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.

REFERENCES:

Alberts SC, Watts HE, Altmann J. 2003. Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus. Anim Behav 65: 821-840.

Andrews M, Kumaran K, Ramanan K, Stolyar A, Vijayakumar R, Whiting R. 2004. Scheduling in a cueuing system in asynchronously varying service rates. Prob Eng Info Serv 18: 191-217.

Bicca-Marques JC, Prates HM, Cunha de Agular FR, Jones CB. 2008. Survey of Alouatta caraya, the black-and-gold howler monkey, and Alouatta guariba clamitans, the brown howler monkey, in a contact zone, State of Rio Grande do Sul, Brazil: evidence for hybridization. Primates 49: 246-252.

Boardman JD, Domingue BW, Fletcher. 2012. How social and genetic factors predict friendship networks. Proc Natl Acad Sci USA 109: 17377-17381.

Brent LJN, Heilbronner SR, Horvath JE, Gonzalez-Martinez J, Ruiz-Lambides A, Robinson AG, Skene JHP, Platt ML. 2013. Genetic origins of social networks in Rhesus macaques. Sci Rep 3 doi: 10.1038/srep01042.

Brooks RC, Griffith SC. 2010. Mate choice. In: Westneat DF, Fox CW, editors. Evolutionary behavioral ecology. Oxford University Press, Oxford, UK. p 416-433.

Burton-Chellew M, West SA. 2013. Prosocial preferences do not explain human cooperation in public goods games. Proc Natl Acad Sci USA doi.10.1073/pnas.1210960110.

Chaves, ÓM, Stoner KE, Arroyo-Rodriguez V. 2012. Differences in diet between spider monkey groups living in forest fragments and continuous forest in Mexico. Biotropica 44: 105-113.

Cody ML. 1986. Diversity, rarity, and conservation in Mediterranean climate regions. In: Soulé ME, editor. Conservation biology. Sinauer, Sunderland, MA. p 123-152.

Crockett CN. 1998. Conservation biology of the genus Alouatta. Int J Primatol 19: 549-578.

Crook JH. 1971. Sources of cooperation in animals and man. In: Eisenberg JF, Dillon WS, editors. Man and beast: comparative social behavior. Smithsonian Institution Press, Washington, DC. p 236-260.

Crook JH. 1972. Sexual selection, dimorphism, and social organization in the primates. In: Campbell B. editor. Sexual selection and the descent of man, 1871-1971. Aldine, Chicago, IL. p 231-281.

Eibl-Eibesfeldt I. 1989. Human ethology. Aldine de Gruyter, New York.

Emmons LH. 1984. Geographic variation in densities and diversities of non-flying mammals in Amazonia. Biotropica 16: 210-222.

Fleming TH, Breitwisch R, Whitesides GH. 1987. Patterns of tropical vertebrate frugivore diversity. Annu Rev Ecol Syst 18: 91-109.

Fowler JH, Settle JE, Christakis NA. 2011. Correlated genotypes in friendship networks. Proc Natl Acad Sci USA 108: 1993-1997.

Frank SA. 2011. Natural selection. II. Developmental variability and evolutionary rate. J Evol Biol 24: 2310-2320.

Fruteau C, van Damme E, Noë R. 2013. Vervet monkeys solve a multiplayer “Forbidden Circle Game” by queuing to learn restraint. Curr Biol 23: 665-670.

Fu F, Nowak MA, Christakis NA, Fowler JH. 2012. The evolution of homophily. Sci Rep 2 doi: 10.1038/srep00845

Gardner A, West SA. 2010. Greenbeards. Evolution 64: 25-38.

Gavrilets S. 2012. On the evolutionary origins of the egalitarian syndrome. Proc Natl Acad Sci USA 109: 14069-14074.

Geisel JT. 1976. Reproductive strategies as adaptations to life in temporally heterogeneous environments. Annu Rev Ecol Syst 7: 7-80.

Groves C. 2001. Primate taxonomy. Smithsonian Institution Press, Washington, DC.

