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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

3 A simple model of male → female aggression in mammals

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

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

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

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

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

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

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

Acknowledgments

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

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.

Human Speciation...Constraints...Phenotypic diversity (Clara B. Jones) [To be revised]

Constraints On Speciation In Human Populations: Phenotypic

Diversity Matters

Clara B. Jones^1*

Director, ¹Mammals and Phenogroups (MaPs), Asheville, NC 28801, USA

*Corresponding Author. E-mail: foucault03@gmail.com Phone: -828-279-4429

ABSTRACT:

A phenotype is an expression of a genotype interacting with a component of an environment. Phenotypic diversity can be generated by mutation, physiological mechanisms, developmental processes, or learning (reinforcing and aversive stimulus-response effects). Causes and consequences of lifetime reproductive success can be partitioned into one or another of the previous mechanisms of phenotypic diversity. This article highlights, in particular, the ways in which behavioral diversity including cultural rules, enhances a phenotype’s relative reproductive success. Expanding Frank’s (2011) theoretical framework, it is argued that, while a diverse (e.g., “modular”) human phenotype may broaden a phenotype’s success in a given landscape, byproducts are produced that increase gene flow between populations, limiting the potential for population divergence and reproductive isolation. The mechanisms discussed herein are not necessarily dependent upon conscious and aware operations.

Key words: Homo sapiens; Behavioral flexibility; Collaboration; Cooperation; Fitness landscape; Gene flow; Multilevel societies; Open groups; Phenotypic diversity

INTRODUCTION:

In the Order Primates, thirteen extant genera are represented by a single species (Groves, 2001; Wilson & Reeder, 2005), indicating that mechanisms and processes characteristic of those taxa have delayed, interrupted, or prevented speciation events. Our own species, Homo sapiens, is one of the thirteen. A review of each genus in the set of thirteen reveals few commonalities. With the notable absence of insectivores, virtually all dietary strategies are represented (omnivore, frugivore-insectivore, folivore-frugivore, granivore). No pattern is detected when the thirteen single-species genera are compared for alpha- (α: within-habitat), beta- (β: between-habitat), or, gamma- (γ: geographic)-diversity (Pimm & Gittleman, 1992; Jones, 1997), the overwhelming ecological dominance of humans is unique. Four of the thirteen genera (31%) are nocturnal, and a mix of crepuscular, arboreal, and terrestrial habits is exhibited. Similarly, a broad range of socio-sexual structures is represented among these primate genera, for example, “solitary” (Mirza, giant mouse lemur), “monogamous” (Symphalangus, siamang), polygynous (Erythrocebus, patas monkey), multimale-multifemale (Oreonax, yellow-tailed wooly monkey), and “multi-level” (Theropithecus, gelada; humans).

Eight of the thirteen species (62%) are typically found in one habitat type or demonstrate a strong preference for same. The remaining taxa, including, humans, have been observed in several habitat types, making them good candidates for a number of comparative analyses (genomics, physiology, and behavior, as well as, population, community, and ecosystem ecology), . Significantly, cooperatively-breeding primates are not represented among the subset of thirteen (but, see, Allocebus, hairy-eared dwarf lemur). On the other hand, several genera, are distinguished by elaborate vocal repertoires (e.g., Lemur, ring-tail lemur; siamang; Homo), and all have one or more exaggerated anatomical or morphological features (e.g., pelage, coloration, genital structures), suggesting evolution by sexual selection, a controversial mechanism of speciation (“macroevolution”: Servedio & Kopp, 2012). Insufficient empirical data exist on the relative significance of historical geographical barriers to gene flow that might have facilitated the speciation process (Jones, 1987; Groves, 2001) or of the roles played by habitat specificity (“habitat selection”: Jones, 1997; but, see Erythrocebus) in limiting a genus to a single species, a condition obscuring patterns that may exist in Nature.

