Modelling Primate Behavioral Ecology

Models play an important role in any mature science because they force us to make explicit our assumptions about how a phenomenon works and allow us to explore the way in which different variables influence a complex biological system. I review the principal kinds of models that could be used to study primate behavior and ecology: linear programming models, systems models, optimality models, stochastic dynamic programming models and agent-based simulation models. Although less use has been made of modelling in primatology than in some other areas of behavioral ecology, there is considerable scope for exploiting the predictive and explanatory power of models in the field.     

Can optimality models and an ‘optimality research program’ help us understand some plant–fungal relationships?

In this paper we suggest that the field of fungal ecology may benefit from the use of optimality models in the context of an ‘optimality research program’ (ORP). An ORP is a research program in the sense of modern philosopher of science Lakatos' [1978. The Methodology of Scientific Research Programmes: philosophical papers, vol. 1. Cambridge University Press, Cambridge] seminal work. An optimality research program has a lengthy history and record of success in the field of behavioural ecology, but has been seldom employed in fungal ecology. We discuss the ORP and provide some examples of how optimality models may be useful in fungal ecology. We suggest that such an approach may benefit experimental fungal ecologists by: providing a framework for organizing knowledge; generating hypotheses; helping in the planning of experiments; aiding in the interpretation of results; and directing the next steps of an experimental research program. We illustrate these benefits by sketching out how an ORP might be used to answer some fundamental questions about the interactions between host plants and arbuscular mycorrhizal fungi.     

Is there a role for culture in human behavioral ecology?

Most research in human behavioral ecology has been acultural, which raises the question of how best to incorporate the concept of culture into this approach. A necessary step in this direction is to pare the culture concept down to its ideational elements, excluding behavior and its material products (Durham 1991; Geertz 1973; Keesing 1974). The cultural and reproductive success hypothesis, though empirically successful (Irons 1993), is not a model for all of culture because of widespread discrepancies between behavior and culture to which it does not call attention. Cultural transmission models are also weakened by such discrepancies, but, more importantly, such models are most relevant to phenomena different from those central to human behavioral ecology. A better way to incorporate culture into human behavioral ecology is to see it as the context of human action and as a tool people use in social manipulation. The study of signal systems is a key to an understanding of social manipulation and to the incorporation of culture into human behavioral ecology. Examples of the manipulation of culture for reproductive benefit include Yanomamö kin term manipulation (Chagnon 1988), incest rules (Thornhill 1990, 1991), and the derogation of sexual competitors (Buss and Dedden 1990). The human behavioral ecological study of social manipulation in cultural contexts needs to be expanded. Two phenomena that might shed light on such manipulation are the Rashomon effect and the audience effect.     

Short‐term insurance versus long‐term bet‐hedging strategies as adaptations to variable environments

Understanding how organisms adapt to environmental variation is a key challenge of biology. Central to this are bet‐hedging strategies that maximize geometric mean fitness across generations, either by being conservative or diversifying phenotypes. Theoretical models have identified environmental variation across generations with multiplicative fitness effects as driving the evolution of bet‐hedging. However, behavioral ecology has revealed adaptive responses to additive fitness effects of environmental variation within lifetimes, either through insurance or risk‐sensitive strategies. Here, we explore whether the effects of adaptive insurance interact with the evolution of bet‐hedging by varying the position and skew of both arithmetic and geometric mean fitness functions. We find that insurance causes the optimal phenotype to shift from the peak to down the less steeply decreasing side of the fitness function, and that conservative bet‐hedging produces an additional shift on top of this, which decreases as adaptive phenotypic variation from diversifying bet‐hedging increases. When diversifying bet‐hedging is not an option, environmental canalization to reduce phenotypic variation is almost always favored, except where the tails of the fitness function are steeply convex and produce a novel risk‐sensitive increase in phenotypic variance akin to diversifying bet‐hedging. Importantly, using skewed fitness functions, we provide the first model that explicitly addresses how conservative and diversifying bet‐hedging strategies might coexist.     

