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 female’s
fitness (increased intensity of intra- and inter-sexual
interactions). May & Anderson’s equation can be modified for
male parasitism of females such that
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 male’s
responses (e.g., by increasing future reproductive rate or switching
to behaviors decreasing likelihoods of male aggression).
The
above scenario may lead to coevolved states between aggressive
males and their female targets or to effective mechanisms of female
defense where females are able to discriminate aggressive from
non-aggressive males, and May & Anderson’s
formula might be employed to predict conditions under which benefits
to males from aggression decrease (e.g., where virulence,
transmission, and recovery rate are independent: Moore 2002;
atelids?, bonobos?).
The
topics discussed in the present note and elsewhere, as well as
related questions and propositions, wait systematic quantitative
modeling and tests, in combination with naturalistic description and
controlled studies under laboratory and field conditions (e.g.,
surgical manipulation of genitalia; regulatory mechanisms).
4
Conclusions, perspectives and directions: the eco-ethology of male →
female aggression
The
previous discussion of adult male → female aggression (MFA)
highlights tactics, strategies, and mechanisms whereby an initial
Signaler (Actor) has the potential to influence the expression and
evolution of traits in a Recipient. Each interaction may affect
statistical parameters of social competition between members of the
pair, third parties in a group or population (“indirect effects”),
including, mutualists and predators. MFA may be regarded as a
time-minimizing, uni- or multi-modal (visual, tactile, auditory,
olfactory) strategy that, in some lineages, occurs as a ritualized
display, a transition expected to reduce costs from aggression for
adult males and adult females. For example,“solitary”
(sexually-segregated) male ground squirrels (Citellus armatus)
and “solitary” male palm squirrels (Funambulus pennant),
with slightly ritualized behavioral repertoires, are notably
aggressive toward females during courtship, while,“solitary” male
grey squirrels (Sciurus carolinensis), displaying somewhat
greater phenotypic ritualization, are less aggressive during
courtship than the two previous species. Aggression is, effectively,
absent in the“solitary” European red squirrel (Sciurus
vulgaris) with highly stereotyped courtship signals and displays.
Of import, compared with its relatives, European red squirrels
inhabit spatiotemporally- and thermally-stressful, deciduous
habitats, highlighting the need for ecological and evolutionary
studies, including, experiments, of ritualized signals and displays
in sexually-segregated and social mammals.
Acknowledgments
I
am grateful to Phyllis C. Lee for helpful feedback that significantly
improved this note.
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.