In the present paper, humans are highlighted in an attempt to identify both general and specific features constraining differentiation of their populations into interbreeding, reproductively-isolated units (“the biological species concept”: see Rundle & Boughman, 2010). Such analyses may contribute to our understanding of Homo sapiens as a “weedy”, invasive species, the most geographically and ecologically successful taxon among terrestrial vertebrates. Though many aspects of human biology are relatively well-known, the capacity of technological societies to maintain high population densities (high α-diversity), to successfully invade virtually all global habitats (high β-diversity), to modify their areal ranges (high γ-diversity), to utilize effective mechanisms of niche invasion and expansion (e.g., cooperation, social learning, fire, tools, migration, war), and to impose profound, deleterious effects on global biogeochemistry demand systematic treatments of hominin ecology, phylogeny, and evolution (Hill et al., 2011). Herein, a tentative attempt is made to identify selected human characteristics associated with interruption, delay, or prevention of reproductive (genetic) barriers (e.g., incompatible habitats, “isolation by distance”, pre- or post-copulation mate selection, or geographic barriers such as rivers, mountains, and soil gradients) sufficient to transition from between-population gene exchange, to (genetic) differentiation of populations (“population divergence”), to the creation of genetic barriers and a completed process of speciation. Behavior and social organization are likely to interest a significant proportion of this journal’s readers. Thus, the present discussion emphasizes phenotypic diversity and population structure, as well as, learning to explain the systematic status of Homo sapiens. This paper introduces a novel interpretation and application of the single-species status of extant Homo inferred from Frank’s (2011) treatment of the mechanisms “smoothing” a “rugged” fitness landscape. Questions regarding the nature of sub-species or racial identities in Homo sapiens are referred to Anthropologists.

Genetic differentiation within and between human populations: incipient speciation?

Genetic differentiation and, possibly, incipient speciation of human populations have been documented. Numerous studies exist identifying clusters (“neighborhoods”) of “single-nucleotide polymorphisms” (SNPs) in human populations, a pattern of results suggesting a past, possibly, continuing, process of adaptation to local abiotic (e.g., soil gradient) or biotic (e.g., plant gradient) regimes (“local adaptation”), a phenomenon similar to “habitat selection”. For example, Xing et al. (2009; also, see ISWG, 2001) identified “shared [genetic] variation” among 27 human populations in Africa, Asia, and Europe, including, “caste and tribal samples” in India, demonstrating a degree of genetic continuity across geographical regions. Further statistical analyses of “SNP microarrays” (“haplotypes”: closely-associated alleles on one chromosome), however, revealed genetic structure between sampled sites, and notably, most individual subjects were accurately assigned to the correct population. All individuals were accurately mapped to continents, though genetic structure was not detected for some “closely-related populations”. Xing et al. (2009) concluded that their results confirmed a statistically significant association between geography and genetics, including social sub-groups (“caste and tribal” sub-populations). Despite the strong patterns revealed by the previous study, it is important to note that the authors’ findings pertain to differences in genetic structure within and between populations, and do not specify the functions (genotypes expressed as phenotypes) of those discernible genotypes.

What mechanisms might determine genetic structuring and differentiation of human populations?

Fowler et al. (2011; also, see Henry et al., 2011; Brent et al., 2013) considered “genetic stratification” within and between human populations to be a function of mate selectivity or kin preferences. These authors investigated whether or not variations in specific genes were associated with social networks of “friends”, where friendship was defined as “stable, non-reproductive [non-sexual] unions”. Using microarray analyses, Fowler et al. (2011) demonstrated that one allele, DRD2, was associated with homophily (assortment of similar types), while, another allele, CYP2A6, was associated with heterophily (assortment of different types). The aforementioned study assessed virtually every possible interpretation and implication of the report, concluding, that “phenotypic similarities between individuals connected in a social network are reflected in their genotypes”. This hypothetical construct, derived from empirical data, advanced the idea that some social traits are correlated with genotype, an association requiring some direct or indirect mechanism of individual recognition. A straightforward extension of the Fowler et al. (2011; also, see Fu et al., 2012) report is that, where (genetically-correlated) homophily recurs over time, reproductive isolation of similar genotypes is expected to occur, that, left unimpeded, has potential to induce barriers to gene flow decreasing likelihoods of genetic “mixing” within and between populations. The latter scenario proposes a necessary, though not sufficient, condition for speciation to occur. The present paper addresses some of the behavioral mechanisms and processes limiting reproductive isolation and preventing speciation in Homo sapiens, emphasizing the ways in which human technology and other innovations (e.g., tools, fire, language, ritualized warfare) have ameliorated the potentially disruptive effects of “rugged” landscapes that might enhance a process leading to speciation.