War and peace: social interactions in infections

One of the most striking facts about parasites and microbial pathogens that has emerged in the fields of social evolution and disease ecology in the past few decades is that these simple organisms have complex social lives, indulging in a variety of cooperative, communicative and coordinated behaviours. These organisms have provided elegant experimental tests of the importance of relatedness, kin discrimination, cooperation and competition, in driving the evolution of social strategies. Here, we briefly review the social behaviours of parasites and microbial pathogens, including their contributions to virulence, and outline how inclusive fitness theory has helped to explain their evolution. We then take a mechanistically inspired ‘bottom-up’ approach, discussing how key aspects of the ways in which parasites and pathogens exploit hosts, namely public goods, mobile elements, phenotypic plasticity, spatial structure and multi-species interactions, contribute to the emergent properties of virulence and transmission. We argue that unravelling the complexities of within-host ecology is interesting in its own right, and also needs to be better incorporated into theoretical evolution studies if social behaviours are to be understood and used to control the spread and severity of infectious diseases.     

Phenotypic Resistance and the Dynamics of Bacterial Escape from Phage Control

The canonical view of phage - bacterial interactions in dense, liquid cultures is that the phage will eliminate most of the sensitive cells; genetic resistance will then ascend to restore high bacterial densities. Yet there are various mechanisms by which bacteria may remain sensitive to phages but still attain high densities in their presence – because bacteria enter a transient state of reduced adsorption. Importantly, these mechanisms may be cryptic and inapparent prior to the addition of phage yet result in a rapid rebound of bacterial density after phage are introduced. We describe mathematical models of these processes and suggest how different types of this ‘phenotypic’ resistance may be elucidated. We offer preliminary in vitro studies of a previously characterized E. coli model system and Campylobacter jejuni illustrating apparent phenotypic resistance. As phenotypic resistance may be specific to the receptors used by phages, awareness of its mechanisms may identify ways of improving the choice of phages for therapy. Phenotypic resistance can also explain several enigmas in the ecology of phage-bacterial dynamics. Phenotypic resistance does not preclude the evolution of genetic resistance and may often be an intermediate step to genetic resistance.     

Dowry and Public Policy in Contemporary India

In modern Indian political discourse the custom of dowry is often represented as the cause of serious social problems, including the neglect of daughters, sex-selective abortion, female infanticide, and the harassment, abuse, and murder of brides. Attempts to deal with these problems through legislative prohibition of dowry, however, have resulted in virtually no diminution of either dowry or violence against women. In contrast, radically different interpretations of dowry can be found in the literatures of structural-functionalist anthropology, economics, and human behavioral ecology which muster wide-ranging forms of qualitative and quantitative evidence to support functional models of dowry as a form of inheritance or investment in daughters and/or their children. This paper argues that a functionalist perspective on dowry could lead to improved dowry policy, and that an approach based in human behavioral ecology (HBE) is uniquely suited to this task. After reviewing the relevant literature on dowry in South Asia, I discuss current dowry legislation and its limitations. I then develop a behavioral ecology model of Indian dowry and test it with quantitative and qualitative data. I conclude that if dowry legislation is to achieve broad support or bring about effective social change, it must address and support the positive motivations for and effects of dowry and take a targeted approach to dowry violence, which is not uniformly distributed across regions, castes, or social classes.     

Energetics of feeding,social behavior,and life history in non-human primates

Energy is a variable of key importance to a wide range of research in primate behavioral ecology, life history, and conservation. However, obtaining detailed data on variation in energetic condition, and its biological consequences, has been a considerable challenge. In the past 20 years, tremendous strides have been made towards non-invasive methods for monitoring the physiology of animals in their natural environment. These methods provide detailed, individualized data about energetic condition, as well as energy allocations to growth, reproduction, and somatic health. In doing so, they add much-needed resolution by which to move beyond correlative studies to research programs that can discriminate causes from effects and disaggregate multiple correlated features of the social and physical environment. In this review, I describe the conceptual and methodological approaches for studying primate energetics. I then discuss the core questions about primate feeding ecology, social behavior, and life history that can benefit from physiological studies, highlighting the ways in which recent research has done so. Among these are studies that test, and often refute, common assumptions about how feeding ecology shapes primate biology, and those that reveal proximate associations between energetics and reproductive strategies.     

