Female traits associated with Mammal Social Evolution [Cooperation (Hamilton); Complex Sociality (specialization)] ... CB Jones, 10/2023

 

Female traits associated with Mammal Social Evolution [Clara B. Jones October 2023]

see 1st blogpost in this blog [link below], Mammal Social Evolution: Major Transitions Approach-- also, available at lulu dot com in hard copy or pinned to my Profile on Twitter [X], @cbjones1943 [see West et al. 2015, cited below]... see, also, cited book linked to my Twitter [X] profile concerning mantled howler monkey (Alouatta palliata) female life-history strategies ...

https://vertebratesocialbehavior.blogspot.com/2022/11/mammal-social-evolution-major.html

c.f. for an early, classic, treatment of Mammal Evolution, including, group-living mammals, see Eisenberg (1971); for an early treatment of females and Mammal Social Evolution, see Wittenberger (1980); among other points, Wittenberger (op. cit.) argued that, for all intents & purposes, mammal females are the "social" sex ... West et al. (2015) is a necessary introduction to "major transitions" & social evolution ...

Terminology & Context: Terminology in the field of Social Biology, here, related to Social Evolution, is not standardized ... for example, WD Hamilton & Stu A. West, define "social" in different ways, the former limiting use of "social" to Cooperation & Altrusim, the two [of four] categories of behavior [Selfish, Cooperation, Altruism, Spite] in which Recipient gains "fitness" benefits ... West, on the other hand, defines "social" as any interindividual interaction where either or both interactants benefit reproductively ... recall that "interdependence" is a necessary precursor to Cooperation, while Cooperation is a necessary precursor to the evolution of Complex Sociality ... here, I am thinking of Cooperation as per Hamilton's general formulation--an interindividual interaction in which both interactants benefit in "fitness"  ... related to the Major Transitions Approach, Complex Sociality [division-of-labor (cooperation between specialists); task, role, &/or morphological specialization] is, particularly, problematic, it seems to me ... if we view specialization along a continuum, say, from feeding specialization to DoL to reproductive DoL with "totipotent" [female] workers or "helpers" to reproductive DoL with more or less "sterile castes" [social insect workers], do we accept the typical usage whereby Advanced Eusocial taxa are the most "complex" societies [the "pinnacle" of sociality as per Wilson (1971)]? ... though many Social Scientists would claim that interindividual interactions in humans represent the "pinnacle" of Complex Sociality, expert consensus among Social Biologists (e.g., Crespi 2014) have concluded that humans cannot be classified, Eusocial, because this species does not display "reproductive division-of-labor," although, the mechanism, Learning, permits humans to maximize the benefits and minimize the costs of generalization & specialization [e.g., (learned) division-of-labor] ... it is worth pointing out that the wide variety of human reproductive structures have not been systematically described, classified, or diagnosed, including, analysis of populations in which more than one architecture is found, such as all modern nation-states [e.g., monogamy, polygamy, promiscuity, etc.] ... whether & how & why these various conformations interact over Time & Space remains to be determined ... it is assumed that 1st Principles [T, E, acquisition, consumption, allocation] relative to abiotic [e.g., climate] & biotic [e.g., food dispersion; breeding sites] environmental regimes, as well as, constraints of limiting resources, as well as, species-typical female traits, always apply ...

Most Mammals are "sexually segregated"* [sometimes termed, "solitary" in the literature], with polygynous male home ranges or territories overlapping the home ranges or territories of however many females he can monopolize ... however, aggregations [temporary clumping of animals] may occur around clumped, limiting resources, especially, food [as, white-tailed deer may do in Spring when food is abundant & clumped]; other aggregations may form when animals migrate from one feeding &/or breeding ground to another; the term "herds" often refers to an aggregation ... the term, "group," is reserved for a reproductive unit ... Hamilton's Rule [rb - c>0 ----> rb > c] is widely accepted as a general formulation of Social Evolution ... according to Hamilton (1964), "social" behavior is limited to Cooperation & Altruism--the only conformations of interindividual interactions [Selfish, Cooperation, Altruism, Spite] whereby Recipient gains in "fitness" ... this definition of "social" should be derivable from Hamilton's equations ...