The aforementioned extension of the research reported by Fowler et al. (2011) provides a plausible explanation for the latter authors’ findings as well as for the findings of Xing et al. (2009). The extension is amenable to quantitative (“individual”- or “agent-based”) modeling as well as empirical testing with opportunistic, “natural experiments” of concurrent mate choice/genotype trait analyses using human subjects in natural conditions. The “green beard effect” is a possible candidate as a sexually-selected mechanism of homophily, including, interindividual recognition (Brooks & Griffith 2010; Gardner & West, 2010), possibly an element of a primate social “toolkit”. For example, suggesting a mechanism for a “greenbeard effect”, Mahajan et al. (2011) identified “inter-group bias” (homophily) in Rhesus macaques (Macaca mulatta). These monkeys, residing in semi-natural conditions, discriminated between in-group and out-group members, demonstrating a reliable choice for particular individuals in their social groups.

Interindividual recognition of the sort reported by Mahajan et al. (2011) probably characterizes all primates whose brains categorize and compartmentalize information into simpler units (Sporns, 2011). Thus, it is no surprise that environmental patterns are classified systematically by a variety of rules, including similarity, proximity, or other assortative features (e.g., psychophysical operations: Matsuno & Fujita, 2009). Recent work by Yun et al. (2012) demonstrates another possible “green beard” (interindividual recognition) mechanism: synchrony of motor patterns between interacting individuals (e.g., gestures: Pollick & DeWaal, 2007; also, see Brooks & Griffith, 2010, Nagasaka et al. 2013). “Greenbeard” traits may be genetically correlated, and the latter in addition to other features (e.g., skin color, morphology) may have facilitated speciation in one genus (Macaca), but interrupted the process in humans, depending upon differential genotype x environment and phenotype x phenotype interactions..

For example, human groups may be more permeable than non-human primate groups, or humans may use a broader range of characters when making decisions about who to associate with. Furthermore, on average, humans may receive greater benefits from associating with different types compared to speciose primate genera. The latter case might be expected where intra-group competition is more intense than inter-group competition (West et al., 2002). Peculiar features of our species, then, may have broadened the areal effect of an individual’s reproductive success in “rugged” landscapes (“fitness landscape”), and phenotypes bearing these features are proposed to have directly or indirectly promoted gene flow within- and between-groups, -populations, and -regions limiting the potential for population divergence, reproductive isolation, and speciation. Other primate genera characterized by a single species are presumed to exhibit traits that spread because of their success in managing thresholds of intra-group competition, subsequently decreasing the likelihood of speciation events by facilitating gene flow, preventing reproductive isolation.

Notwithstanding evidence for clustering of genotypes within and between populations, human behavioral diversity appears to enhance gene flow

Using Frank’s (2011) theoretical framework, I posit that numerous genetically correlated or uncorrelated behavioral and social traits characteristic of human phenotypes mediated genotype-environment and phenotype-phenotype interactions (“reaction norms”). Human technological and other innovations (e.g., language, metacognition) are proposed to have increased the proportional area on an idealized (theoretical, multidimensional: Frank, 2011) or realized (a 3-dimensional abiotic and biotic environment: this paper) “landscape” upon which a genotype, expressed as a phenotype, is more reproductively successful relative to the mean lifetime reproductive success of other genotypes in a population. This perspective can be visualized by imagining a grid superimposed on a space subdivided into areas defined by shared features (e.g., a habitat, a watering hole, a grove of fruiting trees, other singular or clumped resources).

Frank’s (2011) treatment allows us to conceptualize a landscape on which reproductively successful phenotypic innovations generated and spread by mutation, developmental plasticity, or learning increased the proportion of cells on the grid upon which a phenotype is effectively successful. In other words, an individual’s “fitness landscape” will be, proportionally, increased relative to the mean fitness of others in a population not exhibiting the successful traits. In Frank’s (2011) terminology, the aforementioned process is a “smoothing” operation reflecting a phenotype’s capacities to decrease stressful environmental events where degrees of stress can be conceptualized as the extent to which the landscape approximates a very rugged (challenging) or a relatively even (less challenging) space in which to survive and reproduce.