The chemical defense ecology of marine unicellular plankton: constraints, mechanisms, and impacts

The activities of unicellular microbes dominate the ecology of the marine environment, but the chemical signals that determine behavioral interactions are poorly known. In particular, chemical signals between microbial predators and prey contribute to food selection or avoidance and to defense, factors that probably affect trophic structure and such large-scale features as algal blooms. Using defense as an example, I consider physical constraints on the transmission of chemical information, and strategies and mechanisms that microbes might use to send chemical signals. Chemical signals in a low Re, viscosity-dominated physical environment are transferred by molecular diffusion and laminar advection, and may be perceived at nanomolar levels or lower. Events that occur on small temporal and physical scales in the "near-field" of prey are likely to play a role in cell-cell interactions. On the basis of cost-benefit optimization and the need for rapid activation, I suggest that microbial defense system strategies might be highly dynamic. These strategies include compartmented and activated reactions, utilizing both pulsed release of dissolved signals and contact-activated signals at the cell surface. Bioluminescence and extrusome discharge are two visible manifestations of rapidly activated microbial defenses that may serve as models for other chemical reactions as yet undetected due to the technical problems of measuring transient chemical gradients around single cells. As an example, I detail an algal dimethylsulfoniopropionate (DMSP) cleavage reaction that appears to deter protozoan feeding and explore it as a possible model for a rapidly activated, short-range chemical defense system. Although the exploration of chemical interactions among planktonic microbes is in its infancy, ecological models from macroorganisms provide useful hints of the complexity likely to be found.     

Ecological frames of mind: the role of cognition in behavioral ecology.

Cognitive psychology is the study of how information, from the senses and from memory, is used in the production of behavior. Investigation of the specifics of behavioral adaptation has already led some behavioral ecologists into the domain of animal cognition. I make several arguments for the benefits and the necessity of a sophisticated assessment by ecologists of the cognitive aspects of behavioral adaptation. First, because cognition typically serves to produce adaptive behavior, cognitive structure and function should reflect ecological demands; studies of cognition in ecological contexts are opportunities to understand adaptation. Furthermore, constraints on cognitive properties may help determine how behavior meets the environment. Studies of spatial memory in food-caching corvids exemplify how cognitive aspects of behavior may both reflect and determine specifics of adaptation. Second, many models in behavioral ecology assume certain cognitive abilities, such as timing or counting. Cognitive theory and methodology should be used to determine whether animals possess these abilities. I have provided examples. Third, consideration of cognitive function can lead to original ideas about the details of behavioral adaptation. Without a thorough integration of cognitive psychology with behavioral ecology, our understanding of the relation between behavior and selective pressures will be compromised.     

Evolutionary community ecology of plant-associated arthropods in terrestrial ecosystems

In the 21st century, researchers have attempted a synthesis between community ecology and evolutionary biology. This emerging research area, which aims to synthesize community ecology and evolutionary biology, is evolutionary community ecology. Evolutionary community ecology addresses how intraspecific trait variation in community members is essential for predicting community properties and, how community properties are a key component of the selective forces that determine genetic and phenotypic variation in a community member. In this paper, I review recent findings in evolutionary community ecology in plant-associated arthropods in terrestrial ecosystems. I discuss roles of both genetic variation and phenotypic plasticity as a source of trait variation in plants in shaping plant-associated arthropod communities. Also, I discuss effects of genetic variation in herbivores on plant-associated arthropod communities. Furthermore, I highlight community context evolution in which multiple species interactions and community composition affect trait evolution of a community member. Finally, I argue that future studies should investigate a feedback loop between community and evolutionary dynamics beyond unidirectional studies on effects of evolution on a community or vice versa. This approach will provide major insights into mechanistic principles for making predictions of community ecology.     

