insect larva may often have little choice but to accept the level of care it’s given) holds.

References
Hamilton WD (1964) The genetical evolution of social behaviour. J Theor Biol 7: 1-52.
Parker, G (1974) Assessment strategy and the evolution of fighting behavior. J Theor Biol 47: 223-243.
*****Yamamura N, Higashi M (1992) An evolutionary theory of conflict-resolution between relatives: altruism, manipulation, compromise. Evolution 46: 1236-1239.

http://www.kurims.kyoto-u.ac.jp/~kyodo/kokyuroku/contents/pdf/0827-14.pdf

Fragment: Inferences from West-Eberhard (1975) pertinent to Mammals (Clara B. Jones)

2.4 Inferences Pertinent To Mammalian Sociality Can Be Drawn From West-Eberhard (1975)

West-Eberhard’s (1975) summary of general models of social evolution reducible to mechanisms dependent upon inclusive-fitness maximizing is useful as a reminder that Hamilton’s rule is manifested in several ways, dependent upon local condition, sex, role (e.g., reproductive or helper), and lineage. It is noteworthy that each of the six strategies (1a – 3b) is, in one manner or another, applicable to social mammals and to mammalian females living mutualistically or cooperatively in groups. In insects and most mammals, olfaction is the primary mechanism of communication. Thus, coordination and control of conspecifics is expected to be constrained by the spatiotemporal dynamics of chemical properties (rapid delivery, relatively rapid decay, pheromonal repression of selfishness). Despite interspecific similarities, it is possible to derive inferences from West-Eberhard’s (2005) outline that may pertain, especially, to social mammals.

Inference 1: Because the variance on reproductive success is lower among females than among males, ceteris paribus (Trivers 1972), mammalian females will be more closely related, on average, to other females in their group or population than will males be, on average, to each other, to group or population females, and to each other’s offspring. For the same reasons, a mammalian population is likely to include more females than males, and females are more likely to exhibit sociality.

Inference 2: Trivers’ (1972) model, fundamentally, concerns differential energetic investments by males and females and the life-history trajectories deriving from polymorphic allocation patterns. Thus, because female “fitness budgets” are more constrained energetically that those of males, the reproductive female component of a group or population is expected to be more stable, spatiotemporally, than the dispersion of males in the same population. For the same reason, on average, female turnover is likely to be lower, female survivorship higher, female emigration rates lower than for males.

Verbal Model I was advanced by Trivers (1972) and was not, originally, presented as a general model of social evolution. However, this author predicts that social evolution will be biased by initial reproductive allocations or energetic investments (Schoener, 1971). This verbal model is not limited to evolution by sex, encompasses all conditions in which organisms make (“Hebbian”) “decisions”, including, decisions to join (group-formation), or, remain in (group-maintenance), groups, and has the potential to be developed, qualitatively, and, expressed, quantitatively, as a synthetic formulation.

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Inference 3: On average, since females are “energy-maximizers”, “inclusive-fitness maximizing” is expected to mitigate energy losses, and, on average, females should benefit from transferring some component “fitness budget” to others. Thus, females and their female offspring are likely to be the major donors and beneficiaries of the benefits of cooperation and altruism, and, relative to males in her population, an adult female has more to gain in her reproductive lifetime from facilitation.

Inference 4: Since males, “time-minimizers”, are expected to favor direct over indirect reproduction, “inclusive-fitness maximizing”, a relatively time-intense strategy, is unlikely to characterize reproductive males, on average.

Inference 4: Ceteris paribus, and, depending upon threshold reproductive effects relative to ecological conditions, where males cannot discriminate their own young, they should be indiscriminately selfish, concentrating on mating allocation strategies rather than facilitation of conspecifics.