Frank’s (2011) treatment suggests that phenotypic diversity will be induced by novel (e.g., disappearance of a limiting resource) or extreme (e.g., severe drought) environmental events and that responses may be genetic (mutation), cellular (physiological and developmental), or learned (by trial-and-error or by “Hebbian” association). Applied to humans, the present treatment posits that characteristics such as cooperation, tool use, the application of fire for processing food, the manufacture of clothing, language, long-distance dispersal, social learning, and the like, effectively switched an environment (“landscape”) from a stressful (difficult, dangerous, risky, extreme, novel), “rugged” one, to a less stressful, more even, or “smoother” one. Reproductively successful innovative human phenotypes, it is proposed, extended networks within- and between-groups and –populations, connecting networks to one or more resource patches, including, other human individuals and groups, thereby, broadening the effective spaces of phenotypes, decreasing deleterious consequences of environmental challenges for (relative) individual reproductive rates, growth rates of groups, and mean fitness of populations.

Traits characteristic of non-human primates and humans interrupt or prevent population divergence

Empirical examples drawn from the primate literature characterize Frank’s (2011) concept of mechanisms functioning to “smooth” a challenging (“rugged”) landscape. Analyzing species distribution patterns of black howler monkeys (Alouatta pigra) and Central American spider monkeys (Ateles geoffroyi) in Belize, Jones & Jost (2007) showed that black howlers, but not spider monkeys, had successfully traversed the Mayan Mountains/Cockscombe Range in southern Belize. Howler monkeys are adapted to a folivorous diet, an evenly distributed supply of food compared to fruit upon which spider monkeys are heavily dependent. As a consequence of the heterogeneous and often unpredictable availability of their food supplies, Ateles is expected to be more sensitive to environmental perpurbations (Terborgh & Winter, 1980). The ability to consume old leaves is thought to facilitate colonization (Jones & Jost, 2007), providing a relatively accessible food resource in most habitats, allowing flexible “switching” from howlers’ preferred diet (new leaves, flowers, fluit) to less nutritious and physiologically stressful foods (mature leaves) during periods when favored food items are unavailable or scarce (Milton, 1980; Crockett, 1998; Hamilton, 2010).

On the other hand, a diet of fruit presents many challenges because of its low nutritional value and patchy distribution (Terborgh & Winter, 1980; Fleming et al., 1987), factors that may limit or retard the geographical spread of species if appropriate food types or habitats are not encountered. This comparison demonstrates one behavioral mechanism, enhanced niche width, whereby the configuration of landscapes is modified by spatiotemporal effects. The capacity to process old leaves facilitated construction of a comparatively “smooth” landscape for the widely distributed, speciose, hardy genus, Alouatta. Another “smoothing” effect occasioned by a folivorous diet may be reduction of costs from predation, since toxins ingested from leaves may decrease the palatability of howler tissues, a hypothesis supported by one study’s findings that human hunters considered spider monkeys (frugivores) a tastier meat than that of howlers (Jones & Jost, 2007). Differential attractiveness, then, may “smooth” prey landscapes while increasing the ruggedness of predators’. However, the speciose genus, Alouatta, is considered to have differentiated via a process of dietary and geographical partitioning, or, possibly, hybridization (Bicca-Marques et al., 2008). Human adaptations, combined with learning capacities, including cultural exchange, presumably avoided many dietary challenges (e.g., fire, tools, weapons), outweighing deleterious effects, including, tradeoffs, that might have been associated with the innovations (e.g., increased inter-group competition).

