Decisions,decisions, decisions: choosing a biological science of choice

Behavioral ecologists argue that evolution drives animal behavior to efficiently solve the problems animals face in their environmental niches. The ultimate evolutionary causes of decision making, they contend, can be found in economic analyses of organisms and their environments. Neurobiologists interested in how animals make decisions have, in contrast, focused their efforts on understanding the neurobiological hardware that serves as a more proximal cause of that same behavior. Describing the flow of information within the nervous system without regard to these larger goals has been their focus. Recent work in a number of laboratories has begun to suggest that these two approaches are beginning to fuse. It may soon be possible to view the nervous system as a representational process that solves the mathematically defined economic problems animals face by making efficient decisions. These developments in the neurobiological theory of choice, and the new schema they imply, form the subject of this article.     

Proximate and ultimate causes: how come? and what for?

Proximate and ultimate causes in evolutionary biology have come to conflate two distinctions. The first is a distinction between immediate and historical causes. The second is between explanations of mechanism and adaptive function. Mayr emphasized the first distinction but many evolutionary biologists use proximate and ultimate causes to refer to the second. I recommend that ‘ultimate cause’ be abandoned as ambiguous.     

动物个性研究进展

"个性"是指不同时空条件下动物种群个体间行为的稳定差异。大量的理论和实验性研究表明,个性差异在动物界普遍存在,其是种群多度和分布、物种共存及群落构建的重要驱动因子。介绍了动物个性的概念、分类及衡量指标,将前人测量个性类型的方法加以总结;随后介绍了动物个性的生态学意义,尤其是个性对动物生活史策略、种群分布与多度、群落结构和动态、生态系统功能和过程以及疾病与信息传播等的影响。在此基础上,进一步分析了在人类活动增加等全球变化背景下,动物个性如何调控动物个体行为、种群和群落动态对这些环境变化的响应。阐述了动物个性的形成与维持机制,并对未来的研究方向进行了展望。     

Comparative approaches in evolutionary psychology: molecular neuroscience meets the mind

Evolutionary psychologists often overlook a wealth of information existing between the proximate genotypic level and the ultimate phenotypic level. This commonly ignored level of biological organization is the ongoing activity of neurobiological systems. In this paper, we extend our previous arguments concerning strategic weaknesses of evolutionary psychology by advocating a foundational view that focuses on similarities in brain, behavior, and various basic psychological features across mammalian species. Such an approach offers the potential to link the emerging discipline of evolutionary psychology to its parent scientific disciplines such as biochemistry, physiology, molecular genetics, developmental biology and the neuroscientific analysis of animal behavior. We detail an example of this through our impending work using gene microarray technology to characterize gene expression patterns in rats during aggressive and playful social interactions. Through a focus on functional homologies and the experimental analysis of conserved, subcortical emotional and motivational brain systems, neuroevolutionary psychobiology can reveal ancient features of the human mind that are still shared with other animals. Claims regarding evolved, uniquely human, psychological constructs should be constrained by the rigorous evidentiary standards that are routine in other sciences.     

Dynamic decision-making in uncertain environments II. Allais paradox in human behavior

In both animal and human behavioral repertoires, classical expected utility theory is considered a fundamental element of decision making under conditions of uncertainty. This theory has been widely applied to problems of animal behavior and evolutionary game theory, as well as to human economic behavior. The Allais paradox hinges on the expression of avoidance of bankruptcy by humans, or death by starvation in animals. This paradox reveals that human behavioral patterns are often inconsistent with predictions under the classical expected utility theory as formulated by von Neumann and Morgenstern. None of the many attempts to reformulate utility theory has been entirely successful in resolving this paradox with rigorous logic. We present a simple, but novel approach to the theory of decision making, in which utility is dependent on current wealth, and in which losses are more heavily weighted than gains. Our approach resolves the Allais paradox in a manner that is consistent with how humans formulate decisions under uncertainty. Our results indicate that animals, including humans, are in principle risk-averse. Our restructuring of dynamic utility theory presents a basic optimization scheme for sequential or dynamic decisions in both animals and humans.     

Applying evolutionary anthropology

Evolutionary anthropology provides a powerful theoretical framework for understanding how both current environments and legacies of past selection shape human behavioral diversity. This integrative and pluralistic field, combining ethnographic, demographic, and sociological methods, has provided new insights into the ultimate forces and proximate pathways that guide human adaptation and variation. Here, we present the argument that evolutionary anthropological studies of human behavior also hold great, largely untapped, potential to guide the design, implementation, and evaluation of social and public health policy. Focusing on the key anthropological themes of reproduction, production, and distribution we highlight classic and recent research demonstrating the value of an evolutionary perspective to improving human well‐being. The challenge now comes in transforming relevance into action and, for that, evolutionary behavioral anthropologists will need to forge deeper connections with other applied social scientists and policy‐makers. We are hopeful that these developments are underway and that, with the current tide of enthusiasm for evidence‐based approaches to policy, evolutionary anthropology is well positioned to make a strong contribution.     

