The levels of analysis revisited

The term levels of analysis has been used in several ways: to distinguish between ultimate and proximate levels, to categorize different kinds of research questions and to differentiate levels of reductionism. Because questions regarding ultimate function and proximate mechanisms are logically distinct, I suggest that distinguishing between these two levels is the best use of the term. Integrating across levels in research has potential risks, but many benefits. Consideration at one level can help generate novel hypotheses at the other, define categories of behaviour and set criteria that must be addressed. Taking an adaptationist stance thus strengthens research on proximate mechanisms. Similarly, it is critical for researchers studying adaptation and function to have detailed knowledge of proximate mechanisms that may constrain or modulate evolutionary processes. Despite the benefits of integrating across ultimate and proximate levels, failure to clearly identify levels of analysis, and whether or not hypotheses are exclusive alternatives, can create false debates. Such non-alternative hypotheses may occur between or within levels, and are not limited to integrative approaches. In this review, I survey different uses of the term levels of analysis and the benefits of integration, and highlight examples of false debate within and between levels. The best integrative biology reciprocally uses ultimate and proximate hypotheses to generate a more complete understanding of behaviour.     

Social plasticity in fish: integrating mechanisms and function

Social plasticity is a ubiquitous feature of animal behaviour. Animals must adjust the expression of their social behaviour to the nuances of daily social life and to the transitions between life‐history stages, and the ability to do so affects their Darwinian fitness. Here, an integrative framework is proposed for understanding the proximate mechanisms and ultimate consequences of social plasticity. According to this framework, social plasticity is achieved by rewiring or by biochemically switching nodes of the neural network underlying social behaviour in response to perceived social information. Therefore, at the molecular level, it depends on the social regulation of gene expression, so that different brain genomic and epigenetic states correspond to different behavioural responses and the switches between states are orchestrated by signalling pathways that interface the social environment and the genotype. At the evolutionary scale, social plasticity can be seen as an adaptive trait that can be under positive selection when changes in the environment outpace the rate of genetic evolutionary change. In cases when social plasticity is too costly or incomplete, behavioural consistency can emerge by directional selection that recruits gene modules corresponding to favoured behavioural states in that environment. As a result of this integrative approach, how knowledge of the proximate mechanisms underlying social plasticity is crucial to understanding its costs, limits and evolutionary consequences is shown, thereby highlighting the fact that proximate mechanisms contribute to the dynamics of selection. The role of teleosts as a premier model to study social plasticity is also highlighted, given the diversity and plasticity that this group exhibits in terms of social behaviour. Finally, the proposed integrative framework to social plasticity also illustrates how reciprocal causation analysis of biological phenomena (i.e. considering the interaction between proximate factors and evolutionary explanations) can be a more useful approach than the traditional proximate–ultimate dichotomy, according to which evolutionary processes can be understood without knowledge on proximate causes, thereby black‐boxing developmental and physiological mechanisms.     

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.     

Dose‐dependent effects of an immune challenge at both ultimate and proximate levels in Drosophila melanogaster

Immune responses are highly dynamic. The magnitude and efficiency of an immune response to a pathogen can change markedly across individuals, and such changes may be influenced by variance in a range of intrinsic (e.g. age, genotype, sex) and external (e.g. abiotic stress, pathogen identity, strain) factors. Life history theory predicts that up‐regulation of the immune system will come at a physiological cost, and studies have confirmed that increased investment in immunity can reduce reproductive output and survival. Furthermore, males and females often have divergent reproductive strategies, and this might drive the evolution of sex‐specific life history trade‐offs involving immunity, and sexual dimorphism in immune responses per se. Here, we employ an experiment design to elucidate dose‐dependent and sex‐specific responses to exposure to a nonpathogenic immune elicitor at two scales – the ‘ultimate’ life history and the underlying ‘proximate’ immune level in Drosophila melanogaster. We found dose‐dependent effects of immune challenges on both male and female components of reproductive success, but not on survival, as well as a response in antimicrobial activity. These results indicate that even in the absence of the direct pathogenic effects that are associated with actual disease, individual life histories respond to a perceived immune challenge – but with the magnitude of this response being contingent on the initial dose of exposure. Furthermore, the results indicate that immune responses at the ultimate life history level may indeed reflect underlying processes that occur at the proximate level.     

