The Challenge of Comparisons in Primatology

I have been studying the same group of monkeys, known as northern muriquis, in a small forest in southeastern Brazil for nearly 28 years. When I began my research they were called Brachyteles arachnoides. Subsequently, and within the lifetimes of many of the individuals in my original study group, they were reclassified as a new species, B. hypoxanthus, to distinguish them (as northern muriquis) from the southern muriqui, which has retained the original Latin name. I sometimes joke about how I’ve been studying these monkeys for so long that they have had time to speciate. But the reality is that there are good reasons for their reclassification, conservation being the most serious one. Like nearly half of the more than 630 species and subspecies of nonhuman primatesi recognized today, both the northern and the southern muriqui are threatened with extinction. The situation for the northern muriqui is among the most desperate because there are so few of them and so little of their native Atlantic forest habitat is left. By elevating the northern muriqui to the status of a separate species, conservation efforts can rally more effectively for both species at once.

My point here is not to defend or to doubt whether the morphological, genetic, and behavioral differences between the northern and southern muriqui populations are sufficient to justify the decision to assign them to different species. Although a species is supposed to be a biologically and evolutionarily meaningful unit of classification, in the real world different patterns of variation can accumulate in isolated populations to the point that the populations may seem like different species when, in fact, they are still one. The converse situation can also occur if the ranges of closely related populations overlap so that their members can occasionally interbreed. However, the opportunity for genetic exchange is no longer an option for northern and southern muriquis in the wild because deforestation and habitat fragmentation have severed all contact between them. This is also the case for many other primate species, whose ranges have been similarly disrupted by anthropogenic activities and whose remaining populations are now isolated from one another. Many of these same primate species have also recently undergone the same type of taxonomic revisions as the muriqui, raising concerns that so much “taxonomic inflation” could run the risk of backfiring if it ends up confounding our understanding of biodiversity instead of helping to protect it (e.g., Isaac et al. 2004; Tattersall 2007).

To be fair, advances in molecular genetics have brought powerful new analytical tools to the comparative morphological analyses upon which traditional taxonomic classifications have been based. These more sensitive methods should detect more variation than might have previously been perceived. But even results from molecular analyses require interpretation, and this growing tendency to recognize the smallest measurable units of diversity by naming them can be attributed to the growing influence of conservation in primatology.

This influence has intensified during recent decades, as the long-term outlook for many of the world’s most endangered primates has become increasingly grim. It has also extended beyond taxonomy, to converge with primate behavioral ecology, in two significant respects. The first involves the conservationists’ commitment to cataloguing biodiversity, which has helped stimulate the expansion of primate field research into increasingly remote regions. New behavioral and ecological studies on previously neglected primates are now underway, and these studies, together with long-term data on an increasing number of species, are providing new insights into the diversity of primate behavior patterns. They are also challenging past comparative perspectives about the extent to which behavior patterns, such as social and mating systems, vary within taxa and within the same populations over time. This heightened appreciation for behavioral variation below the species level has generated renewed interest in the high levels of phenotypic plasticity that primates display, and represents the second way in which the influence of conservation is being felt in the field.

Primatology’s distinction as an anthropological discipline resides with the comparative evolutionary perspectives that the study of other primates can provide about humans. Consequently, the ways in which we classify and compare the behavior patterns of other primates directly affects how we compare their behavior with our own. Yet, the ways in which we construct these comparisons are far from transparent, as is evident from the recent round of disagreement over whether chimpanzees are the most appropriate referential models for the behavior of the new early hominidii, Ardipithecus (Lovejoy 2009; Whiten et al. 2009). This particular debate pivots on one’s perceptions of the relative importance of phylogenetic proximity versus ecological analogy, and although the two can coincide in carefully constructed comparative models (Moore 1996), the fact that there is any debate at all serves to illustrate the complex underlying assumptions involved in primatological comparisons.

Applications of the comparative method of evolutionary biology have been instrumental in identifying evolutionary patterns in primate behavioral adaptations among closely-related species and higher taxonomic units. The strength of this method comes from the phylogenetic controls it employs to distinguish between shared traits that evolved independently versus those that are shared through common descent (Nunn and Barton 2001). Yet, the procedures for constructing these comparisons among species rely on compressing the intraspecific variation in behavioral traits into species-typical modal values or categorical norms. This is problematic for a number of reasons, including the errors introduced by our uneven knowledge of different species, and the misrepresentations that can arise from making simplifying assumptions about the static properties of behavior patterns that are known to fluctuate in response to different local ecological and demographic conditions.