Why Go There? Evolution of Mobility and Spatial Cognition in Women and Men

Males in many non-monogamous species have larger ranges than females do, a sex difference that has been well documented for decades and seems to be an aspect of male mating competition. Until recently, parallel data for humans have been mostly anecdotal and qualitative, but this is now changing as human behavioral ecologists turn their attention to matters of individual mobility. Sex differences in spatial cognition were among the first accepted psychological sex differences and, like differences in ranging behavior, are documented for a growing set of species. This special issue is dedicated to exploring the possible adaptive links between these cognitive and ranging traits. Multiple hypotheses, at various levels of analysis, are considered. At the functional (ultimate) level, a mating-competition hypothesis suggests that range expansion may augment mating opportunities, and a fertility-and-parental-care hypothesis suggests that range contraction may facilitate offspring provisioning. At a more mechanistic (proximate) level, differences in cue availability may support or inhibit particular sex-specific navigation strategies, and spatial anxiety may usefully inhibit travel that would not justify its costs. Studies in four different cultures—Twe, Tsimane, Yucatec Maya, and Faroese—as well as an experimental study using virtual reality tools are the venue for testing these hypotheses. Our hope is to stimulate more research on the evolutionary and developmental processes responsible for this suite of linked behavioral and cognitive traits.     

Dual Causality and the Autonomy of Biology

Ernst Mayr’s concept of dual causality in biology with the two forms of causes (proximate and ultimate) continues to provide an essential foundation for the philosophy of biology. They are equivalent to functional (=proximate) and evolutionary (=ultimate) causes with both required for full biological explanations. The natural sciences can be classified into nomological, historical nomological and historical dual causality, the last including only biology. Because evolutionary causality is unique to biology and must be included for all complete biological explanations, biology is autonomous from the physical sciences.     

Semiotic Mechanisms Underlying Niche Construction

The explanatory value of niche construction can be strengthened by firm footing in semiotic theory. Anthropologists have a unique perspective on the integration of such diverse approaches to human action and evolutionary processes. Here, we seek to open a dialogue between anthropology and biosemiotics. The overarching aim of this paper is to demonstrate that niche construction, including the underlying mechanism of reciprocal causation, is a semiotic process relating to biological development (sensu stricto) as well as cognitive development and cultural change. In making this argument we emphasize the semiotic mechanisms underlying the niche concept. We argue that the “niche” in ecology and evolutionary biology can be consistent with the Umwelt of Jakob von Uexkull. Following John Deely we therefore suggest that investigations into the organism—environment interface constituting niche construction should emphasize the semiotic basis of experience. Peircean signs are pervasive and allow for flexible interpretations of phenomena in relation to the perceptual and cognitive capacities of the behaving organism, which is particularly pertinent for understanding the relation of proximate/ultimate selective forces as co-productive (i.e., reciprocal). Additionally, theoretical work by Kinji Imanishi on the evolution of daily life and Gregory Bateson’s relational view of evolution both support the linkage between proximate and ultimate evolutionary processes of causation necessitated by the niche construction perspective. We will then apply this theoretical framework to two specific examples: 1) hominin evolution, including uniquely human cultural behaviors with niche constructive implications; and 2) the multispecies and anthropocentric niche of human-dog coevolution from which complex cognitive capacities and semiotic relationships emerged. The intended outcome of this paper is the establishment of concrete semiotic mechanisms and theory underlying niche constructive behavior which can then be applied to a broad spectrum of organisms to contextualize the reciprocal relation between proximate and ultimate drivers of behavior.     

Caregiving within and beyond the family is associated with lower mortality for the caregiver: A prospective study

Grandparenting has been proposed as an ultimate evolutionary mechanism that has contributed to the increase in human life expectancy (see the grandmother hypothesis). The neural and hormonal system – originally rooted in parenting and thus grandparenting – that is activated in the process of caregiving has been suggested as a potential proximate mechanism that promotes engagement in prosocial behavior towards kin and non-kin alike. Evidence and theory suggest that activating this caregiving system positively impacts health and may reduce the mortality of the helper. Although some studies have found grandparental care to have beneficial effects on grandparents' health outcomes, most studies have focused on the detrimental health consequences of providing custodial care for grandchildren. Little is known about how non-custodial grandparental and other forms of caregiving relate to mortality hazards for the care provider. Using an evolutionary framework, we examined whether caregiving within and beyond the family is related to mortality in older adults. Survival analyses based on data from the Berlin Aging Study revealed that mortality hazards for grandparents who provided non-custodial childcare were 37% lower than for grandparents who did not provide childcare and for non-grandparents. These associations held after controlling for physical health, age, socioeconomic status and various characteristics of the children and grandchildren. Furthermore, the effect of caregiving extended to non-grandparents and to childless older adults who helped beyond their families. Potential ultimate and proximate mechanisms underlying these effects are discussed.     