Ultimate explanations concern the adaptive rationale for organism design

My understanding is that proximate explanations concern adaptive mechanism and that ultimate explanations concern adaptive rationale. Viewed in this light, the two kinds of explanation are quite distinct, but they interact in a complementary way to give a full understanding of biological adaptations. In contrast, Laland et al. (2013)—following a literal reading of Mayr (Science 134:1501–1506, 1961)—have characterized ultimate explanations as concerning any and all mechanisms that have operated over the course of an organism’s evolutionary history. This has unfortunate consequences, such as allowing random drift to form the basis for ultimate explanations, and allowing proximate and ultimate explanations to bleed into each other until their distinction is meaningless. Here, I suggest Laland et al’s explanatory framework of “reciprocal causation” is not conducive to successful biological science, and that they have misunderstood key elements of the theory of Darwinian adaptation.     

Intelligence in Corvids and Apes: A Case of Convergent Evolution?

Intelligence is suggested to have evolved in primates in response to complexities in the environment faced by their ancestors. Corvids, a large-brained group of birds, have been suggested to have undergone a convergent evolution of intelligence [ Emery & Clayton (2004) Science , Vol. 306, pp. 1903–1907 ]. Here we review evidence for the proposal from both ultimate and proximate perspectives. While we show that many of the proposed hypotheses for the evolutionary origin of great ape intelligence also apply to corvids, further study is needed to reveal the selective pressures that resulted in the evolution of intelligent behaviour in both corvids and apes. For comparative proximate analyses we emphasize the need to be explicit about the level of analysis to reveal the type of convergence that has taken place. Although there is evidence that corvids and apes solve social and physical problems with similar speed and flexibility, there is a great deal more to be learned about the representations and algorithms underpinning these computations in both groups. We discuss recent comparative work that has addressed proximate questions at this level, and suggest directions for future research.     

Morphology and behaviour: functional links in development and evolution

Development and evolution of animal behaviour and morphology are frequently addressed independently, as reflected in the dichotomy of disciplines dedicated to their study distinguishing object of study (morphology versus behaviour) and perspective (ultimate versus proximate). Although traits are known to develop and evolve semi-independently, they are matched together in development and evolution to produce a unique functional phenotype. Here I highlight similarities shared by both traits, such as the decisive role played by the environment for their ontogeny. Considering the widespread developmental and functional entanglement between both traits, many cases of adaptive evolution are better understood when proximate and ultimate explanations are integrated. A field integrating these perspectives is evolutionary developmental biology (evo-devo), which studies the developmental basis of phenotypic diversity. Ultimate aspects in evo-devo studies--which have mostly focused on morphological traits--could become more apparent when behaviour, 'the integrator of form and function', is integrated into the same framework of analysis. Integrating a trait such as behaviour at a different level in the biological hierarchy will help to better understand not only how behavioural diversity is produced, but also how levels are connected to produce functional phenotypes and how these evolve. A possible framework to accommodate and compare form and function at different levels of the biological hierarchy is outlined. At the end, some methodological issues are discussed.     

Causes,proximate and ultimate

Within evolutionary biology a distinction is frequently made between proximate and ultimate causes. One apparently plausible interpretation of this dichotomy is that proximate causes concern processes occurring during the life of an organism while ultimate causes refer to those processes (particularly natural selection) that shaped its genome. But ultimate causes are not sought through historical investigations of an organisms lineage. Rather, explanations referring to ultimate causes typically emerge from functional analyses. But these functional analyses do not identify causes of any kind, much less ultimate ones. So-called ultimate explanations are not about causes in any sense resembling those of proximate explanations. The attitude, implicit in the term ultimate cause, that these functional analyses are somehow superordinate to those involving proximate causes is unfounded. Ultimate causes are neither ultimate nor causes.     

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.     

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.     

Humans and insects decide in similar ways

Behavioral ecologists assume that animals use a motivational mechanism for decisions such as action selection and time allocation, allowing the maximization of their fitness. They consider both the proximate and ultimate causes of behavior in order to understand this type of decision-making in animals. Experimental psychologists and neuroeconomists also study how agents make decisions but they consider the proximate causes of the behavior. In the case of patch-leaving, motivation-based decision-making remains simple speculation. In contrast to other animals, human beings can assess and evaluate their own motivation by an introspection process. It is then possible to study the declared motivation of humans during decision-making and discuss the mechanism used as well as its evolutionary significance. In this study, we combine both the proximate and ultimate causes of behavior for a better understanding of the human decision-making process. We show for the first time ever that human subjects use a motivational mechanism similar to small insects such as parasitoids and bumblebees to decide when to leave a patch. This result is relevant for behavioral ecologists as it supports the biological realism of this mechanism. Humans seem to use a motivational mechanism of decision making known to be adaptive to a heterogeneously distributed resource. As hypothesized by Hutchinson et al. and Wilke and Todd, our results are consistent with the evolutionary shaping of decision making because hominoids were hunters and gatherers on food patches for more than two million years. We discuss the plausibility of a neural basis for the motivation mechanism highlighted here, bridging the gap between behavioral ecology and neuroeconomy. Thus, both the motivational mechanism observed here and the neuroeconomy findings are most likely adaptations that were selected for during ancestral times.     

