MAMMAL SOCIAL EVOLUTION: MAJOR TRANSITIONS APPROACH--PROPOSED SCHEMA AND NOTES (order hard copy at lulu.com)

MAMMAL SOCIAL EVOLUTION: MAJOR TRANSITIONS APPROACH—PROPOSED SCHEMA AND NOTES

 

Cite [APA style]: Jones, C.B. (October, 2022). Mammal Social Evolution: Major Transitions Approach—Proposed Schema and Notes. Science Blog [vertebratesocialbehavior.blogspot.com]; lulu.com.

 

Clara B. Jones

Silver Spring, MD 20910, USA

Cell: 828-279-4429

Email: foucault03@gmail.com; mapcbj@gmail.com

 

“The major transitions approach provides a conceptual framework that facilitates comparison across pivotal moments in the history of life. It suggests that the same problem arises at each transition: How are the potentially selfish interests of individuals overcome to form mutually dependent cooperative groups? We can then ask whether there are any similarities across transitions in the answers to this problem. Consequently, rather than looking for different explanations for the succession of different taxonomic groups, we could potentially identify a few key factors that have been important again and again at driving increases in organismal complexity. This approach would both unify and simplify our understanding of the evolution of life on Earth.” West et al. (2015)

“[Each] activity performed by an individual can be thought of as incurring a certain probability of death and a certain probability of successful reproduction.” McCleery (1978)

“The key to the sociobiology of mammals is milk.” Wilson (1975)

 

 

TABLE OF CONTENTS

Abstract

Key Words

Foreword

Preface

Introduction

Terminology

Interindividual Interactions and Hamilton’s Rule

SCHEMA: Proposed Transitions to Complex Sociality in Mammals [Pre-social; Sub-social; Social (Cooperation); Complex Social]

Notes [Major Transitions; Cooperation; Division-of-Labor; Humans]

Conclusion

Acknowledgments

References

 Figure 1. Female naked mole-rat (Heterocephalus glaber) Breeder with Helpers and offspring [cf. Bennett & Faulkes (2000) for introduction to African mole-rats, Bathyergidae]. Naked mole-rats are classified, “eusocial,” and are the only species of mammal known to exhibit morphological specialization [dispersal morph, breeder morph?], constituting a “caste” system, comparable to the social insects.  Overlap of generations, cooperative breeding, and reproductive division-of-labor [differentiation into specialized Breeder – Helper tasks, roles, and/or morphology] characterize eusocial taxa, and the three species of social mole-rats meet these criteria [H. glaber; Fukomys damarensis, the Damaraland mole-rat; Cryptomys hottentatus hottentatus, the common mole-rat]. Questions regarding classification of social mole-rats and cooperatively-breeding mammals are in some dispute. Some researchers have attempted to demote social mole-rats to the status of Cooperative Breeders. Furthermore, it is not uncommon for researchers to designate species with communally-breeding females who may demonstrate “helping,” as Cooperative Breeders [e.g., jackals, warthogs]. However, though social mole-rats may not prove to be the only Eusocial mammals [e.g., see, Cape porcupines], necessary conditions for Complex Social classification are “reproductive division-of-labor” and a group structure including, in addition to “Helpers,” only one or a few female Breeders [“Queen(s);” more or less “pure” Breeder[s)]. See text herein for further treatments. ©Chris Faulkes

 

MAMMAL SOCIAL EVOLUTION: MAJOR TRANSITIONS APPROACH—PROPOSED SCHEMA AND NOTES  

 

ABSTRACT

With this document, I attempt to persuade mammalian Social Biologists to adopt the Major Transitions Approach to Social Evolution as the standard model. Herein, I define the latter approach, clarify terminology and definitions, discuss a standardized way to address Interindividual Interactions, and incorporate Hamilton’s Rule as the general law or principle for the discipline. I propose a Schema for classifying mammalian social evolution, highlighting mammalian traits expected to benefit or disadvantage female mammals’ “fitness” [lifetime reproductive success] via mechanisms to reduce maternal costs. Throughout, I highlight the role[s] that abiotic and biotic factors play as regimes with the potential for transitioning from one “grade” to another, and it is paramount to keep in mind that sociality is not an ideal end in itself. Female mammals may reduce maternal costs via a number of pathways, including, remaining solitary breeders. Gregariousness or sociality are not necessary or sufficient to benefit female “fitness.” There are many “routes” to “fitness” that may create barriers to, disadvantage, or benefit living in groups. In some environmental regimes, for example, and for some maternal conditions, selection may favor energy-saving reduction of nursing bouts or shorter periods of offspring development creating opportunities that might be used for the acquisition of food convertible to present and future reproductive demands. Throughout the text, arrows designate comments and notes addressing pertinent questions, concerns, as well as, topics for future investigation.

 

KEY WORDS: mammal social evolution; major transitions approach; interindividual interactions; Hamilton’s Rule; Social Paleontology; Therapsids; solitary breeding; bauplan; group-living; aggregations; Pre-social; Sub-social; Interdependence; Cooperation; Complex Sociality; reproductive division-of-labor; totipotency; specialization; Primitive Eusociality; social mole-rats; humans

 

FOREWORD

Herein, I propose Transitions in Mammals from Solitary [independent] breeding to Pre-social to Sub-Social to Social (Cooperation) and to Complex Social [Division-of Labor (Cooperation between Specialists); Primitive Eusocial (in Mammals, no sterile “castes,” but, “totipotency;” Eusociality requires at least two overlapping generations, Cooperative Breeding, Reproductive Division-of-Labor (Breeder-Helper): Wilson (1971); Task, Role, and/or Morphological Specialization [morphological specialization in mammals, apparently, only found in naked mole-rats, Heterocephalus glaber, Fig. 1 (disperser morph; breeding female morph)]. Currently, among Mammals, only the social mole-rats [African mole-rats: Bathyergidae] are classified, Primitively Eusocial [see Bennett & Faulkes (2000) for scientific names, classification, and other details; also, see Faulkes & Bennett (2009)]. Primitively Eusocial mole-rats are “totipotent” [capable of both Breeding, in addition to, “Helping”]. Primitively Eusocial mole-rats lack “sterile castes” characterizing some social insects. Social insects with more or less “sterile castes” are classified, Advanced Eusocial. Transitions are not inevitable.

--à Energy and Matter came from the Big Bang billions and billions of years ago, and we just keep recycling [moving, transitioning] them around. It is useful to view sociality through this lens. A transition favored by selection in given abiotic [e.g., climate, nutrients] and biotic [e.g., nutrient sources, interindividual contexts] regimes are expected to create an energy-savings that can be used for acquisition, consumption, and allocation of limiting resources to reproduction, enhancing, maternal “fitness.” For reference to “work,” see Schmid-Hempel (1990), and think in terms of the 1^st Principles of Physics and 1^st Principles of Ecology [acquisition; consumption; allocation].

--à Complex: consisting of many different connecting parts, such as, individuals [organisms (see, “major transitions approach:” Maynard Smith & Szathmáry 1995] interacting in a group or population.

--à Complexity: see announcement and descriptions of 2021 Nobel Prize in Physics—complexity emerges from simple rules [algorithms]; also, see Lex Fridman Podcast #234 with Stephen Wolfram via YouTube.

--à Essential Background Reading and Videos:

West et al. [(2015) provides a conceptual overview of the major transitions approach applied to social evolution; also, see Bourke 2011; Cooper & West 2018; JF Eisenberg 1981. Refer to EO Wilson's chapters on non-human mammals and humans in 1975 Sociobiology; Cooper & West 2018; Toth et al. 2007. DeJong 1976 [allocation of energy by females], as well as, Schmid-Hempel 1990 [“work”= Force x  displacement (W= Fs)] are useful. Dugatkin (1998) is an outdated discussion of Cooperation; however, his chapters on mammals provide interesting case studies of behaviors that may classify as “cooperation.” Downing et al. (2020), using a major transitions approach, is a good place to begin for comparisons with cooperatively-breeding birds. For an introductory but comprehensive theoretical treatment of “inclusive fitness,” see, Marshall (2015).