Studying Food Reward and Motivation in Humans

A key challenge in studying reward processing in humans is to go beyond subjective self-report measures and quantify different aspects of reward such as hedonics, motivation, and goal value in more objective ways. This is particularly relevant for the understanding of overeating and obesity as well as their potential treatments. In this paper are described a set of measures of food-related motivation using handgrip force as a motivational measure. These methods can be used to examine changes in food related motivation with metabolic (satiety) and pharmacological manipulations and can be used to evaluate interventions targeted at overeating and obesity. However to understand food-related decision making in the complex food environment it is essential to be able to ascertain the reward goal values that guide the decisions and behavioral choices that people make. These values are hidden but it is possible to ascertain them more objectively using metrics such as the willingness to pay and a method for this is described. Both these sets of methods provide quantitative measures of motivation and goal value that can be compared within and between individuals.     

State dependence,personality, and plants: light‐foraging decisions in Mimosa pudica (L.)

Plants make foraging decisions that are dependent on ecological conditions, such as resource availability and distribution. Despite the field of plant behavioral ecology gaining momentum, ecologists still know little about what factors impact plant behavior, especially light‐foraging behavior. We made use of the behavioral reaction norm approach to investigate light foraging in a plant species that exhibits rapid movement: Mimosa pudica. We explored how herbivore avoidance behavior in M. pudica (which closes its leaflets temporarily when disturbed) is affected by an individual's energy state and the quality of the current environment and also repeatedly tested the behavior of individuals from two seed sources to determine whether individuals exhibit a “personality” (i.e., behavioral syndrome). We found that when individuals are in a low‐energy state, they adopt a riskier light‐foraging strategy, opening leaflets faster, and not closing leaflets as often in response to a disturbance. However, when plants are in a high‐energy state, they exhibit a plastic light‐foraging strategy dependent on environment quality. Although we found no evidence that individuals exhibit behavioral syndromes, we found that individuals from different seed sources consistently behave differently from each other. Our results suggest that plants are capable of making state‐dependent decisions and that plant decision making is complex, depending on the interplay between internal and external factors.     

The mind through chick eyes: memory,cognition and anticipation

To understand the animal mind, we have to reconstruct how animals recognize the external world through their own eyes. For the reconstruction to be realistic, explanations must be made both in their proximate causes (brain mechanisms) as well as ultimate causes (evolutionary backgrounds). Here, we review recent advances in the behavioral, psychological, and system-neuroscience studies accomplished using the domestic chick as subjects. Diverse behavioral paradigms are compared (such as filial imprinting, sexual imprinting, one-trial passive avoidance learning, and reinforcement operant conditioning) in their behavioral characterizations (development, sensory and motor aspects of functions, fitness gains) and relevant brain mechanisms. We will stress that common brain regions are shared by these distinct paradigms, particularly those in the ventral telencephalic structures such as AIv (in the archistriatum) and LPO (in the medial striatum). Neuronal ensembles in these regions could code the chick's anticipation for forthcoming events, particularly the quality/quantity and the temporal proximity of rewards. Without the internal representation of the anticipated proximity in LPO, behavioral tolerance will be lost, and the chick makes impulsive choice for a less optimized option. Functional roles of these regions proved compatible with their anatomical counterparts in the mammalian brain, thus suggesting that the neural systems linking between the memorized past and the anticipated future have remained highly conservative through the evolution of the amniotic vertebrates during the last 300 million years. With the conservative nature in mind, research efforts should be oriented toward a unifying theory, which could explain behavioral deviations from optimized foraging, such as "na?ve curiosity," "contra-freeloading," "Concorde fallacy," and "altruism."     

The Utility of the Proximate-Ultimate Dichotomy in Ethology

We defend the organizing principle that there are fundamentally different levels of analysis in biology, notably proximate and ultimate. Despite recent claims to the contrary, the proximate-ultimate distinction is a true dichotomy, not an artificial division of a continuum. Acceptance of this dichotomy does not imply that ultimate questions are of greater importance than those dealing with proximate mechanisms, nor does it result in confusion of current reproductive consequences with evolutionary causes.     