Ernst Mayr's 'ultimate/proximate' distinction reconsidered and reconstructed

It's been 41 years since the publication of Ernst Mayr's Cause and Effect in Biology wherein Mayr most clearly develops his version of the influential distinction between ultimate and proximate causes in biology. In critically assessing Mayr's essay I uncover false statements and red-herrings about biological explanation. Nevertheless, I argue to uphold an analogue of the ultimate/proximate distinction as it refers to two different kinds of explanations, one dynamical the other statistical.     

Behavioural biology: an effective and relevant conservation tool

'Conservation behaviour' is a young discipline that investigates how proximate and ultimate aspects of the behaviour of an animal can be of value in preventing the loss of biodiversity. Rumours of its demise are unfounded. Conservation behaviour is quickly building a capacity to positively influence environmental decision making. The theoretical framework used by animal behaviourists is uniquely valuable to elucidating integrative solutions to human-wildlife conflicts, efforts to reintroduce endangered species and reducing the deleterious effects of ecotourism. Conservation behaviourists must join with other scientists under the multidisciplinary umbrella of conservation biology without giving up on their focus: the mechanisms, development, function and evolutionary history of individual differences in behaviour. Conservation behaviour is an increasingly relevant tool in the preservation of nature.     

Conceptual Revision and Synthesis of Proximate Factors Associated with Age‐Related Improvement in Reproduction

Improvement in reproductive performance with age, up to the point of senescence, is a predominant pattern among vertebrates. Predictions from life‐history theory provide a powerful framework for understanding the evolutionary basis of these patterns. However, based on the growing number of publications on this topic, there is increased interest in understanding the proximate causes of age‐related improvements in reproductive performance (ARIRP). A formal conceptual framework through which factors related to ARIRP can be examined is lacking. Here, we establish hypotheses with testable predictions for social and ecological factors, including resource quality, mate fidelity, site fidelity, prior breeding experience, and changes in ability to attract mates. We use this conceptual framework to review 55 empirical studies published (between 1900 through 2013) on avian species as birds have the greatest representation in empirical studies of ARIRP. Our synthesis revealed that tests of the breeding experience hypothesis are most prevalent in the literature, whereas tests of the site fidelity hypothesis are least prevalent. Overall, the role of increased mate attraction with age seems to be an important predictor of ARIRP, whereas changes in resource quality with age show the least support among published studies. Because many studies suffered from small sample sizes and did not control for confounding variables, we suggest experimental methodologies for teasing apart hypotheses in empirical investigations and offer statistical approaches for longitudinal datasets. From an ultimate perspective, we also highlight the role of life‐history variation, in shaping within‐individual improvements. Future work should employ a standardized framework to study patterns of ARIRP, as set forward here, to allow for more quantitative comparison of results across studies.     

Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection

From an evolutionary perspective, social behaviours are those which have fitness consequences for both the individual that performs the behaviour, and another individual. Over the last 43 years, a huge theoretical and empirical literature has developed on this topic. However, progress is often hindered by poor communication between scientists, with different people using the same term to mean different things, or different terms to mean the same thing. This can obscure what is biologically important, and what is not. The potential for such semantic confusion is greatest with interdisciplinary research. Our aim here is to address issues of semantic confusion that have arisen with research on the problem of cooperation. In particular, we: (i) discuss confusion over the terms kin selection, mutualism, mutual benefit, cooperation, altruism, reciprocal altruism, weak altruism, altruistic punishment, strong reciprocity, group selection and direct fitness; (ii) emphasize the need to distinguish between proximate (mechanism) and ultimate (survival value) explanations of behaviours. We draw examples from all areas, but especially recent work on humans and microbes.     

Ultimate and proximate mechanisms underlying the occurrence of bears close to human settlements: review and management implications

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The synthetic approach to the study of spatial memory: Have we properly addressed Tinbergen's “four questions”?

In 1963, Niko Tinbergen suggested that to truly understand the behavior of an animal, the ultimate causes (e.g., adaptive value, evolutionary history) as well as the proximate mechanisms (e.g., neurobiology, development) that result in the production of the behavior must be understood in an integrated framework. We examine whether the study of spatial memory in food storing birds has adequately addressed Tinbergen's questions and highlight the work of Sara Shettleworth, who has made a tremendous contribution to this area of study, and whom this issue honors. Our conclusion is that while the study of food caching and spatial memory in birds has been a very good model of a program of research that has addressed Tinbergen's questions, additional work remains.