Optimality models of phage life history and parallels in disease evolution

Optimality models constitute one of the simplest approaches to understanding phenotypic evolution. Yet they have shortcomings that are not easily evaluated in most organisms. Most importantly, the genetic basis of phenotype evolution is almost never understood, and phenotypic selection experiments are rarely possible. Both limitations can be overcome with bacteriophages. However, phages have such elementary life histories that few phenotypes seem appropriate for optimality approaches. Here we develop optimality models of two phage life history traits, lysis time and host range. The lysis time models show that the optimum is less sensitive to differences in host density than suggested by earlier analytical work. Host range evolution is approached from the perspective of whether the virus should avoid particular hosts, and the results match optimal foraging theory: there is an optimal "diet" in which host types are either strictly included or excluded, depending on their infection qualities. Experimental tests of both models are feasible, and phages provide concrete illustrations of many ways that optimality models can guide understanding and explanation. Phage genetic systems already support the perspective that lysis time and host range can evolve readily and evolve without greatly affecting other traits, one of the main tenets of optimality theory. The models can be extended to more general properties of infection, such as the evolution of virulence and tissue tropism.     

The plaza and the pendulum: two concepts of ecological science

This essay explores two strategies of inquiryin ecological science. Ecologists may regardthe sites they study either as contingentcollections of plants and animals, therelations of which are place-specific andidiosyncratic, or as structured systems andcommunites that are governed by general rules,forces, or principles. Ecologists who take thefirst approach rely on observation, induction,and experiment – a case-study or historicalmethod – to determine the causes of particularevents. Ecologists who take the secondapproach, seeking to explain by inferringevents from general patterns or principles,confront four conceptual obstacles which thisessay describes. Theory in ecology must (1)define and classify the object it studies,e.g., the ecosystem, and thus determine theconditions under which it remains the ``same'system through time and change. Ecologistsmust (2) find ways to reject as well as tocreate mathematical models of the ecosystem,possibly by (3) identifying efficient causes ofecosystem organization or design. Finally,ecologists will (4) show ecological theory canhelp solve environmental problems both inpristine and in human-dominated systems. Afailure to solve – or even to address – theseobstacles suggests that theoretical ecology maybecome a formal science that studies themathematical consequences of assumptionswithout regard to the relation of theseassumptions to the world.     

The evolution of human adiposity and obesity: where did it all go wrong?

Because obesity is associated with diverse chronic diseases, little attention has been directed to the multiple beneficial functions of adipose tissue. Adipose tissue not only provides energy for growth, reproduction and immune function, but also secretes and receives diverse signaling molecules that coordinate energy allocation between these functions in response to ecological conditions. Importantly, many relevant ecological cues act on growth and physique, with adiposity responding as a counterbalancing risk management strategy. The large number of individual alleles associated with adipose tissue illustrates its integration with diverse metabolic pathways. However, phenotypic variation in age, sex, ethnicity and social status is further associated with different strategies for storing and using energy. Adiposity therefore represents a key means of phenotypic flexibility within and across generations, enabling a coherent life-history strategy in the face of ecological stochasticity. The sensitivity of numerous metabolic pathways to ecological cues makes our species vulnerable to manipulative globalized economic forces. The aim of this article is to understand how human adipose tissue biology interacts with modern environmental pressures to generate excess weight gain and obesity. The disease component of obesity might lie not in adipose tissue itself, but in its perturbation by our modern industrialized niche. Efforts to combat obesity could be more effective if they prioritized ‘external’ environmental change rather than attempting to manipulate ‘internal’ biology through pharmaceutical or behavioral means.     

Assessing the impacts of phenotypic plasticity on evolution

In the past decade, there has been a resurgent interest in whether and how phenotypic plasticity might impact evolutionary processes. Of fundamental importance is how the environment influences individual phenotypic development while simultaneously selecting among phenotypic variants in a population. Conceptual and theoretical treatments of the evolutionary implications of plasticity are numerous, as are criticisms of the conclusions. As such, the time is ripe for empirical evidence to catch up with theoretical predictions. To this end, I provide a summary of eight hypotheses at the core of this issue, highlighting various approaches by which they can be tested. My goal is to provide practical guidance to those seeking to understand the complex ways by which phenotypic plasticity can influence evolutionary innovation and diversification.     