Inference 5: It follows from “parental manipulation” and “maternal control” models that females can discriminate their mothers and, there own offspring, where females are not “promiscuous” and do not express “favoritism” of a single male during an estrus cycle. On the other hand, cortical circuitry may be favored, permitting females to make “decisions” based on likelihoods of paternity. In order for this neurophysiological strategy to be favored by selection, losses from error must not, on average, compromise relative reproductive success (of the pertinent genotype). It is important to note that “decisions” based on kinship may yield lower group sizes than those based on selfish strategies (Hamilton 1964); thus, the Malthusian optimum for a reproductive female may not concord with idealized mean fitness of her population.

Inference 6: Following from previous inferences, a reproductive female, on average, is expected to lose less from probabilistic tactics and strategies than will a reproductive male of the same population. Related to the previous inference, “inclusive-fitness maximizing” is expected to mitigate the maternal investment : ageing tradeoff for tactical and strategic females, on average, possibly explaining the reproductive advantage of extended post-reproductive lifespan in humans and killer whales: ////.

The previous discussion of West-Eberhard’s (1975) classification (1a-3b) suggests that “inclusive-fitness maximizing” should be more characteristic of reproductive females, on average, than of reproductive males in the same conditions. It is hypothesized that this condition obtains since, theoretically, females are expected to be “energy-maximizers”. The latter life-history strategy should privilege time-intense (“non-damaging”) rather than energy-intense (“damaging”) strategies, theoretically, characteristic of males. Should the aforementioned allocation (thermal) trajectories withstand quantitative, including, experimental, testing, each of them will yield information pertinent to the evolution of mammalian sociality. In particular, on average, each reproductive morph in the same population will respond differentially to density effects that are expected to impact “energy-maximizers” to a greater degree than “time-minimizers” since an increase in population density should correlate positively, ceteris paribus, with increased intensities of competition. Under these regimes, reproductive females should “switch” to or increase dependence upon, time-intense, energy-saving, helper tactics and strategies, including, in some regimes, self- (suicide, “give-up” points) or offspring-elimination (foetal resorbtion, abortion).

Fragment: Where males & females co-reside (Clara B. Jones)

4.3 Where Males & Females Co-reside (Polygynandry; Multi-male, Multi-female Groups): Mammals

More than one reproductive males cohabiting in stable groups with reproductive females are virtually limited to mammals (Wilson 1975, Brown 1975), and most empirical reports of these structures remain descriptive (e.g., Garber and Kowalewski 2013) rather than theoretical or empirical, including, experimental. A paucity of studies is available to describe degrees of relatedness, intrasexual competition, or tendencies for these males to exhibit mate “choice”. Additionally, systematic research on the stability of “fission-fusion” dynamics, frequently characterizing multimale-multifemale and “nested” reproductive groups, has not been conducted. In both multimale-multifemale (Packer and Pusey 1982, Jones 1980, 1985) and “nested” societies (Wiszniewski et al. 2012a), males demonstrate coalitions and alliances, but mammalian males rarely, if ever, demonstrate altruism, achievable only via a subsocial route of evolution involving vertical transmission of reproductive benefits (Chapters 1 and 2).

Recent reports on polygynandrous lions (Mosser and Packer 2009) and hierarchically-organized bottleneck dolphins (Wiszniewski et al. 2012b) suggested that defense of reproductive females may explain benefits to related (via subsocial route) or unrelated (via semisocial route) males from collaboration and/or cooperation. The latter reports indicated, as well, that (presumably, up to some optimal limit) larger group sizes are associated with greater reproductive benefits to males from kinship or from shared interests other than kinship (“shared fates”). Discussing eusocial bathyergids, Lewis and Pusey (1997) reported that higher infant mortality was associated with larger groups, a trend that, if common among mammals, would oppose Allee effects whereby female reproductive success increases with an increase in group size. Compared to sociality among females, the scientific literature on sociality among mammalian males is limited, a topic in need of systematic study, particularly, variations in tactics and strategies for the management of competition attendant to reproductive conflicts of interest, as well as differential behaviors and network characteristics of related and unrelated reproductive males.

