Homoplasy, homology, and the perceived special status of behavior in evolution

Evolutionary biologists tend to tread cautiously when considering how behavioral data might be incorporated into phylogenetic analyses, largely because of the preconception that behavior somehow constitutes a "special" set of characters that may be inherently more prone to homoplasy or subject to different selection regimes than those that operate on the morphological or genetic traits traditionally used in phylogenetic reconstruction. In this review, we first consider how the evolution of behavior has been treated historically, paying particular attention to why phylogenetic reconstruction has often failed to include behavioral traits. We then discuss, from a theoretical perspective, what reasons there are--if any--for assuming that behavioral traits should be more prone to homoplasy than other types of traits. In doing so, we review several empirical studies that tackle this issue head-on. Finally, we examine how behavioral features have been used to good effect in phylogenetic reconstruction. Our conclusion is that there seems to be little justification on theoretical grounds for assuming that behavior is in any way "special"--either particularly labile or particularly prone to exhibit high levels of homoplasy. Additionally, in reviewing historical perceptions of behavior and their links to conceptions of homology, we conclude that there is no compelling reason why behavior cannot be homologized or therefore why it should not prove phylogenetically informative. In subsequently considering several factors related to selection that influence the likelihood of homoplasy occurring in any trait system, we also found no clear trend predicting homoplasy disproportionately in behavioral systems. In fact, where studied, the degree of homoplasy seen in behavioral traits is comparable to that seen in other trait systems. Ultimately, there appear to be no grounds for dismissing behavior a priori from the class of phylogenetically informative characters.     

Modeling for Understanding v. Modeling for Numbers

I draw a distinction between Modeling for Numbers, which aims to address how much, when, and where questions, and Modeling for Understanding, which aims to address how and why questions. For-numbers models are often empirical, which can be more accurate than their mechanistic analogues as long as they are well calibrated and predictions are made within the domain of the calibration data. To extrapolate beyond the domain of available system-level data, for-numbers models should be mechanistic, relying on the ability to calibrate to the system components even if it is not possible to calibrate to the system itself. However, development of a mechanistic model that is reliable depends on an adequate understanding of the system. This understanding is best advanced using a for-understanding modeling approach. To address how and why questions, for-understanding models have to be mechanistic. The best of these for-understanding models are focused on specific questions, stripped of extraneous detail, and elegantly simple. Once the mechanisms are well understood, one can then decide if the benefits of incorporating the mechanism in a for-numbers model is worth the added complexity and the uncertainty associated with estimating the additional model parameters.     

The evolutionary roots of our environmental problems: toward a Darwinian ecology

It is widely acknowledged that we need to stabilize population growth and reduce our environmental impact; however, there is little consensus about how we might achieve these changes. Here I show how evolutionary analyses of human behavior provide important, though generally ignored, insights into our environmental problems. First, I review increasing evidence that Homo sapiens has a long history of causing ecological problems. This means that, contrary to popular belief, our species' capacity for ecological destruction is not simply due to "Western" culture. Second, I provide an overview of how evolutionary research can help to understand why humans are ecologically destructive, including the reasons why people often overpopulate, overconsume, exhaust common-pool resources, discount the future, and respond maladaptively to modern environmental hazards. Evolutionary approaches not only explain our darker sides, they also provide insights into why people cherish plants and animals and often support environmental and conservation efforts (e.g., Wilson's "biophilia hypothesis"). Third, I show how evolutionary analyses of human behavior offer practical implications for environmental policy, education, and activism. I suggest that education is necessary but insufficient because people also need incentives. Individual incentives are likely to be the most effective, but these include much more than narrow economic interests (e.g., they include one's reputation in society). Moralizing and other forms of social pressure used by environmentalists to bring about change appear to be effective, but this idea needs more research. Finally, I suggest that integrating evolutionary perspectives into the environmental sciences will help to break down the artificial barriers that continue to divide the biological and social sciences, which unfortunately obstruct our ability to understand ourselves and effectively address our environmental problems.     