Additionally, I strongly recommend, as introductions to social insect eusociality and for comparative purposes, as well as, terminology, Wilson (1971) and Hölldobler & Wilson (1990). The latter book, Ants, all of which are eusocial, demonstrates the wide variability of group architectures classified as, “eusocial.” Hölldobler & Wilson (2009) treats the distinction, “Breeder,” “Helper,” as the first “grade” of “caste.” Based on studies with social insects, Robinson (1992) suggests that inter-individual behavioral variation [phenotypic variation] may be considered a type of “specialization” and “caste.” Note that, in mammals, & other vertebrates, Breeders exhibit some helping, and Helpers are “totipotent” [capable of both breeding and helping] due to which observation Keller & Perrin (1995) recommended employing a “continuum” approach (cf. Sherman et al. 1995)]. In some mammals, Helpers may breed “opportunistically” [e.g., meerkats], though, often [usually?], mammal Helpers do not breed when “helping.” You will find a wealth of references in my 2014 Springer Brief [e.g., see therein, Table 3.1 on prehistoric mammals] and in my 2020 and 2021 lulu.com monographs [Jones (2020) is attached to the Profile of my Twitter feed, @cbjones1943]. All of these sources highlight the variability of social complexity, as well as, flexibility and/or plasticity of many traits [cf. Gene Robinson 1992; cf. Libbrecht FINE video-lecture (see below)].

Four FINE Seminar Series video-lectures on social insects are highly recommended: C. Penick; R. Libbrecht; R. Gadaghar; K. Kapheim that are available on YouTube or on the FINE website—also, see FINE Twitter feed. Penick makes some comparisons to Mammals. Though, one does not expect perfect correspondence[s] when one takes a comparative approach [whether within and between Genera, Families, or Orders of a Class or between Classes], broad patterns and, even, some analogies [e.g., dominance hierarchies: see Jones 2020; Penick, as well as, Gadagkar FINE videos] may be discovered, especially, for different species in the same environmental regime[s].

Since 1980, I have found the Social Insect literature particularly useful and edifying for assessing comparative social evolution employing a major transitions approach. For example, Christine Nalepa (2010) found that altricial cockroaches gave rise to eusocial termites. The altricial state is primitive in mammals (as per Eisenberg 1981). Students of mammal social evolution must keep in mind that the precocial state may give rise to group-living taxa, also—a topic requiring systematic investigation. For researchers seeking bird or insect models [lab or field] with mammalian traits, polygynandrous acorn woodpeckers, [some] termites and/or [some] wasps are recommended. For many potential models for mammalian social evolution [e.g., Cape porcupines; jackals; hystricognaths], see Macdonald (2009, 2001

 

PREFACE

 

Mammalian Paleontology: As of this writing, Class Mammalia comprises >6,000 species and ~29 Orders. Mammals evolved in the Late Triassic ~210 mbp from Therapsids [Cynodont Clade, sometimes called, "mammal-like reptiles” (they are not dinosaurs)].  Lactation, endothermy [thermoregulation], hair [e.g., thermoregulation], some other mammalian diagnostic traits [e.g., typical jaw, teeth, skin], evolved in Therapsids, and their potential association with the evolution of sociality in the Class requires systematic investigation [see “What is a Mammal?” in Macdonald (2001)]. Eisenberg (1981) advanced the view that marsupials remain mammals’ sole “control group,” and, because both Classes are endothermic, social evolution in birds and mammals should be compared and contrasted.

Therapsids were extant throughout the Permian and the Triassic, and humans are both Cynodonts and Therapsids. The huge initial investments mammalian females make in producing offspring, particularly, lactation, might predispose them to give and/or receive “help” or, on the other hand, not to give or receive “help,” depending upon whether a transition from solitary to gregarious living yields a greater share of lifetime reproductive benefits. These alternate paths to “fitness,” relative to phylogeny, maternal condition, and environmental regime, need directed study. The “litany” is that most mammals are “sexually segregated” [“solitary”]; however, [sexual] selection is expected to act on males and females differentially. For example, in a number of mammalian taxa, such as bats and rodents, males are “solitary,” females, communal [or, “social?”—see below], with varying degrees of Interdependence [below].

--à In addition to the litanies that most mammals are “sexually segregated” [“solitary,” “dispersed”] and polygynous, physical traits—in particular, exterior phenotypes—are said to be generalized, presumably, in response to evolution in extremely heterogeneous regimes (see Eisenberg 1981). The prior conclusions are consistent with the idea that in highly variable environments where patterns of limiting resource availability cannot be detected and tracked, as well as, where any patterns that may exist [e.g., seasonal availability of food] occur in periods greater than a population’s “generation time,” generalized traits will be the optimal and most energetically efficient strategy (see Levins 1968). These topics require systematic investigation to assess their accuracy and their relevance to mammalian social biology.

--à I propose a new sub-discipline of Paleontology to be called, Sociopaleontology or Social Paleontology and/or Comparative Sociopaleontology or Comparative Social Paleontology. Much work needs to be systematically undertaken on mammalian Social Paleontology; however, a fair amount of evidence is available on climate and potential food availability during the Triassic. Unless I am mistaken, the earliest mammals were likely to have been omnivores, herbivores, or insectivores, and the current hypothesis about why they survived the major extinction event is that these small creatures had very “fast” life-histories (cf. Funston et al. 2022; see Stearns & Koella 1986). Mammalian Social Paleontology has been conducted at least since 1902; for recent publications, see Ladeveze, et al. (2011); Jaswoski & Abdala (2017); Weaver et al. (2021). 

 

INTRODUCTION

“Major Transitions” refers to biological transitions from simple to complex, as from single cells to multicellular organization to organism to superorganism (Maynard Smith & Szathmáry 1995). Transitions are not inevitable.  Transitions to mammalian Interdependence or Social “grades”  (“grade” after Wilson 1971), if they occur, embody females breeding alone to females breeding in a group—with or without a breeding male—and polygyny is generally accepted to be the most common population structure in mammals (see, Hex, Tombak, & Rubenstein 2021; Wittenberger 1980)  Often adult males’ territories embrace the locales of more than one group of female breeder[s]. In other words, “polygyny” does not necessarily imply that an adult male cohabits with a breeding female or a group of female breeders [i.e., a “harem”]. Population structure will be a function of abiotic and biotic environmental regimes, including, the dispersion of limiting resources (Crook 1964), including, mates, breeding sites, and food availability.

Transitions embody increasing degrees of interindividual interdependence as we transition from Sub-social to Complex Social “grades, should these condition-, situation-, context- [and, density-?] dependent transitions occur [e.g., groups without Cooperation among group-members may be favored by selection in given selective regimes (see below)]. Transitions in mammalian sociality from Sub-social to Complex Social, also, embody Breeder[s] becoming increasingly dependent upon other group members. If complex sociality evolves, breeding females depend upon “Helpers”—a process associated with reduction of maternal costs and increasing de-coupling between Survival and Fecundity (“trade-off:” Stearns 1989) for the breeding female[s]. Recall that no transition is inevitable. If, when, and under what abiotic [e.g., climate, nutrients] and biotic [including, interindividual context] conditions transitions evolve will, necessarily, depend upon relative gains in "fitness" [“lifetime reproductive success”] of individuals transitioning from one "grade" to another [e.g., from a female breeding in a solitary state to a female breeding in a group, a bauplan in vertebrates].

--à In order for the study of Major Transitions to Social Evolution to be a scientific endeavor, it is necessary for the enterprise to be grounded in 1^st Principles of Physics and in the 1^st Principles of Ecology: acquisition, consumption, & allocation [i.e., allocation of Energy into Survival and, essentially, Reproduction (life-history strategies: Stearns 1992)]. Transitions from one “grade” to another are not inevitable but depend upon the abiotic and biotic [including, interindividual] patterning of environmental regimes. An environmental, Evolutionary Behavioral Ecology approach entails use of John Hurrell Crook’s (1964) schema whereby patterns of individual and interindividual responses, as well as, the architecture of group structures, are functions of dispersion [distribution and abundance] of limiting resources [e.g., food, mates, breeding sites] across Time and Space. With the assistance of quantitative methods, including, models, simulations, and experiments, a major transitions approach simplifies the Behavioral Ecologist's and Evolutionary Biologist's search for patterns and principles [“laws”] within and between Genera, Families, Orders, and Classes. Recall that transitions are not inevitable and depend upon propitious abiotic [e.g., climate, nutrients] and biotic [e.g., limiting food resources; interindividual interactions] regimes favoring the most efficient condition-, context-, situation- [and density-?] dependent mutations arising in a given population. 