In multimale-multifemale groups, accurate discrimination of mates is a component of their survival and fitness, but discrimination often involves a tradeoff between efficiency and flexibility. The tactics and strategies employed by females have received relatively little systematic study by social biologists, particularly in regard to conflicts of reproductive interest among potential mates. In some patches, females will benefit most from maximizing the genetic heterogeneity of a litter of their lifetime reproductive output, conditions favoring disassortative mating (mating with the most divergent genotypes). Similar to the effects of polyandry, disassortative mating by females may also reduce the intensity of sexual selection on males by decreasing competition for mates by unrelated males in a group.

The latter scenario may give rise to sociality via a parasocial route, a condition likely to maintain benefits from dispersal for mammalian males, generating conditions within groups characterized by high asymmetries between chronic states of genetic asymmetries. In these conditions, sequential female “decisions” (“female choice”) effectively manage conflicts of interest among males. In mammals, because of high levels of intrasexual selection attendant to female philopatry, this condition may drive the evolution of sociality among females as a mechanism to manage male-male competition, and it is well-documented that females in many multimale-multifemale mammalian groups, express an array of social behaviors, particularly, grooming, allomothering, and adoption. The aforementioned and related topics deserve systematic study by social biologists because Hamilton’s rule subsumes the resolution of interindividual conflicts of interest. Thus, mechanisms to coordinate and control competition within and between groups may reflect tradeoffs between reproductive conflict and cooperation.

A Note on Male----->Female Aggression in Mammals (~2012) (Clara B. Jones)

A Note on Male → Female Aggression in Mammals (~2012)

1 Male → Female Aggression (MFA) in mammals: stereotypy and flexibility

Female-male relations are generally analyzed from the perspective of sexual selection theory. In brief, competition among males will be intense where females are spatiotemporally clumped since male reproductive success is limited by the number of mates monopolized (per unit time), while female reproductive success is limited by the amount of energy extractible from the environment convertible into offspring. Where food and females are distributed unevenly, some males will control many more females than others, as found among most large mammals. Sexual selection modifies the communication system of any species and acts on males and females differently. Male mammals, ceteris paribus, dominate females in the same conditions because: (1) competition is more intense among males compared to females; (2) group-living males are generally unrelated; and, (3) in the same conditions, males can increase their reproductive output more than females are able to. For these and other reasons, reproductive optima between the sexes are generally asymmetrical.

Energy-savings drives the selection of traits, a thermal regulatory process maintaining usable heat within limits propitious to optimal functioning. Because females are, theoretically, “energy-maximizers”, signaling may represent a significant (relative) fitness cost that, in the same conditions, males, “time-minimizers” in theory, may be in a better position to afford. Energy-saving strategies are, also, indicated for female mammals due to their high “reproductive load” and vulnerability to the effects of offspring competition. Mammalian males can significantly influence population parameters by controlling reproductive careers of females. Such influence can be enhanced by ecological factors (clumped, limiting resources), by tactical and strategic decision-making (male herding behavior, infanticide, “sneaking”), or by females, themselves (passive “female choice”, facilitating male intromission.

On the other hand, traits and “decisions” associated with female mammals have the potential to mitigate male attempts to monopolize them (female-female tolerance and facilitation, female choice of breeding sites, female infanticide, sexually-dimorphic division of labor, female dispersal). Where females utilize an “energy-maximizing” strategy, selection will favor efficient detection, acquisition, consumption, and allocation of resources, a profile opposing the evolution of developmentally costly, ritualized signals and displays, possibly countering the evolution of phenotypic plasticity, a developmental strategy entailing costly neural circuitry designed for rapid and accurate execution in heterogeneous regimes.

Energy-maximization is expected to favor time-intense, “non-damaging” (indirect: grooming, appeasement postures, cryptic responses) and relatively low-cost (vocalizations, grooming, avoidance, withdrawal) competitive tactics and strategies with the potential to stress male time budgets. The tactics and strategies of female mammals, then, may be bounded by a fundamental “tradeoff” where efficiency opposes flexibility, possibly putting this polymorphism at a disadvantage in heterogeneous, unpredictable, or extreme regimes. How might this apparently deterministic tradeoff be mitigated by ecological and evolutionary effects so that female mammals are “emancipated” from the consequences of males’ responses, where such emancipation would be beneficial to lifetime reproductive success of females?