Grueter CC, Li D, Ren B, Li M. 2012. Overwintering strategy of Yunnan snub-nosed monkeys: adjustments in activity scheduling and foraging patterns. Primates doi.10.1007/s10329-12-0333-3

Hamilton IM. 2010. Foraging theory. In: Westneat DE, Fox CW, editors. Evolutionary behavioral ecology. New York: Oxford University Press, New York. p 177-193.

Hanya G, Matsubara M, Hayaishi S, Zamma K, Yashihiro S. 2008. Food conditions, competitive regime, and female social relationships in Japanese macaques: within-population variation. Primates 49: 116-125.

Henry AD, Pralat P, Zhang C-Q. 2011. How social and genetic factors predict friendship networks. Proc Natl Acad Sci USA 108: 8605-8610.

Hill KR, Walker RS, Božičević M, Eder J, Headland T, Hewlett, Hurtado AM, Marlowe F, Wiessner P, Wood B. 2011. Co-residence patterns in hunter-gatherer societies show unique human social structure. Science 331: 1286-1289.

International SNP Working Group (ISWG), 2001. A map of human genome sequence variation containing 1.42 million SNPs. Nature 409: 928-933.

Jones CB. 1987. Evidence supporting the Pleistocene forest refuge hypothesis for primates. Biotropica 19: 373-375.

Jones CB. 1997. Rarity in primates: implications for conservation. Mastozool Neotrop 4: 35-47.

Jones CB. 2005a. Behavioral flexibility in primates: causes and consequences. Springer, New York.

Jones CB. 2005b. Phenotype as developmental bridge: whither nature and nurture. Am J Psychol 118: 141-158.

Jones CB, Jost CA. 2007. Update on studies of Belizean primates, emphasizing patterns of species distribution. Lab Prim News 46: 1-5.

Jones CB, Young J, 2004. Hunting restraint by Creoles at the Community Baboon Sanctuary, Belize: a preliminary survey. J Appl Anim Welf Sci 7: 127-141.

Lee RB. 1976). !Kung spatial organization: an ecological and historical perspective. In: Lee RB, DeVore I, editors. Kalahari hunter-gatherers: studies of the !Kung San and their neighbors. Harvard University Press, Cambridge, MA. p 73-97.

Lewontin RC. 1983. The organism as the subject and object of evolution. Scientia 118: 63-82.

Mahajan N, Martinez MA, Gutierrez NL, Diesendruck G, Banaji MR, Santos LR. 2011. The evolution of inter-group bias: perceptions and attitudes in Rhesus monkeys. J Pers Soc Sci 100: 387-405.

Matsuno T, Fujita K. 2009. A comparative psychophysical approach to visual perception in primates. Primates 50: 121-130.

Millar JS, Zammuto RM. 1983. Life histories of mammals: an analysis of life tables. Ecology 64: 631-635.

Milton K. 1980. The foraging strategy of howler monkeys: a study in primate economics. Columbia University Press, New York.

Nagasaka Y, Chao ZC, Hasegawa N, Notoya T, Fujii N. 2013. Spontaneous synchronization of arm motion between Japanese macaques. Sci Rep 3 doi: 10.1038/srep10051

Pigliucci M, 2010. Phenotypic plasticity. In: Pigliucci M, Müller GB, editors. Evolution: the extended synthesis. The MIT Press, Cambridge, MA. p 355-378.

Pimm SL, Gittleman JL. 1992. Biological diversity: where is it? Science 255: 940-945.

Pollick AS, DeWaal FBM. 2007. Ape gestures and language evolution. Proc Natl Acad Sci USA 104: 8184-8189.

Rundle HD, Boughman JW. 2012. Behavioral ecology and speciation. In: Westneat DF, Fox CW, editors. Evolutionary behavioral ecology. Oxford University Press, Oxford, UK. p 471-487.

Sareni B, Krähenbühl L. 1998. Fitness sharing and niching methods revisited. IEEE Trans Evol Comput 2: 97-106.