Concepts advanced by Frank (2011) are implicit in field research conducted in Mexico by Chaves and his colleagues (2012; also, see Scherbaum & Estrada, 2013). These authors studied Ateles geoffroyi in two conditions of rainforest habitat, continuous canopy and fragmented patches, in order to compare and contrast utilization of available food resources. Consistent with expectation, niche width of monkeys inhabiting fragmented forest was wider than that for monkeys in undisturbed forest, including a higher proportion of leaves. Chaves et al. (2012, pp 109-111) concluded, “It is unlikely that [small fragment size] can maintain viable populations in the long term, they may function as stepping-stones [italics added], facilitating inter-fragment movements and, ultimately, enhancing seed dispersal in fragmented landscapes.” Combined, where necessary, with descent from trees and ground movement, increased niche breadth enhances the behavioral repertoire of spider monkeys, facilitating “initial survival of a genotype in response to novel or extreme environmental challenges, providing an opportunity for subsequent adaptation.” (Frank, 2011, pp 2318-2319). Additionally, variations in other non-human primate traits may function to “smooth” landscapes in feeding and foraging contexts, for example, body size (Wheatley, 1982), “time-energy [“fitness”] budgets” (Grueter et al., 2012), “decision and choice” (Scherbaum & Estrada 2012), social behavior among females (Hanya et al., 2008), “co-residence patterns” and other hunter-gatherer features (Hill et al., 2011), “egalitarian” and other prosocial tendencies (Gavrilets, 2012).

The previous paragraphs in this section presage human habits serving similar functions. Jones & Young (2004), for example, surveyed hunters in Belize, demonstrating that, among non-volant terrestrial or semi-terrestrial vertebrates, niche width varied with food availability, implying an opportunistic (“utilitarian”) strategy based on a hierarchy of preferences. Thirty-four hunters ranked their favorite prey, yielding eight vertebrate species, with paca (Agouti paca) reported to be the most favored bushmeat, “hicatee”, the Central American river turtle (Dermatemys mawii), the least. Prey characteristics (predominantly medium-sized, crepuscular or diurnal, and terrestrial) suggested that energetic factors influenced hunting behavior by Creole men at this site, possibly influenced by gustatory preferences, as suggested above. Indeed, paca’s rich, non-“gamey”-tasting flesh, is considered a national delicacy. Hunting practices of indigenous Belizeans are strongly influenced by cultural practices, in addition to economic ones (Jones & Young, 2004; also, see Wilkie & Godoy, 2001), consistent with Frank’s (2011) emphasis on phenotypic variation (e.g., niche breadth) and learning (e.g., imitation, observational learning, cultural rules) as factors “smoothing a fitness landscape with multiple peaks and valleys”. Combined with spatial “concentration and dispersion” of human populations facilitating the evolution of multilevel population structure, phenotypic diversity in humans broadens a phenotype’s success in a given landscape, while, concurrently, increasing gene flow between populations, effects limiting the potential for population divergence and reproductive isolation.

Humans benefit from phenotypic diversity and learning

Following Frank’s (2011) conceptual framework, the present article posits that numerous traits characterizing Homo sapiens served to decrease environmental challenges deleterious to lifetime reproductive success of individuals. These technological and other innovations, once spread through groups, populations, and regions via sex and social learning increased social and breeding networks, mitigating environmental and social challenges. Tanaka’s (1976) studies of the ≠Kade San (“bushmen”), hunter-gatherers in the Kalahari (southern African desert) clearly demonstrate ways in which a cultural innovation limits mortality and, by extension, enhances reproductive success. The ≠Kade San, comprised of mobile and mobile-subsistence units, inhabit a “marginal” environment characterized by drought (Tanaka, 1976, Fig. 4.1, p 105) and seasonal patterns of food availability (Tanaka, 1976, Fig. 4.2, p 108), a spatiotemporal regime not unlike the heterogeneous environments in which humans are thought to have evolved (Hill et al., 2011). On one occasion, Tanaka (1976) observed chacma baboons (Papio ursinus) foraging in the Kalahari, noting that this primate’s home range was limited by their inability to cross arid land. This researcher compared the monkeys’ habits with those of the ≠Kade San, capable of inhabiting the extreme desert environment as a result of digging through the soil surface to locate and utilize the limiting resource. This cultural practice permits a “band” to expand inherent capacities, “smoothing” effects decreasing likelihoods of sub-lethal or lethal outcomes, and increasing the likelihood of contacts with other “bands” (see below). Such phenotypic diversity is expected to impact individual life-histories (survival and mortality), enhancing mean fitness of populations via increased reproductive rates (Frank, 2011), with consequent effects on higher levels of ecological organization (communities, ecosystems, biomes).