Biases in our comparative knowledge of different primates have resulted from the combination of anthropocentric interests in particular species, and differences in the feasibility and accessibility (due to geography and politics) of establishing field sites and in the visibility of different primates once access to a field site has been gained. The outcome of various combinations of these factors led to learning very little about most species but a lot about some, such as apes, and among them in particular chimpanzees, and semi-terrestrial and relatively abundant monkeys like baboons and macaques. Now, however, comparative data from multiple populations of a diversity of species across the primate order are showing not only that intraspecific variation in behavior patterns co-vary with local ecological and demographic differences, but also that different species may respond to local conditions in different, but nonetheless predictable, ways.

Without these kinds of comparative data, there is no way of knowing whether the behavior patterns observed in a particular group or population truly represent the species, or how past ecological and demographic conditions may have shaped the behavior patterns being observed today. For example, variation in the size, density, and sex ratios of populations will influence the size and composition of primate groups, which in turn affect the number, availability, and identities of potential social and reproductive partners. Fluctuations in these demographic variables can occur rapidly due to stochastic and ecological processes, and because primates are relatively long-lived, individual primates may experience a wide range of social options during the course of their lives. Thus, there is no reason to assume that behavior patterns observed at any particular time in a particular group’s or population’s history reflect the normative, adaptive patterns for a species rather than reflecting stochastic processes or recent historical events (Thierry 2007).

The long-standing reliance on comparisons of species or population behavioral norms also ignores the ways in which the high levels of phenotypic plasticity characteristic of the behavior of many primates are achieved (Chapman and Rothman 2009; Strier 2009). It tends to treat behavior patterns as static properties, despite the evidence that individual primates adjust their behavior in response to local conditions, and through these adjustments, contribute to the construction of their own ecological niches (Fuentes 2010). An individual’s behavioral decisions, such as whether, when, and where to disperse, will affect the social options of other individuals in their own and neighboring groups, as well as determining their own access to close kin and mates and the levels of competition and cooperation they will face (Strier 2008). Considering that all of these social consequences have been shown to affect fitness, one might expect that natural selection would favor individuals with the most expedient responses instead of those whose behavior patterns are fixed (Barrett and Henzi 2005). From this perspective, it would seem that our comparative models could be more informative if they focused on species’ differences in their behavioral flexibility instead of on averaging this flexibility into species-typical traits.

My interest in reconciling the conflict that intraspecific variation poses for interspecific comparisons is directly connected to what I’ve watched the northern muriqui monkeys do. Over the past 28 years, the original study group has grown from 22 to some 107 individuals by the most recent count, and the total muriqui population in this forest has expanded proportionately. Although their grouping patterns have shifted from cohesive to fluid associations, which would minimize the potential for direct feeding competition, there has been no change as of yet in the unusually peaceful, egalitarian social relationships of either males, who are still philopatric, or females, who still typically disperse from their natal groups. It seems obvious now that the population’s size had been unusually depressed when the study began, and that the growth it has been experiencing cannot go on forever. But even after all of these years of intensive study, we still don’t know what the typical group size for this species is, or whether to consider cohesion or fission-fusion the species’ normative grouping pattern.

There are now some comparative data from some of the 12 other northern muriqui populations that persist. But all of them have been affected in one way or another by pressures from hunting, habitat alterations, or both — and are therefore living under different conditions now than they were during their evolutionary past. The same problem plagues nearly all of the world’s primates to at least some degree, and this is yet another reason to be cautious about comparisons that assume all behaviors are adaptive (Schlaepfer et al. 2002).

In an ideal world, we would know enough about a diverse sample of primates to be able to (i) describe the range of variation in the behavior patterns exhibited by each species, and (ii) identify the ecological and demographic conditions that predict the expression of one behavior pattern instead of another. With this information, we could then (iii) derive a more dynamic version of a species’ normative behavior patterns. In this manner, beginning with population-level variation and working up to the species level, we essentially turn the way in which behavioral comparisons have been made in primatology on its head.

i Hereafter, I use primates and primatology to refer to nonhuman primates.
ii I follow Lovejoy (2009) here, but see Marks (2005) for a discussion of hominids versus hominins and other taxonomic issues.