 Terminology: Herein, “Group” is defined as a Reproductive Unit. Thus, I dispense with the Social Scientists' dichotomy between “social system” and “mating system” because, in gregarious animals, breeding takes place within a group. West-Eberhard, in her classic 1979 paper, suggested that “social” and “reproductive” can be thought of interchangeably. 

Further, I propose that we employ the term, “group-living” rather than “social organization” or “social group” unless, or until, Cooperation [reproductive benefits accrue to both Actor and Recipient (+, +), as per Hamilton 1964] arises in a given mammalian population—thus, for example, “group-living” breeders, not “social” breeders. 

Additionally, if or until Cooperation (“Social,” as per Hamilton 1964; see below) arises among individuals in a group-living mammal population, I propose that we employ the term, “gregarious” rather than refer to all interindividual interactions as “social.” “Gregarious” is the term employed in ornithology for group-living birds.

--à Thinking, in particular, of the Complex Social “grade” in the Schema presented below, only females are discussed as “Breeders” because: females produce large and few gametes [eggs] relative to males producing small and copious gametes [sperm], an observation denoted “Bateman’s Rule” (Trivers 1972); thus, females, make a larger initial investment in reproduction compared to males (Trivers 1972 [for optimal female metabolic strategy, see Schoener (1971)] and, in the context of the present work, may be more predisposed to receive “help” where it is beneficial to “fitness;” population-level life table parameters are a function of female traits because population growth depends upon female productivity; and, females are the limiting resource determining male reproductive success [“fitness”]. As noted above, the very high metabolic and other costs of lactation may, in some regimes, predispose female mammals to reduce maternal costs via gains from group-living [e.g., predator defense, more efficient foraging: cf. Alexander 1974].

 

INTERINDIVIDUAL INTERACTIONS AND HAMILTON’S RULE: Behaviors are outputs, also, traits, of an individual—not only action or motor patterns, but, also, cortical, olfactory, auditory, etc., outputs of an individual in response to stimuli. Neurobiological responses are sometimes classified as “behaviors;” however, these are not directly exposed to the abiotic or biotic environments, thus, cannot be acted on directly by selection. Brain structures and mechanisms may be favored by selection via selection on phenotypic traits that are genetically-correlated and associated with a given brain structure, module, or mechanism—relative to environmental regime. I hypothesize that the brain is rule-governed via some inherent Hamiltonian algorithm, probably, a straightforward property or mechanism influencing all brain and behavioral operations.

Hamilton's Rule [rb – c >0 ---> rb > c] is a general principle [law, formulation] where r= coefficient of relatedness; b= benefits to Recipient of an act facilitating reproduction; c= reproductive costs to Actor. An Actor’s “inclusive fitness” is comprised of reproductive benefits accrued from assisting the reproduction of offspring—“direct fitness,” and reproductive benefits accrued from assisting the reproduction of non-offspring relatives—“indirect fitness.” Hamilton’s rule expresses when, and when not, to favor kin. It is a common error in the Animal Behavior literature to assume that Hamilton's Rule directs an individual to always favor kin. It does not. Under conditions of intense local competition, for example, “kin may be ego's worst enemy,” whereby it would be deleterious to Actor’s “fitness” to favor the reproductive interests of a relative. Critical references: for drivers of Social Evolution, see Schmid-Hempel (1990); for general Social Evolution, see Bourke (2011); for recent theoretical treatment of “inclusive fitness theory,” see Marshall (2015); for Major Transitions Approach applied to social evolution (cf. West et al. 2015; Cooper & West 2018; Toth et al 2007). Eisenberg (1981) is a necessary introduction to general mammalian patterns, including, group structures and gregarious behaviors. Some of the older work (e.g., Wilson 1975, Eisenberg 1981) tends to be characterized by group-level thinking.

Herein, Hamilton's Rule (Hamilton 1964) is followed whereby use of the term, “social,” is limited to Cooperation [Actor gains reproductively; Recipient gains reproductively: +, +] or Altruism [Actor bears reproductive Costs; Recipient gains reproductively: –, +]. Thus, interactions whereby the Recipient gains reproductively are considered, “social.” Altruism is, generally, reserved with reference to social insects exhibiting Advanced Eusociality (more or less sterile "castes;" see below); although, most social scientists would claim that humans exhibit Altruism. Specialists still debate how, under what conditions, and whether Altruism [as well as, Spite: -, -] can evolve. Currently, many researchers hypothesize that Altruism [and Spite] can evolve if the long-term reproductive benefits outweigh the short-term reproductive costs. In practice, especially, in the field, it may be difficult to differentiate between Selfish and Cooperative interactions, emphasizing the need for researchers to investigate interindividual asymmetries and to specify operational definitions and/or assays for each behavioral category (cf. Lehmann & Keller 2006). Reciprocity (Trivers 1971) and other mechanisms [e.g., “group” selection, “byproduct” effects] that have been put forward to explain and account for the evolution of Cooperation and Altruism are assumed, herein, to be a function, instead, of Hamilton’s Rule. As stated above, I take Hamilton’s Rule as a general principle of social evolution; though, consistent with Information Theory, any series of interactions will exhibit some degree of “noise” and “error.”

--à Importantly, Hamilton’s Rule emphasizes the fundamental property of individual-level selection because each partner, Actor and Recipient, are affected differentially [reproductive Benefits in the case of a Recipient, reproductive Costs in the Actor’s case]. Selection acts differentially upon each individual—Actor and Recipient—not on the interaction itself [sometimes termed a “bond,” especially, in the Primatology literature].

--à In 2011, Bourke stated, “No level of ecological benefit can bring about altruism if relatedness is not above zero.” Although this author is speaking of Hamiltonian “altruism” [-, +] in this quote, it raises the question of whether or not there is some, situation-dependent, threshold that must be met before Actor assists the reproduction of a Recipient. Clearly, actors interact with other group-members, and some of these interindividual interactions appear to be collaborative [e.g., coalitions, grooming, “allomothering” (see “Interdependence” below)]. In the Animal Behavior literature, such interindividual interactions are usually termed, “Cooperation.” But, are they?

This question confronts mammalian social biologists at every turn; and, as alluded to above, it may be very difficult to distinguish between selfish [+, -] and cooperative [+, +] interactions in practice. Unless actors are subject to error [to a degree deleterious to their own “fitness”]; unless Actor is pathological; unless, Actor is the victim of self-deception, or unless Recipient is perpetrating deception to which Actor is susceptible (see Trivers 2014, Otte 1975); or, unless, in point of fact, Actors simply do not assist the reproduction of non-relatives, we need to address when and under what conditions Actor will Cooperate with an unrelated Recipient. A satisfying answer to this apparent conundrum is provided by West et al. (2002) who suggest that Actor [or, Actor’s algorithm] takes into consideration [not necessarily in a conscious or aware manner] the reproductive effects of her/his actions, not only on Recipient, but, also, on all of those affected by Actor’s action. Thus, for example, it may benefit Actor to assist the reproduction of an unrelated Recipient if the act’s effects reduce competition for his/her kin in the group or population. Related to the aforementioned, it is useful to recall Maynard Smith & Szathmary’s (1995) caveat: “The evolution of sociality does not depend only on relatedness: there must be something useful that individuals can do for one another.”

--à Conceptualizing Social Evolution requires that interindividual interactions may be positive [+], negative [-], or neutral [0] relative to future reproductive success [“fitness”] and that, except for clones [in mammals, monozygotes (“identical twins”)], each individual's interests differ; in other words, each individual of an interacting dyad has different, condition-/situation-/context- [density-?] dependent “fitness optima.” Ubiquitous “genetic conflict[s]” and other asymmetries between individuals [e.g., body size; age; sex; rank; matriline] determine an entity's “fitness optima”—relative to other individuals, as well as, environmental regime.