“Bands” of “bushmen” from a variety of cultural groups share the desert environment, sometimes interacting with one another (cf. Lee, 1976, Map 3.2, p 85; Map 3.3, p 87; Map 3.4, p 93; also, see Tanaka, 1976; Hill et al., 2011). These flexible land-use patterns (“spatial organization”), limited by availability of water, are one component of a “rugged landscape”, ensuring relatively frequent contact with other cultural groups. As Tanaka’s (1976; also, see Lee’s chapter in the same volume) chapter highlights, fluid patterns of interaction increase potential for conflicts which the bands prevent or resolve via cultural innovations such as reciprocity, cooperation, common ceremonies, and the like, minimizing conflict and aggression, permitting shared access to resources, cooperative manufacture of tools and weapons, and overlapping ranges. Though Tanaka’s (1976) report does not address the nature of intimate relations among “bands” (see Lee, 1976), transfer of individuals between groups and opportunities for sexual congress probably occurred, leading to gene flow sufficient to prevent reproductive isolation and speciation events. This scenario is consistent with the interpretations of hunter-gatherer data reviewed by Hill et al. (2011).

The evolution of human prosocial behaviors and constraints on speciation

Two recent papers provided a detailed empirical review of “co-resident patterns in hunter-gatherer societies” (Hill et al., 2011) and a preliminary quantitative (mathematical) treatment of “the egalitarian syndrome” characterizing Homo sapiens (Gavrilets, 2012; see Crook, 1971). Hill et al. (2011) analyzed datasets for 32 extant hunter-gatherer societies with a mean “band” size of 28.2 individuals. These authors documented a profile including bisexual dispersal from natal groups, similar to other apes and Neotropical Atelines. Though opposite-sex [adult] siblings resided, with some frequency, in the same reproductive unit, group membership comprising non-kin prevailed across “bands”. Patterns of kinship and group architecture resulting from dispersal, resulted in nested networks of relatives and non-relatives from “bands” embedded in local (“patch”) contexts to higher levels of sociosexual organization. These “multilevel” (“hierarchical”) societies exhibited relatively “open” structures, permitting selective immigration and emigration, and have been described for other mammalian taxa (e.g., some cetaceans, elephants, geladas; Hamadryas baboons, Papio hamadryas).

In “hierarchical” and other complex societies, problems associated with temporal and spatial coordination and control must be managed, and the theoretical literature on “scheduling” indicates that such challenges are solved via within- and between-group “queuing” (Andrews, 2004; also, see Alberts et al., 2003; Fruteau et al., 2013). Within- and between-levels, hunter-gatherers exhibit a broad array of mechanisms, effectively, (1) increasing the similarity of shared fitness optima (“fitness-sharing”: Sareni & Krähenbühl, 1998) and (2) decreasing asymmetries (“egalitarian syndrome”: Gavrilets, 2012). Hill et al. (2011), and most other students of human behavior and social organization (e.g., Crook, 1971; 1972; Eibl-Eibesfeldt, 1989; West et al., 2006), characterize these mechanisms as one or another manifestation of “cooperation” (and/or collaboration). However, despite the benefits provided by cooperation, queuing, and similar features in many conditions, limits on “prosocial” behavior in humans must, also be addressed (Jones, 2005a, b; Burton-West et al., 2006; Chellew & West, 2013).

The two aforementioned mechanisms are consistent with Frank’s (2011) “smoothing” paradigm, operating to “solve” environmental challenges, to repress selfishness and competition, to enhance access to resources, and to decrease inter-individual and inter-group conflicts. In these instances, social traits benefiting a conspecific’s fitness are posited to limit morbidity and mortality, as well as to enhance relative reproductive rates compared to benefits that might accrue from alternative, selfish interactions (e.g., “non-damaging” and “damaging” aggression). Discussing hunter-gatherer “spatial organization”, Lee (1976) employed maps to show how patterns of “concentration and dispersion” promote inter-unit cooperation (“reciprocal access to resources”), flexible access to abundant and scarce resources via communication networks, and conflict-management via “social” separation. Lee (1976) found that “concentration and dispersion” increased unit size, on average, an effect that he showed was correlated with higher rates of population increase.