Scherbaum C, Estrada A. 2013. Selectivity in feeding preferences and ranging patterns in spider monkeys, Ateles geoffroyi yucatanensis, of northeastern Yucatan Peninsula, Mexico. Curr Zool 59: 125-134.

Servedio MR, Kopp M. 2012. Sexual selection and magic traits in speciation with geneflow. Curr Zool 58: 510-516.

Sporns O. 2011. Networks of the brain. MIT Press, Cambridge, MA.

Tanaka J. 1976. Subsistence ecology of Central Kalahari San. In: Lee RB, DeVore I, editors. Kalahari hunter-gatherers. Harvard University Press, Cambridge, UK. p 98-119.

Terborgh J, Winter B, 1980. Some causes of extinction. In: Soulé ME, Wilcox BA, editors. Conservation biology: an evolutionary-ecological perspective. Sinauer, Sunderland, MA. p 119-134.

West SA, Pen I, Griffin AS (2002) Cooperation and competition between relatives. Science 296: 72-75

West SA, Gardner A, Shuker DM, Reynolds T, Burton-Chellew M, Sykes EM, Guinee MA, Griffin AS. 2006. Cooperation and the scale of competition in humans. Curr Biol 16: 1103-1106.

Wheatley BP. 1982. Energetics of foraging in M. fascicularis and Pongo pygmaeus and a selective advantage of large body size in the orang’utan. Primates 23: 348-363.

Wilkie DS, Godoy RA. 2001. Income and price elasticities of bushmeat demand in lowland Amerindian societies. Cons Biol 15: 761-769.

Wilson DE, Reeder DM, eds, 2005. Mammal species of the world (2 volumes). Smithsonian Institution Press, Washington, DC.

Wolf JB, Brodie III ED, Moore AJ. 1999. Interacting phenotypes and the evolutionary process II. Selection resulting from social interactions. Am Nat 153: 254-266.

Xing J, Watkin WS, Witherspoon DJ, Zhang Y, Guthery SL, Mara R, Mowry BJ, Bulayeva K, Weiss RB, Jorde LB. 2009. Fine-scaled human genetic structure revealed by SNP microarrays. Genome Res 19: 815-825.

Yellin JE. 1976. Settlement patterns of the !Kung: an archaeological perspective. In: Lee RB, DeVore I, editors. Kalahari hunter-gatherers. Harvard University Press, Cambridge, MA. p 47-72.

Yun K, Watanabe K, Shimojo S. 2012. Interpersonal body and neural synchronization as a marker of implicit social interaction. Sci Rep doi.10.1038/srep00959

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

My years as a Behavioral Ecologist (1973----->) (Clara B. Jones)

My years as a Behavioral Ecologist (1973----->) [Behavioral Ecology: study of how Dispersion [Distribution & Abundance] of organisms "maps" onto Dispersion of limiting resources in Time & Space--the [John Hurreel] Crook-ian Model, John Hurrel Crook

Behaviour. Supplement No. 10, The Evolution of Social Organisation and Visual Communication in the Weaver Birds (Ploceine) (1964)

Conceptual Framework: FIRST PRINCIPLES OF BEHAVIORAL ECOLOGY:: E[nergy]: Acquisition->Consumption->Allocation====> Worker &/or Reproductive &/or Dependent...(Males, T[ime] Minimizers; Females, E[nergy] Maximizers)

#womeninscience #womeninbehavioralecology

1. The Science culture that I experienced 45 years ago might be called a "Brigade System" (or, perhaps, rather, an apprentice system)--hard-nosed, mostly male, rigid, rigorous--with obsessive attention to detail and no hand-holding. It was understood that many wouldn't survive the regime--we took this for granted--bad experiences were just part of the obstacle course. This system motivated me to be the best scientist I could be--emulating the work and standards of the premier Behavioral Ecologists of that time [especially, the early work of, John Hurrell Crook (birds, primates), Stephen C. Emlen (birds, humans, one of my professors), Jack Bradbury (bats, one of my professors), Ruth Buskirk (spiders, baboons, one of my professors), & Sandy Vehrencamp (birds, bats, a fellow graduate student)--the Behaviorist, M.E.P. Seligman, and the Social Biologist, Mary Jane West-Eberhard, were also critical to my early career].