--à Recall that, consistent with Hamilton’s (1964) general treatments, “Social”= Cooperation or Altruism [the latter, seemingly rare or absent in mammals, including, humans: see West et al., 2015]. Thus, interindividual interactions are not “social” unless they have been demonstrated to be Cooperative [+, +]. Interactions deemed to be “Social,” necessarily presume an interindividual interaction in which the Recipient gains reproductively [+]. Interpreting and quantifying all non-agonistic interindividual interactions as “social” interactions, is a ubiquitous error employed in the fields of Animal Behavior and in the Social Sciences.

 

 

SCHEMA: PROPOSED TRANSITIONS TO COMPLEX SOCIALITY IN MAMMALS [Pre-social ---> Sub-social → Social (Cooperation) → Complex Social]

 

Logic: Female Mammals bear a costly, initial investment in reproduction, primarily due to lactation. Mechanisms and processes favoring reduction of maternal costs may benefit mammal females in some environmental regimes. Sociality is not the only route to “fitness” whereby female mammals can reduce maternal costs. For example, selection may favor females who “park” their young or who reduce the number of nursing bouts or who rest more, presumably, freeing mothers to forage for nutrients convertible to present and/or future maternal effort. “Mixed” cost-reducing strategies may, of course, be selected. In all cases, transitions from one mode of breeding to another will be a function of “fitness” benefits to females, as well as, intensity of selection pressures under changing abiotic and biotic conditions. Transitions are not inevitable. Whenever one notes a female trait, the observer should ask whether the trait has the potential to or might be a pre-adaptation for reduction of maternal costs. The present schema pertains to mammalian populations and species in which transitions to social evolution may occur—may have the potential to benefit female “fitness.” It is important to note that most mammals are “sexually-segregated,” though breeding females may form groups of interacting individuals, with or without Interdependence, a necessary precursor for the evolution of Cooperation, the first “grade” of sociality (cf. West et al. 2015, 2021; see below). Even where sociality is beneficial to female mammals, the researcher must recall that there are, always, “tradeoffs” in Survival and Fecundity. In a classic paper, Alexander (1974) discussed the costs, as well as the benefits of sociality. Because specialized traits are uncommon in Mammals compared to other Vertebrate Classes, and because specialization is one feature of Complex Sociality, the Primitively Eusocial naked mole-rats [H. glaber], exhibiting morphological specialization like the Social Insects, stand out as the pinnacle of social evolution in mammals.

 

Pre-social “grade” 1: Therapsid breeding independently [“solitary” breeding] with maternal care (see Toth et al. 2007).  Mothers provide all “work” associated with offspring care before emancipation. Mother and offspring contact [e.g., “huddling” for thermoregulation] may be a precursor to retention of some young in unit; the very high energetic costs of lactation and nursing may set the stage for selection to favor mechanisms to reduce maternal costs [e.g., precocial young] and may have, but not necessarily, preadapted mammal breeders to conditions favoring group-living and the benefits that may accrue that can be allocated to Survival and Fecundity [e.g., increased offspring survival or quality; increased predator protection; secure breeding sites; increased access to food or reduced foraging costs]. Because of the high energetic costs of lactation, female mammals might seem to be preadapted for social life; however, solitary breeding may be the most adaptive mode (see Eisenberg 1981).

--à Mammalian females would seem to be pre-adapted for gregariousness and sociality because of the high initial costs associated with gestation and, particularly, lactation and nursing. But, keep in mind that relative costs and benefits to maternal lifetime reproductive success [“fitness”] depend upon numerous factors pertaining to abiotic and biotic environmental regimes, dispersion [distribution and abundance in time and space] of limiting resources [including, mates, breeding sites, food, etc.], as well as, local conditions [e.g., competition and density-dependence]. Alexander (1974), in particular, reminded us of the tradeoffs associated with social evolution.

--à Interindividual interactions, including, mother-offspring interactions, are not deemed, “social” or “cooperative” unless Hamilton’s criterion is met [+, +; also see, Trivers 1972]. In this sense, mothers suffer reproductive costs from maternal care and mother-offspring genetic conflict, explaining Trivers’ (1972) proposition that mothers terminate maternal investment at some threshold level of investment at which offspring have some minimum likelihood of survival until reproduction at which “point” mothers redirect their allocation to preparing for future reproductive events. In mammals, and other vertebrates, females may resume breeding before a prior offspring or litter has reached emancipation.

--à Actors, should be unwilling to cooperate with prospective unrelated Recipients unless reproductive Benefits would accrue to Actor by way of kin [in the group or population] affected by the Recipient (West et al. 2002).

--à As per Eisenberg (1981), the altricial state is “primitive” [ancestral] in mammals. The roles of lactation (cf. Pond 1977) and of altricial young [e.g., in mammals: marsupials; most rodents; cats; dogs; primates, including, humans] and other ancestral mammalian traits, for the evolution of Interdependence and Cooperation [sociality] requires systematic investigation [e.g., fur (e.g., thermoregulation), endothermy (e.g., thermoregulation)]. That gregariousness has been described in species with precocial young [e.g., most ungulates], demonstrates that the precocial state may be a route to sociality.

 

Pre-social “grade” 2: Aggregations: Incipient group-formation that may transition to group-maintenance (see Bourke 2011). Aggregations are unstable and impermanent in Time and Space. Aggregations [clusters of conspecifics—as distinguished from, “guilds”] may form around clumped, limiting resources [e.g., as typically “solitary” deer in Spring may cluster around clumped food]. It seems an open question whether or not Aggregations [or, opportunistic encounters] are a. necessary precursor to group-maintenance and group-living (see Jones 2014, Table 3.1). Based on the prehistoric evidence that I am aware of, aggregations appear early in mammalian evolution which some researchers have interpreted as evidence of "gregarious" or "social" groups. Weaver et al. (2021) suggest that sociality is a "labile" trait in mammals. While “aggregations” are not “groups” in the sense that they are not reproductive units [see above], opportunities for mating, including, multiple mating, would, likely, present themselves.

 

Sub-social “grade” 1: As in Pre-social “grade” 1 except, females transition from breeding independently [“solitary breeding”] to breeding in a group—without Interdependence [below] (for critical references pertaining to this transition, see Crook 1964 and Emlen 1982). In vertebrates, a transition from independent [“solitary”] breeding to breeding in a group is a universal transition [a “bauplan”] if group-living and breeding in groups evolves at all. Whether or not females can skip this grade, going directly—evolutionarily—from, say, Pre-social “grade” 1 to Sub-social “grade” 2 [Interdependence] is not clear to me. Systematic comparative research is needed. Hystricognaths would be good candidate study models.

--à In Sub-social “grade” 1, interindividual interactions within groups are, I suggest, undifferentiated but interactions are expected to be non-random because of asymmetries between individuals (e.g., by genotype; age; sex; body size). Asymmetries result in Actor and Recipient having different “fitness optima,” with “genetic conflict” being a necessary driver. As pointed out above, interindividual interactions may be positive [+], negative [-], or neutral [0] with respect to Benefits or Costs to either or both interacting individuals' future, inclusive, reproductive success [“fitness”], including, mother → young interactions, adult → adult interactions, mother → offspring or non-offspring interactions, as well as, offspring → offspring interactions with kin or non-kin. 

--à Thus, I suggest that, +, + interactions will be some sub-set of all interactions, but, interactions, whether +, +; +, -; -, -; or, 0, 0 [+, -, or 0 with respect to reproductive benefits or costs], will not be stable or structured in Time or Space [i.e., interindividual interactions have not yet differentiated or become structured or iterated via selection]. As noted above, transitions, if they occur, depend upon their being favored in given, abiotic and biotic, environmental regimes and depend upon energy-savings afforded to females representing gains in “fitness.” I propose that, relative to abiotic and biotic conditions, selection may, for example, favor cooperative [+, +] interindividual interactions, disfavor, selfish [+, -], altruistic [-, +], or spiteful [-, -], or some combination of the possible interactions. In some regimes, one of the other possibilities, or some combination of their genes may be favored so that genes besides cooperative ones may be retained in the population, functioning, possibly, according to density- and/or frequency-dependent processes.