Clustering of “bands” at “patchy” sources of water and food may have induced social competition, leading to social selection favoring the evolution of collaboration, cooperation and behavioral diversity (e.g., social learning, imitation, tool use). Increased inter-individual contact with associated gene flow would be a byproduct of this model, discussed using primate examples, by Crook (1971, 1972; also, see Lee, 1976; Tanaka, 1976; Yellin, 1976). As a result, likelihoods of gene flow between reproductive units (“bands”) would increase, decreasing rates of population divergence and opportunities for speciation events. The fitness strategies discussed in this paragraph constitute adaptive mechanisms responding to environmental challenges, transforming a rugged landscape to a smoother one, enhancing lifetime reproductive success of individuals. Interpretations of the literature advanced in this article are testable empirically and quantitatively, and initial agent-based treatments might be conducted employing the data presented in Hill et al. (2011). It would also be beneficial to compare populations and regions exhibiting high, moderate, and low degrees of genetic differentiation in an attempt to discern similarities and differences among humans and their networks in each condition. For instance, is network strength greater or lesser across these conditions, and do these conditions and their features correlate with measures of success (e.g., income, education, rules governing immigration and emigration).

DISCUSSION

Frank’s (2011) treatment of the ways in which phenotypic diversity and phenotypic novelty serve individual interests by facilitating lifetime reproductive success provides a schema that can be applied to most human tactics and strategies. In particular, the model permits researchers to evaluate the extent to which human responses to environmental challenges promote problem-solving in a variety of ways. The mechanisms addressed herein, as well as other responses not discussed (altruism, spite, role-reversal, facultative division-of-labor), are expected to facilitate the individual’s avoidance, circumvention, delay, or confrontation with challenges sufficiently severe, risky, rare, or difficult to compromise lifetime reproductive success, including, the effects of morbidity and mortality. Mortality records for extant hunter-gatherers require quantitative treatments since humans are iteroparous breeders with a typical litter-size of one, characteristics associated with predictable environments in which adult survivorship is uncertain (Stearns, 1982; Millar & Zammuto, 1983). Breeding positions of individuals in mammal groups with the aforementioned characteristics are generally precarious (Millar & Zammuto, 1983), and the diverse phenotypic adaptations and novelties reviewed herein may increase environmental predictability by increasing individuals’ abilities to cope with stressors.

Following Hill (1976), humans appear to combine iteroparity with a high fertility rate and notably high “reproductive effort”. This combination of traits is not usually associated with mammals in heterogeneous (“rugged”) regimes (Millar & Zammuto, 1983). Similarly, most mammals are poor colonizers, and social mammals are generally constrained by their dependence upon conspecifics and group life (Cody, 1986), challenges that humans have overcome via the “concentration and dispersion” spatiotemporal patterns and multilevel societies described by Lee (1976), Tanaka (1976), Yellin (1976), and others (Hill et al. 1976), in combination with rule-governed repression of selfish behavior (“culture”). Investigating patterns of juvenile and female mortality should reveal relative survivorship, indicating whether or not “bet-hedging” strategies were featured among early Homo. This information, once modeled, may expose in greater detail thresholds of reproductive benefits that may have accrued to humans from responses designed to solve problems presented in lethal or sub-lethal regimes, mechanisms with byproducts decreasing likelihoods of reproductive isolation and the potential for speciation. Finally, students of mammalian taxa exhibiting noteworthy phenotypic diversity (e.g., mammals exhibiting multilevel social organization) must bear in mind that “plastic” traits will not yield the highest relative fitness in many regimes (Jones, 2005a, 2005b; Pigliucci, 2010, Frank, 2011, pp 2312-2313). Thus, differential reproductive costs and benefits of genotype x environment interactions require systematic investigation for the human case.

ACKNOWLEDGMENTS:

I am grateful to Steven A. Frank for commenting on an earlier version of this paper. Jesse Marczyk’s extensive critique significantly improved the manuscript.

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Citation: Jones CB. 2013. Constraints On Speciation In Human Populations: Phenotypic Diversity Matters. Hum Bio Rev, 2 (3), 263-279.