2 The eco-ethology of male → female aggression (MFA)

Among mammals, some environments have a high potential for male → female aggression, reducing pressures on the differential fitness optima of each sex (“sexual conflict”). Female mammals may be vulnerable to male coercion and force, coordination and control, because high maternal investment predisposes them to phenotypes designed for efficient execution of maternal roles (estrogen, mammaries, mate selectivity). Though the ethological perspective holds that ritualized signals and displays function to decrease likelihoods of aggression among conspecifics, both opportunistic or “voluntary” (learned) as well as ritualized (stereotyped) characteristics may significantly stress reproductive females’energy-reserves.

It has been suggested that male and female mammals engage in an ongoing evolutionary “arms race” to impose greater (reproductive) costs on each other or to “hold one’s own” in such a competitive “chase”. Males appear to have more influence in some taxa (Agouti; Northern elephant seals: Mirounga angustirostius; walrus: Odobenus rosmarus; Hamadryas baboons: Papio hamadryas; chimpanzees: Pan troglodytes; lions: Panthera leo; domestic cats: Felis catus). In other taxa, females have, apparently, more influence (Hawaiian monk seal: Monachus schauinslandi, lemurs: Lemuridae; bonobo: Pan paniscus; mantled howler monkey: Alouatta palliata; coati: Nasua narica; African elephant: Loxodonta africana; reindeer: Rangifer tarandus), including, species in which females are dominant to males. In a few species, intersexual relations have been characterized as “egalitarian” (striped mice: Rhabdomys pumilio, fox: Lycaon; muriquis:Brachyteles arachnoids), while, in others, intersexual influence and “power” generally vary by context (squirrel monkeys: Saimiri spp.; most socially “monogamous” mammals involving single male-single female co-residence; humans: Homo sapiens). P.C. Lee (personal communication) suggested that the previous patterns may be influenced by alternative reproductive strategies employed by males, reported for grey seals (Halichoerus grypus).

According to Estes (1992), aggression, including coerced or forced copulation (“rape”: orangutans: Pongo; Northern elephant seals), by males → reproductive females, is likely to be favored by selection in two conditions. First, females of polygynous mammalian species (red deer: Cervus elaphus, hartebeest: Alcelaphus caama) don’t copulate outside their receptive periods. Polygynous human systems represent one exception to this pattern. My review of (carnivorous) pinnipeds, as well as other mammal groups, strongly suggests that high levels of male → female aggression is associated with non-ritualized behavioral repertoires (ground squirrel: Citellus armatus, humans), high population density, breeding on land (pinnipeds), a “catholic” (broad niche or opportunistic) diet (pinnipeds, humans), male dominance hierarchies (rather than resource- or female-defense: lions, chimpanzees), limited periods of male or female fertility (lions, walrus: Odobenus rosmarus), high infant mortality (polygynandrous lions; Northern elephant seals; but, see, mastiff bats: Tadarida brasiliensis), multiple-mating by females (chimpanzees), and very lengthy periods of female pregnancy, lactation, or maternal care (chimpanzees, humans). Thus, a suite of ecological, including, social, factors facilitates male trajectories, and it is unclear to what extent reproductive males or females embody opportunities to override these conditions, topics in need of investigation.

For example, a few cases documented by Estes (1992) complicate a search for socioecological correlates. In some conditions, “promiscuous” females are not monopolized by males (atelids; bonobos), decreasing effectiveness of male → female aggression and lowering the strength of sexual selection as well as “sexual conflict”. In a few taxa (Agouti; humans), apparent monogamy is associated with high levels of male agonism during courtship. Furthermore, Estes (1992) concluded that male → female aggression is relatively common where females remain in their natal groups (most mammals), but not among patrilocal taxa (apes), and in some conditions, female dispersal may have been an adaptive counterstrategy to male coercion and force (atelids?, humans?).