 

Sub-social “grade” 2 [Interdependence]: As in Sub-social “grade” 1, except interindividual interactions are differentiated [structured: e.g., evolution of grooming or “allomaternal” care (see Hrdy 2011, Hawkes 2004)]. If a transition to this grade is favored, it is, like other transitions, expected to reduce maternal costs. Interdependent interactions are common in group-living mammal populations. Interdependence is recognized to be a necessary precursor to the evolution of Cooperation [sociality], which is, itself, the "gateway” to the evolution of Complex Sociality in Mammals and other taxa (cf. West et al. 2021; also, see Cooper & West 2018).  The FINE lecture by L. Ebensberger reporting his results for South American Degus [related, as hystricognaths, to African mole rats], seems to suggest that the transition from solitary breeding to breeding in a group may be driven by assistance given to mothers by other females in female-female but not female-male units. The paper by West et al. (2021) highlights that the potential for and/or transition to Cooperation in mammals evolves from monogamy or groups of female relatives (see, importantly, Wittenberger 1980).

--à Rather than view differentiated interdependent interactions between an Actor and a Recipient as necessarily positive for the “fitness” of each member of the dyad [i.e., Hamiltonian +, + interactions], it may be more accurate to hold that differentiated, interdependent interactions may have some combination of positive, negative, or neutral consequences for an Actor’s and a Recipient’s “fitness.” In some environmental regimes, it is posited, +, + interactions will be favored by selection, yielding a stable state in a group or population—relative to environmental regime. I would speculate that genes with negative or neutral outcomes relative to the “fitness” of individuals in differentiated, interdependent interactions would be maintained with some frequency in the given population since environments, including, interindividual contexts, are expected to vary and change, implying that frequency-dependent mechanisms, in addition to density-dependent ones, would be operating.

 

 

 

Figure 2. A moving unit of Hadza hunter-gatherers in Tanzania, part of a larger “band.” Mothers and their offspring are accompanied by other related and unrelated group-members who might serve as “allomothers” [caregivers, including, siblings, other than the mother]. “Allomothering” or “alloparenting” may take many forms, such as, “babysitting,” “grandmothering,” play, or transport. A complicating factor in Homo sapiens is that caregivers may be paid for their services, an economic transaction that may have different causes and consequences than “allomothering” in non-human animals. ©Brian Wood

 

 

Social “grade” [Cooperation: +, + interactions]

 --à In some environmental regimes, Hamiltonian sociality [Cooperation: +, +] may be favored if beneficial to breeders’ reproduction [if energy-savings can be converted to offspring]. Recall that transitions are not inevitable. Interdependence is a necessary precursor to the evolution of Cooperation (West et al. 2015). Cooperation is the “gateway” to Complex Sociality [below]. My tentative speculation for the evolutionary transition from Interdependence to Social [Cooperation] is that, during Sub-social “grade” 2, Interdependence, selection acts on +, + interindividual interactions with greater selection intensity in some environmental regimes [e.g., following models in Behavioral Ecology, a change in climate might effect greater variability in rainfall leading to clumping or greater ephemerality of limiting resources favoring group-formation and consequent interindividual interactions, possibly, followed by group maintenance, possibly followed by interindividual Interdependence, possibly, transitioning to Cooperation where conditions and selection favor +,  + interactions].

These mutually-beneficial [+, +] interactions [“relationships”] may become more frequent [more structured; more predictable] in certain environmental conditions [“environmental potential” for Cooperation] compared to selfish or neutral interactions which may be favored in other [abiotic and/or biotic] regimes. This "rugged" fitness incline must have been difficult to climb or not advantageous to female mammals since there seems to be a consensus that most members of the Class are “sexually segregated” (“solitary”). However, in some regimes inhabited by mammals, communal or cooperative interactions, particularly among females, have proven to be a stable and more energetically efficient strategy than solitary breeding or non-cooperative interactions The question of how common Cooperation [+, +] may be among mammal species, including, humans, is unclear [see below]. Cooperative interactions and genotypes may coexist with non-cooperative interactions and genotypes in the same group or population.

--à If transitions to Cooperation [+, +] occur, it must be because selection has favored a mutation correlated with a trait or traits [e.g., via pleiotropy] leading to this “grade,” increasing efficiency, driven by energy-savings [“Selection always increases efficiency.” DeJong 1976; for optimal female metabolic strategy, see Schoener 1971]. The present treatment assumes that a population must include C(ooperation)C, CS(elfish), and SS genotypes.

--à In this grade, resulting from interindividual asymmetries, some females find it advantageous to concentrate upon breeding, some, on “helping.”  In mammals, Breeders may “help,” and “Helpers” retain the capacity to breed [“totipotent” condition]. Where this differentiation arises, females may be pre-adapted for Complex Sociality—Reproductive Division-of-Labor and Specialization. Such interindividual asymmetries, then, may set the stage for Cooperation between Specialists [Division-of-Labor between more or less exclusive Breeders and more or less exclusive “Helpers” in the present case]. While this phenomenon of incipient differentiation needs systematic investigation, one can detect these features in “allomothering;” “grand-mothering;” and dominance hierarchies whereby different individuals appear to be taking on different roles.

 

Complex Social “grade:” In some environmental regimes [“clumped,” limiting food sources; intense local competition?; “poor” habitats?; moderate to high environmental heterogeneity, such as, ephemeral food?; seasonal environments?], sociality as per Cooperation [among members of a group or population] may transition to Complex Sociality, if, like other transitions, this transition occurs at all relative to environmental conditions and selection on phenotypic variability (see West & Cooper 2016): Specialization---->Reproductive Division-of-Labor [Cooperation among specialists—more or less exclusive Breeders, more or less exclusive “Helpers”], which may lead, in Mammals, to Primitive Eusociality [task, role, and/or morphological (naked mole-rats) Specialization]. Advanced Eusociality, more or less sterile “castes,” is absent in Mammals. According to Macdonald (2001), some naked mole-rat “helpers” never have an opportunity to breed throughout their lifetimes.

--à Received wisdom is that mammals are characterized by generalized traits (cf. Eisenberg 1981), a condition that should have placed significant limits on mammals’ potential for “specialization,” and, Complex Sociality, to evolve. In light of the foregoing, naked mole-rats must be viewed as a remarkable, possibly, unique, example of Eusociality in the Class, having evolved morphological specialization.

--à Again, in mammals, the transitions, should they occur, entail transitions from Solitary Breeding by Females --à Females breeding in a group without Interdependence --à Females breeding in a group with Interdependence --à Females breeding in a group with Cooperation --à Complex Sociality [Reproductive Division-of-Labor; Specialization]. In mammals, reproductive division-of-labor is found among Cooperative Breeders, as well as, the social mole-rats [see below].

Naked mole-rats [H. glaber] exhibit size “polyethism,” “temporal” division of labor [age “polyethism”], reproductive division-of-labor, as well as, morphological specialization [disperser morph; female breeder morph]. Damaraland mole-rats [F. damarensis] exhibit “temporal” division-of-labor, as well as, reproductive division-of-labor [for temporal division-of-labor in primates, see Jones 2020 and Hrdy & Hrdy 1976]. Social mole-rats [Bathyergidae] are, currently, the only mammals classified, “eusocial” [for “cooperatively-breeding” mammals, see below], and naked mole-rats are the only mammals recognized to exhibit morphological “castes.” As pointed out previously, Breeding and Helping roles and tasks in mammals are not obligatory in that Breeders usually do some work and Helpers may breed in various proportions, lending support to the view that Breeding and Helping may be conceptualized along a continuum (cf. Keller & Perrin 1995; for an earlier treatment on the continuum concept, see ,Sherman et al. 1995). Robinson (1992) suggested that interindividual variability [resulting from differential intraindividual "personality" or "behavioral syndromes"] may be viewed as primitive “castes,” and Hölldobler & Wilson (2009) pointed out that the initial differentiation into Breede -Helper roles represents an early “caste” stage.