The Particular Maternal Effect of Propagule Size, Especially Egg Size: Patterns, Models, Quality of Evidence and Interpretations

SYNOPSIS. Propagule size is perhaps the most widely recognizedand studied maternal effect in ecology, yet its evolution isnot well-understood. The large body of extant optimality theorytreats parental investment solely as an ecological problem,largely from the perspective of progeny. This approach has hadlimited success explaining the ubiquitous variation in propagulesize within and among natural populations at most temporal andspatial scales. This problem aside, an unassailable gap in propagulesize theory is that it pays little heed to the fact that offspringsize is a joint phenotype of two individuals- the offspringand its mother. Hence, the ecology of mothers is decidedly asimportant in shaping the evolution of propagule size phenotypes.There are two reasons to suspect that this gap may account forthe lack of success of optimality theory to explain variationin nature. The first is that optimality models of propagulesize make no allowance for, nor can they explain, widespread,multivariate correlations between maternal characters and clutchparameters, namely the positive phenotypic covariances of maternalage, size, fecundity, and per-propagule investment found inmany organisms. If per-propagule investment is optimized byselection based on the expectation of offspring fitness, thenwhy should that phenotype be a function of maternal age or sizewhen the ecological circumstances of progeny are not changingas a function of maternal age or size? The second gap in currenttheory is that, like all optimization theory, it is patentlynon-genetic in that it is assumed that the phenotypes optimizedare evolutionarily accessible. Recent maternal effects theoryindicates that traits subject to maternal influence behave inunanticipated ways. Specifically, there may be time lags inresponse to selection, and hence, selection away from the optimumphenotype. This paper explores a suite of issues pertainingto the evolution of propagule size from the broader perspectiveof propagule size as a maternal effect (PSME) with a goal ofwidening the lens through which propagule size is viewed byevolutionary ecologists. Two themes are developed. First, Isuggest that, to understand egg size variance and its implicationsfor both maternal and offspring fitness, it is necessary toconsider explicitly the ecological context in which a motheris producing eggs, not just that into which offspring will enter.I argue that some of the variables that have only been incorporatedin pairwise fashion (or not at all) into studies of propagulesize might account for the lack of agreement about how thisimportant life history feature evolves. Further, I suggest thatfailure to consider other sources of selection on maternal phenotypes,driven by a narrow adaptationist view that has historicallybeen taken of PSMEs, has obfuscated many interesting questionssurrounding their coevolution with maternal characters. Thus,the second theme is that it is necessary to consider other explanationsfor why prop-agule size varies apart from those pertaining tooffspring fitness per si. Based on a detailed review of theempirical literature, I conclude that the concept of an optimalpropagule size is not only an insufficient construct to explainthe evolution of propagule size, but that continued relianceon an optimization approach is likely to stifle developmentof more realistic and predictive theory for the evolution ofthis key life history trait. Novel theory should incorporaterealities from physiology, development and genetics and shouldaccommodate the dynamic nature of the selective environmentsin which propagule size evolves, all of which have been shownby empiricists to play a role in determining propagule sizephenotypes. A key feature of this theory should be the explicittreatment of propagule size as a maternal effect.     

Why pest management needs behavioral ecology and vice versa

Behavior manipulation is becoming an accepted tactic in pest management, however, there are many ways in which the approach can be improved. In this review, I explain how and why insect behavioral response to various stimuli can vary dramatically under different conditions and that it is this variable response that must be understood before behavior manipulation becomes widely accepted in pest management programs. I propose that entomologists use concepts from behavioral ecology to manipulate pest behavior in a predictable manner. The key is to study behaviors that maximize fitness in natural environments and then exploit these behaviors in agriculture. I provide examples from a range of behavior manipulation tactics, including use of attracticides, kairomone‐mediated biological control, use of marking pheromones, and push‐pull manipulation.