Among primates, for example, female dispersal is associated with energetically costly, more evenly dispersed, plant material, particularly, mature leaves, while matrilocal societies, and, male → female aggression, are associated with nutritionally-poor, clumped, ephemeral, fruit resources (but, see, chimpanzees and spider monkeys: Ateles). The previous ecological scenarios, and, others, are expected to impose energetic costs on both sexes, and relative costs and benefits to males and females require systematic analysis. When the differential factors (climate, soil gradients, ecological, phylogenetic, stochastic) are understood more completely, apparent inconsistencies, paradoxes, or outliers (chimpanzees, spider monkeys, humans) may resolve. Following from my review, male → female aggression may sometimes benefit female reproductive success (reducing offspring mortality, increasing female fitness) by providing information to females. Information-acquisition may occur in “extreme” environments (deserts, shoals), may be associated with rare conditions (catastrophic events), or may be associated with benefits in other regimes (danger, risk, difficulty). On the other hand, sexual segregation may provide greater benefits to females in the previous conditions (most mammals). In defense of the latter speculation, four of the five mammalian taxa characterized by recurrent and severe, including, lethal, male → female aggression are group-living (domestic cats, lions, Hamadryas baboons, chimpanzees, humans).

Estes (1992) documented low occurrences of male → female aggression where females are dominant to males (ring-tailed lemurs: Lemur catta, bonobos) and where females exert strong “choice” of mates (“leks”, most multimale-multifemale societies). On the other hand, Manson (1994) argued that sexual preferences by mammalian females may incur significant aggressive costs from non-preferred males (Hamadryas baboons, Northern elephant seals). Wilson and Daly (1978), as well as Brooks & Jennions (1999), summarized differential costs, benefits, and tradeoffs from the perspective of both sexes. Mammalian males in several genera coerce females with some frequency (Hanichoerus, Papio, humans), suggesting that phylogeny, in addition to ecology, needs to be considered as a correlate of male → female aggression (pinnipeds). Studying mantled howler monkeys, Jones & Cortés-Ortiz (1998) reported that male → female aggression was unlikely to be expressed where some threshold unpredictability of clumped, ephemeral resources rendered females too costly for males to monopolize. In such extreme regimes, females become “moving targets”, increasing costs in time to the aggressor (see bats). It is clear that, for energetic and, probably, other reasons (disruption of information, induced ovulation: hedgehogs: Erinaceinae), coercion and force of females are not always to a male’s advantage.

For example, dominance hierarchies may arise from a compromise between intraspecific competition (“social competition”) for resources and for mates sensitive to asymmetries in “resource-holding potential” and asymmetries in fitness optima among conspecifics. Differential patterns of rank may be viewed as systems of signals communicating differential tendencies among individuals to attack or retreat, reflecting relative reproductive costs and benefits of aggressive or appeasement behavior as a function of interindividual distance. The rare mammalian society mentioned previously, female dominance to males (Clutton-Brock 1977), insures low likelihoods of MFA, allowing tests of some hypotheses related to the ability of females to escape male coercion and force. The previous system has been identified, in particular, with multimale-multifemale organization, among other population structures: indri, Indri indri; ring-tailed lemur, Lemur catta; Verreaux’s sifaka, Propithecus verreauxi; pygmy marmoset, Cebuella pygmaea; talapoin, Cercopithecus talapoin; vervet, Chlorocebus (formerly, Cercopithecus) aethiops (P.C. Lee, personal communication); and, blue monkey, Cercopithecus mitis. Similarities between the last two species suggest that adaptations to heterogeneous conditions may favor the evolution of “female dominance” since they are the only members of the genus distributed in its extreme northern and southern ranges.