2. Having said the above, we had mutual respect among all deserving parties, whatever their rank, and had a lot of fun.

3. A necessary and sufficient component of my own motivation was falling in love with fieldwork in 1973 [I was 30--a "late-bloomer"] after which nothing ever competed with my work/career. Another factor important to my progress was relieving myself of most caretaking responsibilities [in 1979].

4. At one point during my graduate training, I asked my undergraduate advisor, Harry Levin (linguistics), what was necessary to be successful as a scientist. He replied, "Learn to cope with humiliation." Afterwards, it occurred to me that I would need to have a "thick skin." It was, also, clear that I would have to make it work for me, by myself, on my own, but on others' terms--the terms set by those at the top of my fields--Behavioral Ecology, Social Biology, Ethology, and, to a lesser degree, Behaviorism. Serious Scientists would let me know--straightforwardly--when they thought I was not "measuring up." I could leave Science, or, I would need to find a way to "measure up." Combined with the ability to "hear" critical and negative feedback, I, eventually, enjoyed the challenges inherent to intense competition.

At another point--after  completing my Ph.D.--my major advisor, Ethologist (birds--Agapornis) William C. Dilger, told me, "You have done less with more than any other graduate student I've had." This feedback shook me; however, the lesson was clear--it is very difficult, indeed, to earn the right to be taken seriously by a serious Scientist. Indeed, in graduate school, it was standard not to call ones-self "Scientist" until a recognized scientist had labeled you "Scientist." Dilger's comment reinforced that I needed to take myself and my aspirations seriously if I, and, more importantly, my work, were to earn the opportunity to be taken seriously. A consequence of this experience has been that I consider it a female's responsibility--to herself, more, even, than to others-- to find a way to develop her potential to the fullest, relative to the highest standards of her field[s].

These words of wisdom & feedback from two highly-regarded scientists were instrumental in motivating me to be my best while understanding realities of the academic/professional/research landscape. The path is difficult, and there are no guarantees.

5. When I found my path in Behavioral Ecology to be difficult, I reminded myself that, if I didn't find a way to make it work, there was always another female breathing down my neck who was not defeated by trying or who was making it work.

6. It is central to who I am as a Scientist to view myself having a role comparable to a Judge of the Court. My colleagues and I, if taken seriously, get to "weigh in" on difficult decisions, using critical thinking, data, other components of scientific methods, and expertise.

7. It is important to me that I never used a sex/gender card, a race card, a class card, or a disability card.

8. I consider myself a feminist in the molds of Simone de Beauvoir and, especially, Francoise Giroud whose autobiography, I Give You My Word, which I read early in graduate school, changed my life forever. Everything changed after I read that book--combined with my first field season in 1973.

9. I free myself; others do not free me. All know the way.

10. So-called "imposter syndrome" represented important, valid feedback to me that something needed to be corrected. I did not deny my gut and brain. I figured it out. I realized, there was/is always another female prepared to take my place. That other female would have dealt with her sense of imposition, if she had such, and would have self-corrected.

11. As a woman of color (WOC) in Science who conducted fieldwork, I ran away, rapidly, from anyone who wanted to treat me with kid gloves or treat me differently than the non-marginalized person. This did not always work to my advantage or prove to be the shortest route to authenticity*, but it preserved my self-respect.

12. I think I have few, if any, complaints as a WOC in Science because: [1] I almost always see the glass as half-full rather than half-empty; [2] I take almost nothing personally--what another person does or says reflects on them, not me; [3] I have an uncanny ability to focus without distraction; [4] I try, and, mostly, succeed, at not multitasking, [5] I have an uncanny ability to compartmentalize; [6] I chose, and, continue to choose, very, very carefully, whose critical feedback I weight heavily; and, [7] I, simply, kept my nose to the grindstone [though, primarily for health reasons, I started & re-started quite a few times]. Related to the foregoing, I may be "tone deaf" about what the outspoken and activist young females want to achieve as scientists [I am thinking, particularly, of fieldworkers]. It has taken me a long time to "get" the notion that what I wanted out of a career is not, necessarily, what other females wanted/want. Decisions, choices were straightforward for me. I, simply, chose whatever option[s] would get me closer to my goal which was to be the best scientist I could be, given my talents & given the fact that I did not have higher-order quantitative skills. This is a very simple decision-rule. I, actually, think that many women in Science use this strategy.