Motivational Salience Signal in the Basal Forebrain Is Coupled with Faster and More Precise Decision Speed

The survival of animals depends critically on prioritizing responses to motivationally salient stimuli. While it is generally believed that motivational salience increases decision speed, the quantitative relationship between motivational salience and decision speed, measured by reaction time (RT), remains unclear. Here we show that the neural correlate of motivational salience in the basal forebrain (BF), defined independently of RT, is coupled with faster and also more precise decision speed. In rats performing a reward-biased simple RT task, motivational salience was encoded by BF bursting response that occurred before RT. We found that faster RTs were tightly coupled with stronger BF motivational salience signals. Furthermore, the fraction of RT variability reflecting the contribution of intrinsic noise in the decision-making process was actively suppressed in faster RT distributions with stronger BF motivational salience signals. Artificially augmenting the BF motivational salience signal via electrical stimulation led to faster and more precise RTs and supports a causal relationship. Together, these results not only describe for the first time, to our knowledge, the quantitative relationship between motivational salience and faster decision speed, they also reveal the quantitative coupling relationship between motivational salience and more precise RT. Our results further establish the existence of an early and previously unrecognized step in the decision-making process that determines both the RT speed and variability of the entire decision-making process and suggest that this novel decision step is dictated largely by the BF motivational salience signal. Finally, our study raises the hypothesis that the dysregulation of decision speed in conditions such as depression, schizophrenia, and cognitive aging may result from the functional impairment of the motivational salience signal encoded by the poorly understood noncholinergic BF neurons.     

Towards an integrative model of sociality in caviomorph rodents

In the late 1990s and early 2000s it was recognized that behavioral ecologists needed to study the sociality of caviomorph rodents (New World hystricognaths) before generalizations about rodent sociality could be made. Researchers identified specific problems facing individuals interested in caviomorph sociality, including a lack of information on the proximate mechanisms of sociality, role of social environment in development, and geographical or intraspecific variation in social systems. Since then researchers have described the social systems of many previously understudied species, including some with broad geographical ranges. Researchers have done a good job of determining the role of social environments in development and identifying the costs and benefits of social living. However, relatively little is known about the proximate mechanisms of social behavior and fitness consequences, limiting progress toward the development of integrative (evolutionary-mechanistic) models for sociality. To develop integrative models behavioral ecologists studying caviomorph rodents must generate information on the fitness consequences of different types of social organization, brain mechanisms, and endocrine substrates of sociality. We review our current understanding and future directions for research in these conceptual areas. A greater understanding of disease ecology, particularly in species carrying Old World parasites, is needed before we can identify potential links between social phenotypes, mechanism, and fitness.     

Signaling,solidarity, and the sacred: The evolution of religious behavior

Anthropologists have repeatedly noted that there has been little theoretical progress in the anthropology of religion over the past fifty years.^1–7 By the 1960s, Geertz² had pronounced the field dead. Recently, however, evolutionary researchers have turned their attention toward understanding the selective pressures that have shaped the human capacity for religious thoughts and behaviors, and appear to be resurrecting this long‐dormant but important area of research.^8–19 This work, which focuses on ultimate evolutionary explanations, is being complemented by advances in neuropsychology and a growing interest among neuroscientists in how ritual, trance, meditation, and other altered states affect brain functioning and development.^20–26 This latter research is providing critical insights into the evolution of the proximate mechanisms responsible for religious behavior. Here we review these literatures and examine both the proximate mechanisms and ultimate evolutionary processes essential for developing a comprehensive evolutionary explanation of religion.     

Decision-making in the leech nervous system

Previous models of behavioral choice have described two types of hierarchy, a decision hierarchy, in which different classes of decisions are made at each level (Tinbergen, 1951), and a behavioral hierarchy, in which one behavior will take precedence over others (Davis, 1985). Most experimental work on the neuronal basis of decision-making has focussed on the latter of these: a behavioral hierarchy is described for an animal, and the neuronal basis for this hierarchy, hypothesized to depend on inhibitory interactions, is investigated. Although the concept of "dedicated command neurons" has been useful for guiding these studies, it appears that such neurons are rare. We present evidence that in the leech, most neurons, including high-level decision neurons, are active in more than one behavior. We include data from one newly-identified neuron that elicits both swimming and crawling motor patterns. We suggest that decisions are made by a "combinatorial code": what behavior is produced depends on the specific combination of decision neurons that are active at a particular time. Finally, we discuss how decision neurons may be arranged into a decision hierarchy, with neurons at each sequential level responsible for choosing between a narrower range of behaviors. We suggest additional sensory information is incorporated at each level to inform the decision.