Mammalian phenotypes are usually generalized (see Eisenberg op. cit.) though there are noteworthy exceptions, & many mammal species display generalized, as well as, specialized, traits ... the evolution of Complex Sociality requires Specialization [division-of-labor; task, role, &/or morphological specialization]; Interdependence [among interacting group members] is a necessary precursor to the evolution of Cooperation ... since Cooperation is a necessary precursor to the evolution of Complex Sociality, specialization must evolve at some point during the Cooperation "grade" ... Hamilton (op. cit.) classifies "cooperation" as an interaction in which both Actor & Recipient benefit reproductively ... as a significant aside, in taxonomic studies, "specialization" is used to diagnose "primitive"/"ancestral" from "derived"/recent characters, where "specialization" is a criterion for "derived" classification ...

Depending upon environmental regime, an advantage of a generalized phenotype is promotion of phenotypic flexibility [reversible response] &/or phenotypic plasticity [irreversible response]--responses that are usually condition-, context-, situation-dependent ... in extreme &/or highly time-varying environments, responses may be "decided" statistically or probabilistically, even under Hamilton's Rule [op. cit.; often termed "kin selection"] ... it is worth pointing out that a] Hamilton's Rule [rb - c >0 ----> rb>c] does not predict that it is always beneficial to assist the reproduction of kin] the evolution of sociality does not necessarily require individual recognition, e.g., "greenbeards" may operate or "decisions" may be based on probabilities or likelihoods ...

The observation that most mammalian phenotypes are more or less generalized is usually attributed to evolution in time-varying environments ... because most mammalian phenotypes are generalized & because Complex Sociality requires the evolution of specialization, it is expected that Complex Sociality, &, possibly, Cooperation, would be uncommon in the Class & in other taxa with generalized phenotypes ... except for cooperatively-breeding mammals & the [eu]social mole rats, reproductive division-of-labor [cooperation between specialists] has not been described to date in mammals, though, "temporal division-of-labor" ["age polyethism"] has been described for mantled howler monkeys (Jones op.cit.) and probably exists in numerous other species, particularly, folivore/herbivores relying on "clumped" limiting resources [e.g., food] ... "bioaccumulation" has been proposed for the evolution of TDL in mantled howler monkeys [see blogpost above] task, role, & morphological specialization are described so far only for the social [eusocial] mole rats & is learned in humans ... several other species of mammals are potential candidates for specialization [see David Macdonald's edited reviews of Mammal Orders, and many species of mammals exhibit both generalized & specialized traits ... in humans, whose phenotypes are generalized in the mammalian mode, the evolution of learning mechanisms permits [learned] specializations such as division-of-labor and task, role specialization ... learning may have evolved in mammals with generalized phenotypes, in part, to minimize the costs of solitary living and maximize the benefits of group-living ... the question of whether morphological specialization has evolved in humans has not, to my knowledge, been systematically studied in humans; however, Race [ecotype] may be a candidate for morphological specialization in Homo sapiens ...

Since most mammals' phenotypes are more or less generalized, the evolution of Complex Sociality [&, possibly, Cooperation] is expected to be severely constrained in the Class ... however, it is noteworthy that some mammals are specialists, & many mammals are characterized by both generalized & specialized traits ... importantly, some mammalian characteristics [e.g., Learning; phenotypic flexibility (reversible) & phenotypic plasticity (irreversible) may have been favored by selection to minimize the costs & maximize the benefits of Generalization &/or Specialization.

1... females are expected to be "energy-maximizers," males, "time-minimizers" (Schoener 1971), a formulation based on 1st Principles ... all female [&/or male] traits/phenotypes should be investigated & measured relative to 1st Principles [Physics: T, E; Ecology: acquisition, consumption, allocation [to survival, &, especially, reproduction] ... see Bateman for evolution of female & male life-history trajectories ["fitness optima"] from initial gamete size [eggs large & costly to produce; sperm many & cheap to produce] ... the evolution of any phenotypic trait can be partitioned into G[enetic] x E[nvironmental] components ... 1st Principles influencing individual [genotype] "fitness" may result from variability of abiotic &/or biotic factors, e.g., climate; dispersion of limiting resources, especially, food, mates, where "dispersion" is the distribution & abundance of limiting resources in Time & Space; interactions with other group members [interindividual events], etc. ... interindividual interactions may be beneficial to, deleterious to, or neutral with respect to an individual's [an entity's] lifetime reproductive success ["fitness"] ... it is imperative for Behavioral Ecologists studying mammals [& other Vertebrates] to investigate the many strategies that have evolved to reduce reproductive, especially, maternal costs ... these strategies often take the form of females' reducing maternal care by one means or another [e.g., "parking;" reduction of fat in milk; evolution of precocial young; "bet hedging;" seasonal breeding, etc.] ... human females are extreme in these strategies since they can reduce maternal costs completely, including, the metabolic costs of ovulation [by culling eggs] ...

