Sunday, December 30, 2018

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


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


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

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

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

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

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

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

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

It has been suggested that male and female mammals engage in an ongoing evolutionary “arms race” to impose greater (reproductive) costs on each other or to “hold one’s own” in such a competitive “chase”. Males appear to have more influence in some taxa (Agouti; Northern elephant seals: Mirounga angustirostius; walrus: Odobenus rosmarus; Hamadryas baboons: Papio hamadryas; chimpanzees: Pan troglodytes; lions: Panthera leo; domestic cats: Felis catus). In other taxa, females have, apparently, more influence (Hawaiian monk seal: Monachus schauinslandi, lemurs: Lemuridae; bonobo: Pan paniscus; mantled howler monkey: Alouatta palliata; coati: Nasua narica; African elephant: Loxodonta africana; reindeer: Rangifer tarandus), including, species in which females are dominant to males. In a few species, intersexual relations have been characterized as “egalitarian” (striped mice: Rhabdomys pumilio, fox: Lycaon; muriquis:Brachyteles arachnoids), while, in others, intersexual influence and “power” generally vary by context (squirrel monkeys: Saimiri spp.; most socially “monogamous” mammals involving single male-single female co-residence; humans: Homo sapiens). P.C. Lee (personal communication) suggested that the previous patterns may be influenced by alternative reproductive strategies employed by males, reported for grey seals (Halichoerus grypus).
According to Estes (1992), aggression, including coerced or forced copulation (“rape”: orangutans: Pongo; Northern elephant seals), by males → reproductive females, is likely to be favored by selection in two conditions. First, females of polygynous mammalian species (red deer: Cervus elaphus, hartebeest: Alcelaphus caama) don’t copulate outside their receptive periods. Polygynous human systems represent one exception to this pattern. My review of (carnivorous) pinnipeds, as well as other mammal groups, strongly suggests that high levels of male → female aggression is associated with non-ritualized behavioral repertoires (ground squirrel: Citellus armatus, humans), high population density, breeding on land (pinnipeds), a “catholic” (broad niche or opportunistic) diet (pinnipeds, humans), male dominance hierarchies (rather than resource- or female-defense: lions, chimpanzees), limited periods of male or female fertility (lions, walrus: Odobenus rosmarus), high infant mortality (polygynandrous lions; Northern elephant seals; but, see, mastiff bats: Tadarida brasiliensis), multiple-mating by females (chimpanzees), and very lengthy periods of female pregnancy, lactation, or maternal care (chimpanzees, humans). Thus, a suite of ecological, including, social, factors facilitates male trajectories, and it is unclear to what extent reproductive males or females embody opportunities to override these conditions, topics in need of investigation.

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

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

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

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

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

3 A simple model of male → female aggression in mammals

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

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

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

The above scenario may lead to coevolved states between aggressive males and their female targets or to effective mechanisms of female defense where females are able to discriminate aggressive from non-aggressive males, and May & Andersons formula might be employed to predict conditions under which benefits to males from aggression decrease (e.g., where virulence, transmission, and recovery rate are independent: Moore 2002; atelids?, bonobos?).
The topics discussed in the present note and elsewhere, as well as related questions and propositions, wait systematic quantitative modeling and tests, in combination with naturalistic description and controlled studies under laboratory and field conditions (e.g., surgical manipulation of genitalia; regulatory mechanisms).

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

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



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



References
Brooks, R., & Jennions, M.D. 1999:. The dark side of sexual selection. Trends Ecol. Evol. 14, 336-337.
Clutton-Brock, T.H., ed. 1977: Primate Ecology. Academic, New York.
Estes, R. 1992: The Behavior Guide to African Mammals Including Hoofed Mammals, Carnivores, and Primates. University of Chicago Press, Chicago, IL.
Jones, C.B. & Cortés-Ortiz, L. 1998: Facultative polyandry in the howling monkey (Alouatta palliata): Carpenter was correct. Boletin Primatologico Latinamericano 7, 1-7.
Moore, J. 2002: Parasites and the Behaviour of Animals. Oxford University Press, Oxford, UK.