--à In humans and some other mammals exhibiting post-reproductively sterile females (see Cant et al. 2009), more or less, sterile “castes” [for a discussion of post-reproductive sterility in humans, see Foster & Ratnieks 2005] have not been classified, “eusocial,” because unambiguous, specialized, and stable reproductive division-of-labor [Breeder and Helper roles and tasks] have not been identified—even if the species meet all other criteria for eusocial status [overlap of generations and cooperative breeding (for humans, see Crespi 2014)]. On the other hand, if Breeding and Helping are considered as occurring along a continuum from, proportionately, less to more as per Keller & Perrin (1995), this diagnostic trait classification may need revision. Nonetheless, currently, cooperative breeders and social mole-rats are the only mammalian taxa known to exhibit reproductive division-of-labor, and, as a consequence, the only mammalian taxa exhibiting “complex" social traits, as per a major transitions approach.

On related matters, Jones (2014) suggested that cooperatively-breeding mammals might be considered, eusocial, with the social mole-rats, based on the criteria that both exhibit reproductive division-of-labor, combined with, overlap of generations, as well as, cooperative breeding. On the other hand, Clutton-Brock (2021, 2016) and his colleagues, apparently, classify social mole-rats, cooperative breeders, though, Markus Zöttl has informed me that the two social systems are considered synonymous by some social biologists. Following the aforementioned treatments, Crespi (2014) concluded that, while humans exhibit a number of “insectan” traits, the species does not meet the criterion for exhibiting reproductive division-of-labor (see sections on humans in Jones 2020, 2021; also, see Foster & Ratnieks 2005).  

 

 Superorganism “grade:” This “grade,” characterized by social insect nests and mounds, may be absent in mammals. Unless I am mistaken, some Anthropologists, students of “gene-culture co-evolution,” for example, claim that “complex” human societies [e.g., organizations; nation-states] are “superorganisms,” presuming that group-level selection is operating (for treatments of the topic of “superorganism,” see Holldobler & Wilson 2009; for “superorganismality,” see Boomsma & Gawne 2018).

 

 

NOTES

Major Transitions:

--à Evolutionary social theorists studying mammals must model “Solitary,” Pre-social, Sub-social, Social [Cooperation], and Complex Social “grades,” relying upon Hamilton's (1964) formulations (see Marshall 2015 for an introductory mathematical treatment). Also, it will be important for behavioral ecologists to quantify the relative proportion of Selfish and Cooperative genotypes and phenotypes in given populations of group-living mammalian [and, other group-living vertebrate] taxa as well as, the abiotic [e.g., climate, nutrients] and biotic [including, interindividual] regimes associated with group-living populations and species. The possible “rule-governed” [lawful] nature of [demographic] ratios should be evaluated (cf. Oster & Wilson 1978), as well. Furthermore, genomic studies can assess the degree of monomorphism or polymorphism for Selfish vs. Cooperative phenotypes, as well as, what traits correlate with those genotypes [see work of Gene E. Robinson's lab ("socio-genomics:" Robinson, Grozinger, & Whitfield 2005)]. These studies will, also, identify genomic “toolkits” and convergences (cf. Woodard et al. 2011). 

--à A major component of a scientist's job is to simplify; to build models and algorithms; to unpack variation; as well as, to conduct laboratory and/or field experiments. The Major Transitions Approach to Social Evolution provides a straightforward way to proceed from independent [“solitary”] breeding with maternal care to Complex Sociality; from Primitive [ancestral] to Derived; and, for group-living taxa, from less to greater dependence of Breeders relying upon Helpers, including, the process of uncoupling Survival and Fecundity during a breeder’s life-history trajectory across transitions, should they be favored. In the Social [Cooperation] and Complex Social [reproductive division-of-labor; specialization] “grades,” females are not expected to breed successfully or not able to maximize “fitness optima” without assistance from conspecifics, usually, offspring and other female relatives. Transitions driven by the Costs [to reproduction] of maternal care, may lead, in some regimes, to the evolution of a range of mechanisms to reduce those Costs [see Fig. 2]. The FINE videos recommended above help us to conceptualize what variables might play a part in some females becoming more or less obligate [“pure”] Breeders, some females becoming, more or less obligate “Helpers.” In mammals and birds [CB Jones, unpublished], species exhibiting reproductive division-of-labor [a type of morphological specialization or “caste,” as per Hölldobler & Wilson 2009], all Breeders and Helpers are more or less non-obligate—in various proportions.

--à We have the necessary data to test and to revise the proposed schema of Mammalian Social Evolution using a Major Transitions Approach. Indeed, treatments of mammalian sociality advanced by Wilson (1975), as well as, Eisenberg (1981), hint at "major transitions” thinking, a method not unrelated to comparative phylogenetic studies. There are many existing descriptive and natural history data sets, in addition to, museum work, as well as, lab and field research, whose data sets permit testing of assumptions, conduct of experiments, and development and application of models and simulations to address my proposed schema and other topics herein. Experiments can be conducted with simulations. As a first approximation, the present treatment yields numerous questions that lend themselves to scientific methodologies.

--à In his 2019 book, Genesis, EO Wilson proposed a set of six transitions that differ from the series employed by West et al. (2015) and, herein. Thus, "The centerpiece of Genesis is a listing and discussion of the six so-called ‘great transitions of evolution’…. These stages are: (1) the origin of life; (2) the invention of complex (“eukaryotic”) cells; (3) the invention of sexual reproduction, leading to a controlled system of DNA exchange and the multiplication of species; (4) the origin of organisms composed of multiple cells; (5) the origin of societies; and, finally, (6) the origin of language." (L.D. Wilson, amazon.com review of Genesis). The inclusion of language as the pinnacle of social complexity is consistent with a Social Sciences, Scala Naturae Approach, to evolutionary transitions. It is important to point out that, by 2019, Wilson had become a dedicated group selectionist, though, according to Robert L. Trivers, [personal communication] this tendency is present in Wilson’s whole oeuvre.

 

Cooperation:

--à How common is Cooperation [Hamilton’s Social “grade”] in Mammals? We need systematic research on this topic, including, the development of assays, in order to differentiate Interdependence from Cooperation. There are many candidate traits to consider in the literature [e.g., see Wilson’s 1975 and Dugatkin’s 1997 chapters on mammals and humans. Also, Eisenberg (1981) should be consulted. The anthropologist, LH Morgan’s discussion of human social traits may be useful, as well as, economist, Adam Smith’s writings]. The “litany” and “received wisdom” are that most mammals are “sexually-segregated” or “solitary.”

I suspect that systematic work will show that Hamiltonian Cooperation [+, +] is less common among group-living mammals than Hamiltonian Selfish interactions, though, “alliances” would seem to be a possible candidate for Cooperation [see below]. My chance observations of the seemingly infrequent dyadic displacements of a third group member by adult male or adult female dyads of the polygynandrous mantled howler monkey (A. p. palliata), suggested that these events were opportunistic in nature (see, Jones 1980). Rather than Cooperation, coalitions and alliances may be types of Interdependence, such as, coordination, collaboration, or facilitation, deserving systematic investigation.

Whatever the case may be, it might be expected that there are various types and degrees of Interdependence that might function as precursors to the evolution of Hamiltonian sociality [Cooperation]. Of course, like all action and motor patterns, as well as, behaviors, responses are expected to be situation-dependent, and their classification may be expected to vary depending upon varying abiotic and biotic environmental regimes.

--à It will be necessary for students of Social Biology to determine whether coordination and/or collaboration that is imposed by a third-party or his/her representatives or that is imposed by one Actor in the case of division-of labor, [imposed via persuasion, coercion, force, or manipulation (e.g., exploitation)], so common in humans, should be termed "Cooperation” and considered, “Social.” Probably not. To date, it appears that little, or no, systematic investigation has been made of this issue which, at once pertains fundamentally to terminological, as well as, social biological questions. Related to this question for the human case, should non-human mammals in which collaboration is imposed by the Breeder’s olfactory emissions be considered, “Cooperation?”

--à Transitions from Selfish [+, -] to Cooperative [+, +] relationships, then, may be only apparent. Interacting individuals may collaborate for one purpose or in one way that appear to be cooperative without being so.