References Cited

  • Barrett L, and Henzi P. 2005. The social nature of primate cognition. Proc Biol Sci 272:1865-1875.
  • Chapman CA, and Rothman JM. 2009. Within-species differences in primate social structure: evolution of plasticity and phylogenetic constraints. Primates 50:12-22.
  • Fuentes A. In press. Social Systems and Socioecology-Understanding the Evolution of Primate Behavior. In: Campbell CJ, Fuentes AF, MacKinnon KC, Panger M, Bearder S, and Stumpf R, editors. Primates in Perspectives, 2nd edition New York: Oxford University Press.
  • Isaac NJ, Mallet J, and Mace GM. 2004. Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol Evol 19:464-469.
  • Lovejoy CO. 2009. Reexamining human origins in light of Ardipithecus ramidus. Science 326:74e71-78.
  • Marks J. 2005. Phylogenetic trees and evolutionary forests. Evol Anthropol 14:49-53.
  • Moore J. 1996. Savanna chimpanzees, referential models and the last common ancestor. In: McGrew WC, Marchant LF, and Nishida T, editors. Great Ape Societies. Cambridge: Cambridge Univ Press. p 275-292.
  • Nunn CL, and Barton RA. 2001. Comparative methods for studying primate adaptation and allometry. Evol Anthropol 10:81-98.
  • Schlaepfer MA, Runge MC, and Sherman PW. 2002. Ecological and evolutionary traps. Trends in Ecology and Evolution 17:474-480.
  • Strier KB. 2008. The effects of kin on primate life histories. Ann Rev Anthropol 37:21-36.
  • Strier KB. 2009. Seeing the forest through the seeds: Mechanisms of primate behavioral diversity from individuals to populations and beyond. Current Anthropol 50:213-228.
  • Tattersall I. 2007. Madagascar’s lemurs: cryptic diversity or taxonomic inflation? Evol Anthropol 16:12-23.
  • Thierry B. 2008. Primate socioecology, the lost dream of ecological determinism. Evol Anthropol 17:93-96.
  • Whiten A, McGrew WC, Aiello LC, Boesch C, Boyd R, Byrne RW, Dunbar RI, Matsuzawa T, Silk JB, Tomasello, M, van Schaik, CP, Wrangham, R. 2010. Studying extant species to model our past. Science 327:410; author reply 410-411.

9 comments to The Challenge of Comparisons in Primatology

  • In her always-cogent manner, Karen Strier points to the wide significance of one of primatology’s most robust findings: Individuals within primate populations (as well as populations within primate species) express a great deal of behavioral plasticity.

    In my work on gestural communication of African apes, and in reading my colleagues’ work on field and captive study of ape behavior, I’m struck by how this behavioral plasticity embraces emotional responses as well as cognitive ones (though I realize this dichotomy is itself suspect). The “anecdotes are not data” school of primatology may still be kicking around, mistakenly assuming that study of individuals need be anecdotal, but much work (by e.g., M. Nakamura and B. Smuts as well as A. Fuentes) now shows that an individualistic focus on emotion and cognition may be cutting-edge and exciting as well as scientifically rigorous.

    To stick with the great apes for a moment, just because I know them best, here’s how I see it: Every great ape is a self-aware, thinking and feeling self. There is no generalized “ape nature” or “chimpanzee nature”, or even “Gombe chimpanzee” or “Tai chimpanzee nature”. The intersection of developmental dynamics, cultural tradition and individual life history produces the variable responses to local conditions of which Strier writes.

    Might this behavioral plasticity be phylogenetically conserved, so that it was present in the common ancestor of great apes and humans? Might anthropologists use this line of thinking to challenge some of the more reductive models of human behavior and its evolution coming from certain avenues within evolutionary psychology? The debate Strier mentions about chimpanzees, Ardipithecus, and referential models is surely engaging, but we can look more broadly. Can the primatological focus on behavioral plasticity at the individual as well as the populational level tell us something that matters conceptually about the evolution of human behavior?