2... Vertebrates, social behavior [Cooperation, Altruism, as per Hamilton op. cit.] & Complex Sociality [specialization*], cannot evolve unless females transition from breeding in a solitary state to breeding in a group* [a "bauplan"], & it is important to define what "breeding in a group" can mean ... for example, the offspring of solitary mammal breeders may disperse when the next generation is produced--or, soon after ... this solitary state may, depending upon relative costs & benefits to breeders, including, species-typical traits & environmental regime [abiotic & biotic], evolve to a state whereby young from one generation overlap with the next generation, a precondition for the evolution of Complex Sociality [Specialization, as per "reproductive division of labor" characterizing Cooperative Breeding & Eusociality] ... more commonly in mammals, breeders may form communal units ... other conformations exist, such as, Chimpanzees (Pan troglodytes) for which females coexist more or less in a solitary state with their young in association with other females breeding in a more or less solitary state on overlapping home ranges [also see breeders' conformations in other non-human great apes] ... in this system, related, collaborative [cooperative?] males monopolize some number of female home ranges, & the female sex disperses--opposite from the norm in Mammals ... all non-human ape breeders exhibit a more or less solitary mode of maternal care ... the chimp, and other non-human ape sociosexual pattern may have evolved to minimize costs of breeding in a solitary state while maximizing benefits of breeding in a group, e.g., predator defense, access to mates ... a similar tradeoff may explain the female reproductive strategy in mantled howler monkeys (Alouatta palliata) whereby females breed in a more or less solitary state embedded within a multimale-multifemale sociosexual group structure ... each of the aforementioned examples is characterized by female traits minimizing maternal costs ... female reproductive strategies described for all mammalian sociosexual systems can be assessed for mechanisms to reduce maternal costs [primarily, gestation &, especially, lactation], e.g., "parking" young in protected place, usually, associated with reduced number of nursing bouts; reducing amount of fat in milk--in a few mammalian species, the amount of fat varies with stage of infant development; in groups, mothers may reduce maternal costs by receiving "help" from other group members [usually, other female offspring or female kin], sometimes termed, "allomothering" (Hrdy 1976); mantled howler monkeys reduce the duration of maternal care combined with harsh weaning of young as soon as the issue can feed on its own ... the great apes, except humans, are an interesting case because females breed in groups but permit little contact between offspring & other group members, thereby, assuming high maternal costs, an apparent strategy whereby costs and benefits of group-living are minimized, as well as, maximized ... importantly, humans may be the only animal species in which all reproductive costs can, effectively, be eliminated by females [and males, also]... all phenotypic traits of vertebrate, here, mammal females should be evaluated in terms of their ability to minimize the costs of maternal care ... costs & benefits to young should, also, be evaluated and whether young can ever "win" in "fitness" conflicts with the mother ... Trivers (1972) was of the opinion that, in certain contexts, offspring can "win;" Alexander (1974) was skeptical ... the question can only be resolved by measuring the "fitness" costs of offspring's behavior toward mothers, & vice versa ...

3... Currently, the consensus is that Humans are not characterized by "reproductive division-of-labor;" thus, the consensus is that humans are not "eusocial" (cf. Crespi 2014) ... Human females [& human males] are unique in being able to relieve themselves of reproductive costs except for the production of eggs [ovulation (& ejaculation) can be avoided by culling of eggs (& sperm)] ... this remarkable capacity for reproductive flexibility contrasts with social insect Queens [females] who relieve themselves, obligately, from all tasks associated with reproduction except for insemination, egg production, & laying ... in Mammals, Eusociality may be viewed as a continuum whereby more or less exclusive [though, not, obligate] "Queens" [social mole rats; cooperative breeders] may perform most or all production of offspring and, also, perform other tasks or roles [e.g., feeding of young; defense] ... it is important to note that, given our knowledge to date, all mammalian [more or less non-reproducing] "helpers" are "totipotent," capable of breeding, & mammals exhibit a variety of mechanisms whereby reproduction is suppressed ... as David Macdonald has pointed out, Class Mammalia is characterized by phenotypic flexibility ... as an aside, solitary breeding, non-human great ape breeding mode, Cooperative Breeding, & Eusociality may be differentiated by breeders' relative degrees of task & role specialization [& investment] ...