13. Just as a hunch, I would suggest that a critical factor in determining a female's success as a scientist is not so much whether she marries or has children but whether she assumes caretaking responsibilities. Whatever the case, I think these factors deserve further study. I would, especially, like to see intense investigation of what traits characterize those women who achieve high rank as scientists [as usual, I am, particularly, thinking of women who conduct fieldwork in the biological sciences]. For example, are there, beyond chance occurrences, married women with or without children who have careers like, say, Mary Willson's, or, perhaps, most notably, Louise Emmons'? If so, lets highlight these women. If not, why not? These are all issues that can be addressed empirically, including, consideration & tests of alternative hypotheses. If only by chance alone, sexism cannot account for all of the differences that we see between male scientists and female scientists in the same discipline. What are all of the factors that are at play?

14. Probably the only whining I'll permit myself: ... throughout my whole career, with a few exceptions [Mary Jane West-Eberhard, Ruth Buskirk, Sandy Vehrencamp, & Mary Willson being notable exceptions], female scientists haven't given me "the time of day"... virtually, all of the scientists who have provided constructive criticism, encouragement, & who have shared ideas, have been men... additionally, with a couple of exceptions, all of the researchers who have treated me dismissively, to my face or via other sorts of communication, have been females-- all of them Primatologists-- a fact in no manner related to my low estimation of Primatology ["Biological Anthropology"] as a field...

15. Now, getting back to Science: Every material outcome has a mathematical proof.

*The hardest thing for anyone in Science is to earn the right to be taken seriously.

Clara B. Jones
929 Bonifant Street
Apt. 512
Silver Spring, MD 20910, USA
Cell: (828) 279-4429
E-mail: foucault03@gmail.com; mapcbj@gmail.com

Conducting Fieldwork Remotely (Clara B. Jones)

Conducting Field Work Remotely

I am presenting this blogpost hoping that some researchers might find it useful--especially, females who want to remain fieldworkers while assuming caretaking responsibilities. At one point [~2006], I was unable to travel far from my home base but wanted to conduct a project in Brazil. I collaborated with a Brazilian colleague--a [then] young professor, Julio Cesar Bicca-Marques, who suspected hybridization between two species of howler monkeys at one of his study sites. We brainstormed, deciding that I would write a proposal to obtain funding. My colleague commented on the first draft, I incorporated his suggestions and revised the proposal, and we were awarded funding by two conservation organizations. My colleague conducted the research with two of his graduate students, drew some amazing maps, took some amazing photographs, & collected the data. We collaborated on data analysis. I wrote the first draft of the resulting paper after which my colleague revised and submitted the final version. Our paper was accepted for publication, and we were both satisfied with the order of authorship and assignment of corresponding author.* This procedure, or, some variant of it, might work for others with limited mobility. I do not intend to suggest that one can build a career on these sorts of accommodations; however, intermittently, or, for brief periods of time, such arrangements, or, some variant of same, might work very well.

Bicca-Maarques JC, et al. (2008) Survey of Alouatta caraya, the black-and-gold howler monkey, and Alouatta guariba clamitans, the brown howler monkey, in a contact zone, State of Rio Grande do Sul, Brazil: evidence for hybridization. Primates 49(4): 246-252.

https://link.springer.com/article/10.1007/s10329-008-0091-4

*At the time, I justified being final & corresponding author on the basis of my having designed a highly original survey method and on the basis of having written a successful proposal. However, in retrospect, I think a strong case could be made that it would have been appropriate for Bicca-Marques to have been assigned those roles. As an aside, he went on to conduct additional work on this topic and published the research that I did not participate in.