    I think the answer is yes. If we have learned anything from our colleagues who have interrogated an earlier wave of reductive claims, e.g., from Keller’s Century of the Gene or Marks’s What It Means to be 98% Chimpanzee, we must look hard at models that give pride of place to simplistic biology in understanding changes in hominid and human populations. When genes, or oxytocin, or fixed brain modules are championed “”over and above the power of contingent developmental and social processes**, might the study of apes offer a cautionary tale? Apes may focus our gaze in ways that help us think in comparative contexts more clearly.

  • As a sociologist who is interested in how primatological knowledge is constructed, and in the mutual implications of parallel epistemological debates in primatology and in the social sciences, I find Karen Strier’s article extremely interesting, and its argument a bold and exciting one.

    It seems to me that the fundamental problems being raised by the extent of sub-species variation and adaptation for the underlying assumption of species normativity that underpins the logic of inter-species comparison is an essentially philosophical one. It is also one which has played a key role in the development of the social sciences, perhaps unsuprisingly given their focus on humans, those most variable and adaptive of social animals. It seems ultimately to raise the fundamental question as to what is a norm, and what sort of ontological architecture do we unwittingly invoke when we employ a comparative logic based on the assumption of such units as might render norms meaningful.

    Perhaps the normative itself needs to be understood differently, not as bound to species units assumed to be pinned to some evolutionarily rooted biological essence, away from which they may diverge only so far, but instead as something always relatively contingent, transient, and determined by historical, demographic and ecological events and processes.

    Taking this a step further, describing the variation within a species necessarily assumes a norm from which there is variation, but what if variation is the norm? If the norm is relativised through and through, then the logic of comparison would have to become less nomothetic and more ideographic. In other words, it would have to move towards treating all groups and even individuals as in principle unique, rather than viewing them as merely a particular individual expression of a biological collectivity which is given explanatory primacy.

    I thoroughly applaud the working through of some of the implications of acknowledging that ‘species’ is itself a contested category, not something objectively and indisputably given. I agree that beginning foundationally from homogenised species-units rather than observed behaviour for the purposes of comparison therefore seems deeply problematic. Again, the necessary reponse seems to me to be a move away from a deductive rationalism and towards a more inductive empiricism. I am therefore very enthusiastic about the suggestion that primatological comparisons should begin from the assumption of intra-species variation, begin from difference, to use the sociological parlance, and then look for recurrent patterns or structures, rather than beginning from a buried assumption of intra-species normativity or homogeneity and then looking for variation.

    This seems to follow logically from the recognition that these creatures are ‘cultural’, which surely suggests that what needs to be explained is not variation – this is to be expected, but the persistence of certain behavioural patterns – how do these get reproduced over time?

    I also note with particular interest that the impact of human incursion upon many primate species, in dividing geographic groups from each other for example, has impacted profoundly on their patterns of behavioural adaptation, as well as (through the influence of conservation and ‘taxonomic inflation’) our classification of these groups, even to the extent of influencing what is deemed a distinct ‘species’. From my own perspective this underlines the extent to which both the human (primate) ‘subjects’ of taxonomic classification and the nonhuman primate ‘objects’ of classification are all bound up in the same historical-political-ecological nexus. All knowledge production inevitably occurs ‘inside’ this matrix, rendering the search for an objective species norm somewhat illusory. Species are fluid, not only phylogenetically, but because their identification is always the product of political-social-historical contingencies.

    In light of this, the identification of species-normative behaviours for the purposes of setting up evolutionary models seems thoroughly misconceived, especially given the plasticity of both classificatory practices and actual behavioural variation. It seems plausible that there is no evolutionary norm, no point at which there were no contingent impacts upon behavioural patterns, no externalities. Even prior to the impact of humans, there would have been ecological, climatic, demographic and inter-species relational contingencies. In other words, it seems that if we are to follow through the implications of acknowledging that these species are ‘social’ beings, then we must also acknowledge that they are historical beings, with no behavioural ‘essence’ outside of their historical development. If they have an essence, the factors which ‘distort’ it have always already been there.

  • Jon Marks

    Of the many interesting anthropological issues about primates raised in Strier’s essay, one in particular jumps out at me. We perennially hear from a certain corner of biology that anthropology should not consider humans as different from other animals, but should consider humans instead as “nothing but” another species of primates, and look to primate biology to guide us in an objective, scientific study of humans. An earlier generation of evolutionary theorists, like Julian Huxley and G. G. Simpson, derided such theorizing as “nothing-butism”.