--à Regarding the aforementioned, and related, conundrums, an economy based on money exchange may be a mechanism for enforcing Cooperation, increasing the likelihood that recipients will cooperate, and/or decreasing the likelihood that recipients will “cheat” [be “free-riders”]. Adam Smith (2003) stated, “It’s not from the benevolence of the butcher, the brewer, or the baker that we expect our dinner, but their regard to their own self-interest.” Smith’s idea may indicate that, before an economic medium of exchange beyond barter emerged, the value of resources exchanged might have led to a greater degree of inequality and conflict than in a barter economy, highlighting the difficulty of evolving Hamiltonian Cooperation [+, +]. Of course, an economy based upon monetary transactions would not be expected to completely eliminate coercion, force, exploitation, or “subterfuge.” A related quote by Crook (1971) is, also, pertinent: “Social behaviour is a subterfuge.”

 

Division-of-Labor:

--à Division-of-labor is defined as “cooperation between specialists” (Cooper & West 2018). There is a large literature on “generalization” and “specialization,” and their evolution, in the Ecology literature. Division-of-labor necessarily implies “complexity,” in the sense that a whole task or other outcome is “broken down” into component parts for which different individuals are responsible. In the social insect literature, the “fitness” advantages to reproductive division-of-labor have been speculated or shown to be: increased survival rates; increased reproduction rates; increased “productivity;” more efficient developmental timing; and/or more efficient co-ordination among breeders and “workers.” Research on social insects has, also, shown that the benefits of reproductive division-of-labor scale positively with group size [mean group size in naked mole-rats is comparatively large: Bennett & Faulkes 2000].

I assume that specialization must evolve before or concurrent with Cooperation, possibly, during an advanced stage of Interdependence—precursor to the evolution of Cooperation [+, +], “gateway” to the evolution of Complex Sociality [reproductive division-of-labor; specialization]. There seems to be a consensus among mammalogists that bodily phenotypes are usually generalized, though, body plan does not seem to predict, say, a generalized diet [see, for example, many rodent species], and behavioral flexibility, as well as, phenotypic plasticity, may compensate for or enhance a generalized morphology. Environmental regime, in particular, moderate to extreme heterogeneity [variability], relative to generation time, may favor generalized body plans (see Jones 2009).

--à “Helping” may be age-dependent [“temporal division-of-labor” (“age polyethism”)]. Among Primates, adult female, as well as, adult male mantled howler monkeys [A. p. palliata] exhibit “age polyethism” (Jones 1996, 2020), and, in the Asian Hanuman langurs, females are characterized by “age polyethism.”

--à Do humans exhibit Complex Sociality? According to the Major Transitions Approach, the criterion for the first stage of Complex Sociality—subsequent to the evolution of Cooperation, should Cooperation evolve within groups—is reproductive division-of-labor and, after Crespi (2014), the general consensus is that humans do not exhibit reproductive division-of-labor; thus, by inference, humans have not evolved, Complex Sociality, though, in future, application of the continuum approach to the evolution of eusociality proposed by Keller & Perrin (1995) may revise this conclusion.

--à Division-of-labor is conceptualized in the Social Sciences [e.g., Adam Smith: Economics; Lewis H. Morgan: Anthropology] to be highly advantageous, indeed, necessary, to the appearance of “complex” [multi-component, multi-level, modular] groups, including, organizations and nation-states. In particular, Adam Smith’s (2003, 1776) many ideas and verbal formulations about division-of-labor in humans can often be extrapolated to general discussions about social evolution. In the same book, Smith suggested, for example, that division-of-labor reduces average costs of output, increases quality of output, facilitates large-scale production, and “reduces scarcity—the latter, in terms of Population Ecology, possibly, meaning that division-of-labor reduces competition among members of a group or population for limiting resources, freeing up availability. Smith, as well, advanced the seemingly obvious idea that division-of-labor facilitates teamwork and Cooperation [n.b., coalitions and alliances]. This economist, known as, “the father of Economics” also, believed that division-of-labor was linked to a higher standard of living and quality of life, possibly, relevant for all female mammals.

--à In an interesting and useful paper, Smith & Riehl (2022) recently reviewed and assessed empirical studies of and additional evidence for "division-of-labor," emphasizing animal taxa other than social insects. These authors rely upon common usage in the Animal Behavior and Social Sciences literature whereby all non-agonistic interindividual interactions are termed, "social." As highlighted in a major transitions approach, however, population structure may transition from one "grade" to another, say, from "solitary" breeding to breeding in a group, if, and only if, it benefits the reproduction of individuals in a population to do so, presumably, in response to changing environmental regimes and energy-savings sufficient to allocate to reproduction, moving closer to an individual's "fitness optimum." Indeed, Smith & Riehl barely give a nod to the ecological factors—causes, as well as, consequences—favoring social evolution and its contingent transitions.

Furthermore, transitions to group-living may, under propitious conditions, occur without the evolution of Cooperation, in particular, as pointed out by West et al. (2015), it must be demonstrated that Interdependence has evolved as a precursor to Cooperation. The point is that transitions are not inevitable, and group-living does not necessarily imply that Cooperation characterizes interindividual interactions in groups. In mammals, for example, breeding females may cohabit without cooperating—in the Hamiltonian sense as treated herein [+, +].  

Finally, the "grade," Complex Sociality, entails the evolution of "reproductive division-of-labor" and task, role, and/or morphological specialization. By concentrating almost exclusively on "task" specialization, these authors overlook the concept that the fundamental "division"/specialization entails a division between Breeder and Helper [in social insects, "worker"], not specialization by task per se.

--à Four FINE Seminar Series video-lectures [Social Insects: C. Penick; R. Libbrecht; R. Gadaghar; K. Kapheim: available on YouTube or on the FINE website], suggest that there are other ways, besides, Cooperation, that may be precursors to reproductive division-of-labor [e.g., asymmetries in dietary profiles or physiology; dominance rank relations], as well as, the researchers providing insights on what factors might lead some females to become “pure” breeders, some females, workers [in mammals, totipotent “helpers”—the differentiation being the first appearance of “caste,” according to Hölldobler & Wilson (2009)]. If differential dominance rank is shown to be a precursor to Cooperation in mammals as one possible feature of the Interdependence “grade,” then, we might conclude that density-dependent contest competition may factor in to the evolution of Cooperation. It seems to me that differential dominance rank may be viewed as a type of rudimentary “caste” system, though systematic study is required to evaluate the utility of this idea.

--à In my 2020 monograph on [herbivorous] mantled howler monkey [A. p. palliata] female life-history using a major transitions approach, a negatively age-graded dominance hierarchy [younger individuals dominant to older individuals] combined with differential access to limiting nutrient [food] resources [diet], in particular, ephemeral food sources, instantiated “temporal division-of-labor” [“age polyethism”], though, it is not clear to me how to treat “temporal division-of-labor” in my schema proposed above. Neotropical howler monkeys [Alouatta], do not exhibit reproductive division-of-labor. This topic, as well as, the possibility that other mammals utilizing limiting, ephemeral, food resources [e.g.,the Neotropical primates in the Family, Atelidae] or who are folivores [e.g., langurs among the Old World Primates (see Hrdy & Hrdy 1976 for “temporal division-of-labor” in langurs)], deserve systematic investigation. To my knowledge, social mole rats exhibit “temporal division-of-labor,” and age as a main effect should be systematically investigated in all group-living mammals.

--> It is important to keep in mind that "division-of-labor" is defined as "cooperation between specialists;" thus, a major impediment to the evolution of Complex Sociality in mammals, including, humans, is that, for the most part, mammalian phenotypes are generalized, as pointed out by Eisenberg (1981), making the cooperatively-breeding mammals and the social mole-rats, especially, H. glaber, all the more remarkable.

  

Humans:

--à When considering human evolution, it is, always, important to keep in mind “behavioral flexibility,” “phenotypic plasticity,” and, variation writ large, in addition to, noise and error in the sense of complexity and Information Theory.