4... Finally, recall that the evolution of groups* [from group formation to group maintenance], as well as, the evolution of/transition to sociality [Cooperation as per Hamilton op. cit., &, under some environmental conditions, the possible transition (evolution)  to Complex Sociality (specialization: division-of-labor--especially, Reproductive DoL; task, role, &/or morphological specialization)] is not inevitable or necessarily reproductively beneficial from the female's ["fitness"] perspective ... Interdependence, the precursor to the evolution of Cooperation is not inevitable, or, necessarily, beneficial, either ... the evolution of groups depends upon abiotic [e.g., climate] and biotic [especially, (clumped) food dispersion] environmental regimes, as well as, species-typical phenotypic traits ... the evolution of Complex Sociality is necessarily dependent upon the evolution of specialization which must first evolve at some point in the "grade," Cooperation ... in addition to environmental factors, the evolution of the female transition from the reproductive costs & benefits of breeding in a solitary state to breeding in a group depends, in part, upon evolved species-specific  traits of females [& offspring], as well as, environmental context, such as, dispersion of  breeding sites, and predation pressure] ... competition with other females from access to these and other limiting resources will, to a large degree, determine the relative reproductive costs & benefits of breeding in a solitary state to breeding in a group and, ultimately, female dispersion [distribution and abundance in Time & Space] ... a major factor determining whether or not it is reproductively beneficial for females to transition [evolve] from breeding in a solitary state to breeding in a group is her ability to narrow her niche [in particular, her feeding niche], becoming more specialized, in order to minimize competition for limiting resources, one of the major "fitness" costs of group life [see RD Alexander 1974; also, cf. reference cited below] ... in short, ceteris paribus, comparing the relative reproductive costs and benefits to a female from breeding in a solitary state to breeding in a group, either might be most beneficial depending upon initial conditions--species-typical female [& offspring] traits, as well as, environmental regime ... it is not necessarily beneficial for females to breed in groups or for sociality [Cooperation as per Hamilton op. cit.] & Complex Sociality, to, subsequently, evolve ... "decisions" about breeding in a solitary state vs. breeding in a group context depend upon differential costs & benefits to breeders' "fitness" ["relative reproductive success"] ...

*after group-formation, group-maintenance will not evolve unless limiting resources are "clumped" in T & S ... the evolution of group-maintenance is not necessarily beneficial to an organism's lifetime reproductive success ["fitness"] ... some Behavioral Ecologists have hypothesized that groups will not evolve in response to predation alone ...

References

Alexander RD (1974) The evolution of social behavior. Ann Rev Ecol Syst 5: 325-383.

Eisenberg JF (1981) The mammalian radiations: an analysis of trends in evolution. The University of Chicago Press, IL.

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

Hrdy SB (1976) Care and exploitation of non-human primate infants by conspecifics other than the mother. Adv Stud Behav 6: 101-158.

Jones CB (2020) Female mantled howler monkey (Alouatta palliata palliata: Primates, Atelidae) life-history strategies--a "major transitions approach" to mammalian social evolution. lulu dot com

Schoener TH (1971) Theory of feeding strategies. Ann Rev Ecol Syst 22: 369-404.

Sheppard CE, et al. (2018) Intragroup competition predicts individual foraging specialization in a group-living mammal. Ecology Letters 21: 665-673.

Trivers RL (1972) Parental investment and sexual selection. In B Campbell (ed) Sexual selection and The descent of man (1871-1971). Aldine, Chicago, pp 136-179.

West SA, et al. (2015) Major evolutionary transitions in individuality. PNAS 112(33): 10112-10119.

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

Wittenberger JF (1980) Group size and polygamy in social mammals. Am Nat 115: 197-222.

Clara B. Jones, October 2023, Silver Spring, MD, USA