    In this context, the recent formal division of Brachyteles arachnoides, and the consequent transformation of Strier’s monkeys into B. hypoxanthus, affords a salutary lesson. This taxonomic judgment is instrumental, to enlist science in the cause of conserving the animals, and as a result of such interests, the number of official primate species has more than doubled over the last two decades. Such taxonomic inflation, strategically over-tabulating taxonomic diversity in the interests of the animals themselves, is well-known and is by no means restricted to the primates, as Strier notes. Nevertheless, the principal physical feature now distinguishing the two zoological species of Brachyteles from one another is simply their complexion.

    This is consequently a very instructive situation, in which the scholarly study of humans should most definitely not be guided by primate biology.

  • Karen B. Strier

    I agree completely with Barbara King’s well-reasoned point about considering the emotional as well as cognitive plasticity of individuals, and there is no reason to think that this plasticity is not a phylogenetically conservative trait from the common ancestor of apes and humans. But I would go one step further and suggest that such levels of behavioral plasticity are not restricted to ape-human ancestors, or even to primates. Instead, I suggest that behavioral plasticity is more likely than not to characterize all long-lived, social beings, and particularly those with slow life histories during which long periods of offspring dependency and over-lapping generations provide extensive opportunities for learning.

    This would also be consistent with Richie Nimmo’s proposal that behavioral variation is the normative pattern for many, if not all, primates. But, I would not be prepared to dismiss the power of evolution in shaping the patterns in this variation across different species and populations and depending on the particular behaviors in question. Pursuing new analytical methods for characterizing this variation would require greater integration across units of study, from individuals to groups and populations, without abandoning an evolutionary approach to understanding behavior.

  • Barbara

    Yes, Karen, I definitely agree that plasticity in behavior goes beyond apes and beyond primates. I should have made my tossed-off “just because I know apes best” more clear in this regard! As we learn about the behavior of a variety of mammals and birds (and perhaps other taxa) the more compelling becomes an argument for widespread behavioral plasticity. On the other hand, I’m also interested in ways to figure out how to make comparisons about degrees of such plasticity across taxa… as you say, a challenge for the future.

  • Jim Moore

    When I entered graduate school, we knew that Japanese and rhesus macaques were (biologically) characterized by “youngest ascendancy” in which daughters came to rank just below their mothers in reverse age order, and olive baboon society was organized around aggressive male competition and social dominance. And we had no idea what to make of Hanuman langurs, which lived in peaceful multimale groups at some sites and at others, infanticidal males ruled single-male harems.

    We now have good reason to believe that macaque youngest ascendancy and baboon dominance are not inherent properties of the species, but reflect predictable results of simple behaviors played out in certain demographic contexts. The puzzling dichotomous variation in langur social organization appears driven by the intersection of individual behavioral tactics with population density. There are species norms, but at least some elements of them lie in the interaction of individuals with their environment, not exclusively “inside” the individuals. At the same time, species-typical “natures” do exist (c.f. Rosenblum’s macaque comparisons in the 1960s, and more recently Clarke and Boinski 1995 — Am. J. Primatol. 37:103). Strier challenges us to work out which is which, and to understand the mechanisms underlying variation and adaptation at both intraspecific and interspecific levels.

    Strier (and King) point to an important sea-change in how we approach the study of socioecology. They (and I) advocate shifting from an emphasis on discrete categorization of taxa and investigation of differences between categories to a focus on continuous variation and the mechanisms responsible (both outside animals, like demography, and inside them, like the emotion/cognition which makes up temperament [aka behavioral syndromes]). The field could not have started this way; the categories we’ve constructed give us a way to frame variation that otherwise would have appeared vast and confusing and purely historical (c.f. Nimmo). But time to move on.

    I am persuaded by Koenig and Borries’ response to Thierry that it is too soon to abandon “the socioecological model”; it has not yet received the “true testing [that] would require comparing ecological conditions and all the predicted aspects for MULTIPLE populations and MULTIPLE species.” (Evol. Anthropol. 18: 166, 2009; original emphasis). They appear to be recognizing the same issue as Strier: that understanding variation below the species level is critical to interpreting both the patterns we see across species, and more importantly the mechanisms by which those patterns arise. However, while that testing goes on we can – and should – work towards the ideal world of Strier’s last paragraph. One promising tool for this is social networks analysis, which may offer useful ways to quantify relationships and thus take comparative studies beyond categorical approaches (see e.g. Wey et al., Anim. Behav. 75: 333, 2008).