--à Geographically, humans and social insects are the most widely distributed terrestrial taxa, a concordance that, alone, justifies comparing and contrasting mammals and social insects using a major transitions approach. For example, both taxa are heralded for their notable behavioral flexibility and phenotypic plasticity. As top predators, humans dominate food chains; thus, they have less energy to extract from available food resources compared to animals at other trophic levels. This condition should lead to intense intraspecific, as well as, interspecific, competition for limiting resources that might, in some regimes, favor group-living, Interdependence, and, possibly, Cooperation. Intraspecific competition needs to be considered as a likely context for the evolution of mammalian sociality, including, density-dependent competition, frequency-dependent competition, and the spectrum of possible causes and consequences of intense intraspecific competition—pressures that are likely to have favored traits with the potential to minimize the deleterious effects of competition for conspecifics’ “fitness” [e.g., the evolution of dominance hierarchies; mechanisms to partition resources; dispersal patterns; behavioral flexibility and phenotypic plasticity]. Mortality may, also, be a significant effect of intraspecific competition influencing life-history strategies (see Stearns & Koella 1986).

Humans’ unusual life-history strategy combining a relatively long developmental period with a relatively “fast” reproductive rate (see Stearns 1992 for “fast” and “slow” life-histories) may, also, be related to competition for limiting resources, as might be, the evolution of noteworthy behavioral flexibility and phenotypic plasticity, the latter traits being ones that Macdonald (2001) considers characteristic of the Class. In addition, Stearns & Koella (1986) highlight the importance of studying mortality rates whenever life-history is investigated. All human, and other mammalian species’, traits should be viewed in the light of intraspecific competition and mortality, particularly, as they may relate to evolutionary transitions to sociality, keeping in mind that transitions depend upon the differential reproductive costs and benefits to individuals in given environmental regimes and are not inevitable.

--à According to Bernie Crespi (2014; also, see Jones 2020, 2021), humans do not exhibit reproductive division-of-labor. Some have claimed that the presence of post-reproductive “sterility” in human females strongly suggests eusociality (Foster & Ratnieks 2005). I argue in my 2020 and 2021 monographs that any gregarious groups that post-reproductive females may be part of are not necessarily characterized by a Breeder-Helper class/”caste” structure, nor are post-reproductive females in this species obligated to perform “helping” roles or tasks at all. The wide variety of composition of human reproductive units requires systematic investigation and “unpacking.” A human “ethogram” would be of great assistance. Though the potential combinations and recombinations of motor and action patterns exposed to the environment, particularly, other individuals, would be impossible to measure and classify, the motor and action patterns, themselves, should not be numerically exhaustive to describe because of fundamental constraints within and between human populations imposed by similar anatomical structures. When attempting to unpack human “complexity,” perhaps cultural evolutionary anthropologists should begin with the null hypothesis, Humans are not “complex.”—contrary to the opposite assumption automatically assumed in the Social Sciences. West et al. (2021) point out the importance of employing “null” models.

--à Related to the topic of human social evolution, broadly speaking, quite a few authors have concluded that most human interactions are Selfish [Actor benefits reproductively; Recipient, bears reproductive costs (as per Hamilton 1964: +, -)]. These papers can be found in the earlier Social Psychology and Learning Theory [Behaviorism] literature. Recently, two empirical papers by Burton-Chellew (e.g., Burton-Chellew & West 2013, Burton-Chellew & West 2021) reported that humans demonstrate primarily “selfish” tendencies. Suggestively, West et al. (2021) advance the opinion that Altruism will be found to be rare [or, absent?] in humans.

--à Kirschner & Gerhart’s (1998) treatment of “Evolvability” provides support for the following ideas. First, that the extreme behavioral flexibility and phenotypic plasticity exhibited by humans, functions to enhance or maximize Evolvability [potential for evolution], on whole. Extreme behavioral flexibility and phenotypic plasticity, also, may function as, “tinkering,” and Kirschner & Gerhart discuss the “exploratory” functions of evolvability in the context of their core discussion about functions that are, at once, flexible and robust. There is a large literature on “exploratory behavior” in the Psychology literature which may provide some useful ideas regarding evolvability in humans and other mammal taxa. Investigation of mammal species with a broad array of “stereotyped” signals and displays [e.g., Neotropical howler monkeys, Atelidae, Alouatta; Old World cercopithecines], should, also, be studied, since they provide examples of “plastic” [irreversible] traits that can be combined and recombined. Notably, human phenotypes are virtually devoid of ritualized signals and displays, with at least one exception being the “eyebrow flash” (Eibl-Eibesfeldt 1989).

Second, extreme behavioral flexibility and phenotypic plasticity may function to conceal the intent of Actor and/or to confuse Recipient when it is in the [reproductive] interest of Actor to do so [“Social behaviour is a subterfuge.”, op cit.]. This idea tentatively suggests that Actor may “control”—not necessarily in a conscious or aware manner—the expression of some of the components of his/her phenotypic arrays, genetically-correlated or not. Related to the aforementioned, Information Theory emphasizes costs to complexity—“noise” and “error.” These topics require systematic investigation.

--à When thinking about the extant Great Apes, including, humans, as Gene Robinson's “sociogenomic” (Robinson,Grozinger, & Whitfield 2005) work with social insects shows, every taxon has its own “toolkit,” though convergences are often identified, even, among distantly-related taxa, including, across Classes [see Robinson's landmark paper on convergent evolution at the genomic level, Woodard et al. (2011), which includes data for mammals]. Berens et al. (2015) demonstrated that, in fact, across taxa, genes may differ—it is the pathways that are often be conserved.

--à Like all non-human apes, chimpanzee [Pan troglodytes] females breed in a group but breed independently [little or no “allomothering,” “babysitting,” or other contact or “help” by kin or non-kin of either sex]. This phenomenon [that has been noted in the Animal Behavior literature] compared to the impressive variety of interdependent traits in humans, deserves systematic investigation. This contrast between humans and other apes may relate, evolutionarily, to other diagnostic human features [e.g., gestures and language; maximum group sizes; extreme reliance upon reward mechanisms (e.g., associative learning; Herrnstein's "matching;" observational learning); mimicry; "fast" reproductive rate combined with slow development; potential to completely decouple Survival & Fecundity (only modern Humans, given the advent of technology, can completely decouple Survival and Fecundity after egg production and harvesting), emancipating human females to allocate energy to other activities besides breeding and caretaking—should they “choose;” extreme "phenotypic plasticity," as well as, behavioral variability/flexibility—primitive traits in animals (Nijhout 2003); intense sensitivity to and awareness of contextual stimuli (sensation and perception); mechanisms of punishment (see Clutton-Brock & Harvey 1995) and other types of “enforcement;” “social learning” and culture; "complex" societies, as per, combination and re-combination of differentiated interindividual responses; learned, rather than inherently predisposed, task and role division-of-labor; broad geographical success of Homo sapiens]. Not all of these features depend upon higher-order and/or conscious and aware, cognitive processes, including, individual recognition.

--> Human social evolution probably requires significant revision. Though there seems to be general agreement that humans do not exhibit "reproductive division-of-labor," the remarkable behavioral flexibility and phenotypic plasticity of human responses permits a wide range of conformations, including, division-of-labor," possibly, subsequent to further investigation, "reproductive division of labor" in some reproductive units." Keep in mind that some human responses will be genetically-correlated.

CONCLUSION: The Major Transitions Approach to the evolution of organismal complexity is the consensus model, including, its assumptions for and applications to conceptualizing and investigating Social Evolution (West et al. 2015) which I hope will be adopted by all Mammalian Social Biologists.

 

 

ACKNOWLEDGMENTS

Too many people to mention individually have contributed to my scientific career, directly and indirectly, by providing information and feedback, as well as, encouragement and constructive criticism. Nonetheless, without the early assistance of Mary Jane West-Eberhard, as well as, the late Harry Levin, the late John F. Eisenberg, and the late Masao Kawai, in addition to, the faculty of Tropical Ecology course, OTS-‘73, my career never would have happened. I appreciate being permitted to use the amazing photographs shared by Chris Faulkes [Fig. 1] and Brian Wood [Fig. 2]. Much gratitude to J. Gordon Faylor for providing the technical expertise required to create a lulu.com text based on my blogpost at vertebratesocialbehavior.blogpost.com. My highest praise and thanks are extended to my son, Miguel Luke Jones, who makes it all possible.

 

 

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