The previous overview of conditions in which mammalian females are most and least vulnerable to male coercion and force demonstrates that life histories of females of this Class are not necessarily coordinated and controlled by male behavior and spatial dispersion. Mammalian females’ tactical and strategic counterstrategies to reproductive conflicts between the sexes may be favored by selection, such as the “bared-teeth mouth display” expressed by mantled howler females, effectively inhibiting male aggression. Nonetheless, it is not clear to what degree female opportunities are determined by socioecology, genetic, and, other constraints (e.g., copulatory plugs: moles, Talpidae), and available evidence strongly suggests that life history trajectories of mammalian females are significantly impacted by consequences of males’ “decisions”, circumstances expected to favor female tactics and strategies that mitigate their “rugged landscapes”, where the“adaptive zone” permits.

3 A simple model of male → female aggression in mammals

Male → female aggression may be modeled as male parasitism of the opposite sex whereby a male exploits a female for reproductive or social advantage (“social parasitism”). Quantitative modeling puts these responses in perspective. Consider a male aggressor, the Sender, exploiting the time-energy budget of a reproductive female (a Receiver). Following May and Anderson (1990, in Moore 2002), Moore pointed out that fitness of a parasite (here, an adult male aggressor) can be measured as reproductive rate (R_o), a density-dependent value. May and Anderson’s equation formalizes virulence (rate of deleterious effects of male → female) by way of a measure of cost to a female’s fitness (increased intensity of intra- and inter-sexual interactions). May & Anderson’s equation can be modified for male parasitism of females such that

R_o= y (N) / (a + b + v),

where y is transmission rate (e.g.,“virulence”, in the present case, reproductive and social costs imposed upon females by males), N is population density of reproductive females, a is rate of cost to reproductive females, b is rate of cost to reproductive females from all but virulence (opportunity costs), and v is a model’s recovery rate (a female’s ability to completely or partially escape) from deleterious effects of an aggressor male’s responses (e.g., by increasing future reproductive rate or switching to behaviors decreasing likelihoods of male aggression).

The above scenario may lead to coevolved states between aggressive males and their female targets or to effective mechanisms of female defense where females are able to discriminate aggressive from non-aggressive males, and May & Anderson’s formula might be employed to predict conditions under which benefits to males from aggression decrease (e.g., where virulence, transmission, and recovery rate are independent: Moore 2002; atelids?, bonobos?).

The topics discussed in the present note and elsewhere, as well as related questions and propositions, wait systematic quantitative modeling and tests, in combination with naturalistic description and controlled studies under laboratory and field conditions (e.g., surgical manipulation of genitalia; regulatory mechanisms).

4 Conclusions, perspectives and directions: the eco-ethology of male → female aggression

The previous discussion of adult male → female aggression (MFA) highlights tactics, strategies, and mechanisms whereby an initial Signaler (Actor) has the potential to influence the expression and evolution of traits in a Recipient. Each interaction may affect statistical parameters of social competition between members of the pair, third parties in a group or population (“indirect effects”), including, mutualists and predators. MFA may be regarded as a time-minimizing, uni- or multi-modal (visual, tactile, auditory, olfactory) strategy that, in some lineages, occurs as a ritualized display, a transition expected to reduce costs from aggression for adult males and adult females. For example,“solitary” (sexually-segregated) male ground squirrels (Citellus armatus) and “solitary” male palm squirrels (Funambulus pennant), with slightly ritualized behavioral repertoires, are notably aggressive toward females during courtship, while,“solitary” male grey squirrels (Sciurus carolinensis), displaying somewhat greater phenotypic ritualization, are less aggressive during courtship than the two previous species. Aggression is, effectively, absent in the“solitary” European red squirrel (Sciurus vulgaris) with highly stereotyped courtship signals and displays. Of import, compared with its relatives, European red squirrels inhabit spatiotemporally- and thermally-stressful, deciduous habitats, highlighting the need for ecological and evolutionary studies, including, experiments, of ritualized signals and displays in sexually-segregated and social mammals.

Acknowledgments

I am grateful to Phyllis C. Lee for helpful feedback that significantly improved this note.

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