    One quibble: in a response, Strier extends her ideas to “all long-lived, social beings”; this may be too restrictive. Interest in intraspecific variation has been fueled by e.g. behavioral syndromes in guppies, and even squid may show complex variation responding to the intersection of temperament, demography and habitat (Sinn et al., Beh. Ecol. Sociobiol. 64: 693, 2010).

  • Agustin Fuentes

    Karen Strier’s concluding comment “beginning with population-level variation and working up to the species level, we essentially turn the way in which behavioral comparisons have been made in primatology on its head” is an important call for those interested in the comparative approach to understanding human and primate behavior. Strier points out that many of the datasets currently used in the construction of comparative models are relatively depauperate in regards to group and population level variation. This results in a static model of “adapted” or “species typical” behavior being used in the construction of hypotheses and models for primate and human evolution….which has caused, and will continue to cause, serious errors in conclusions about humans and other primates. For example, if we did accept the chimpanzee as a relatively good comparative model for humans (this is debatable as already noted in the thread of comments here) we then have to decide which populations and patterns are the “normative” ones to use for the comparison. This leads to an approach that prioritizes the search for somewhat static universal traits in species, which can result in, sometimes, myopic models about behavioral evolution.

    As Strier and many of the participants in this discussion have noted, holding a concept that variation at multiple levels is the norm can be a powerful tool in sincere attempts to utilize the comparative method. It is also worth including the possibility that phenotypic plasticity and niche construction play core roles as processes in shaping behavior and the evolution of behavioral systems. Strier’s relatively rare experience of long-term research on a single population of primates enables her move this call along based on actual data and set of relevant experiences, an important contribution indeed.

  • I agree with Fuentes about the potential importance of plasticity and niche construction (conceptually allied with the Baldwin effect). I have to take issue though with the notion that using chimpanzees as models for human evolution requires a decision about “the normative chimpanzee” and then canalizes a search for static universals. I THINK that Agustin and I actually agree about the essentials; my message is simply that his model of a model is not the only model!

    Models (referential or strategic) are methodological tools, as are regression analysis or RIA for fecal hormones. As with all methods, people can make mistakes using models (look at the single species hypothesis, a strategic model based on the competitive exclusion principle which held that robust and gracile australopithecines were male and female of the same species). Nevertheless, sometimes people get things right.

    The most productive form of chimpanzee referential modeling lies precisely in understanding the reasons why populations differ; the focus is on the dynamics of change, not on static comparison. Savanna chimpanzees are important for understanding human evolution not because they are australopithecines (a stunningly obvious point made by some of the Ardipithecus team recently), but because comparing them with forest chimpanzees (multiple populations of each) allows us to identify patterns in how a primate of comparable brain size, body size, etc. adapts to open environments. It is ABOUT process and variation. I discuss this at greater length in my 1996 paper cited by Strier.

    This is not to say that static and/or normative models CAN’T sometimes be informative — but as Fuentes rightly cautions, they must be used with great care or they constrain our thinking, to our cost.

  • Karen B. Strier

    I very much like the careful distinctions that Agustin Fuentes and Jim Moore make regarding the importance of distinguishing between the processes that can lead to intraspecific behavioral variation. Some of this variation is predictable, as Moore notes, such that all populations of a particular species can be expected to respond in similar ways under similar ecological and demographic conditions. Yet, as Fuentes emphasizes, history and stochasticity can also shape these responses. The dual influences of predictability, which reflects evolutionary selection pressures, and stochasticity, which does not, make it much more difficult to compare the behavior patterns of primates than it was when our knowledge was more limited and we could base our conclusions on single studies of particular groups or populations of particular species. The expansion of primatology—and all of the behavioral variation we now know to exist—has stimulated the kind of expanded comparative approaches that have been discussed in this Forum.

    How we ultimately compare other primates with one another has implications for how we characterize biodiversity, and for how we understand our own place, as humans, in nature.