Consequences of population topology for studying gene flow using link‐based landscape genetic methods

Many landscape genetic studies aim to determine the effect of landscape on gene flow between populations. These studies frequently employ link‐based methods that relate pairwise measures of historical gene flow to measures of the landscape and the geographical distance between populations. However, apart from landscape and distance, there is a third important factor that can influence historical gene flow, that is, population topology (i.e., the arrangement of populations throughout a landscape). As the population topology is determined in part by the landscape configuration, I argue that it should play a more prominent role in landscape genetics. Making use of existing literature and theoretical examples, I discuss how population topology can influence results in landscape genetic studies and how it can be taken into account to improve the accuracy of these results. In support of my arguments, I have performed a literature review of landscape genetic studies published during the first half of 2015 as well as several computer simulations of gene flow between populations. First, I argue why one should carefully consider which population pairs should be included in link‐based analyses. Second, I discuss several ways in which the population topology can be incorporated in response and explanatory variables. Third, I outline why it is important to sample populations in such a way that a good representation of the population topology is obtained. Fourth, I discuss how statistical testing for link‐based approaches could be influenced by the population topology. I conclude the article with six recommendations geared toward better incorporating population topology in link‐based landscape genetic studies.     

The impossibility and necessity of quality of life research

There are probably a number of reasons why the medical community pays surprisingly little systematic attention to quality of life, either in research or in clinical care. Possibly our society's fascination with high technology and the rescue of endangered lives has encouraged the medical profession to focus on acute care, where their interventions can bring dramatic results. And perhaps because such high-tech acute care requires great knowledge and skill, medical educators have not devoted as much time to educating students and residents about the more mundane matters of medicine. Another reason, on which I will focus here, is the fact that scientific research into quality of life is particularly difficult, methodologically. It does not lend itself easily to the crisp, clean answers for which we strive in basic science. It is "soft," inexact, not "hard." In this article I hope to explain why such research is indeed fraught with hazard. The scientists are attempting a task that is, in a profound philosophical sense, impossible. They have no direct access to the data they most need, and every method of validating their results is fundamentally flawed. Nevertheless, I will also suggest how we can fruitfully undertake such research and, equally important, why we must.     

Why are behavioral and immune traits linked?

Through behavior, animals interact with a world where parasites abound. It is easy to understand how behavioral traits can thus have a differential effect on pathogen exposure. Harder to understand is why we observe behavioral traits to be linked to immune defense traits. Is variation in immune traits a consequence of behavior-induced variation in immunological experiences? Or is variation in behavioral traits a function of immune capabilities? Is our immune system a much bigger driver of personality than anticipated? In this review, I provide examples of how behavioral and immune traits co-vary. I then explore the different routes linking behavioral and immune traits, emphasizing on the physiological/hormonal mechanisms that could lead to immune control of behavior. Finally, I discuss why we should aim at understanding more about the mechanisms connecting these phenotypic traits.     

What was Fisher's fundamental theorem of natural selection and what was it for?

Fisher's 'fundamental theorem of natural selection' is notoriously abstract, and, no less notoriously, many take it to be false. In this paper, I explicate the theorem, examine the role that it played in Fisher's general project for biology, and analyze why it was so very fundamental for Fisher. I defend and Lessard (1997) in the view that the theorem is in fact a true theorem if, as Fisher claimed, 'the terms employed' are 'used strictly as defined' (1930, p. 38). Finally, I explain the role that projects such as Fisher's play in the progress of scientific inquiry.     

Simulation of biological evolution and the NFL theorems

William Dembski (No free lunch: why specified complexity cannot be purchased without intelligence, 2002) claimed that the NFL theorems from optimization theory render darwinian biological evolution impossible. Häggström (Biology and Philosophy 22:217–230, 2007) argued that the NFL theorems are not relevant for biological evolution at all, since the assumptions of the NFL theorems are not met. Although I agree with Häggström (Biology and Philosophy 22:217–230, 2007), in this article I argue that the NFL theorems should be interpreted as dealing with an extreme case within a much broader context. This broader context is in fact relevant for scientific research of certain evolutionary processes; not in the sense that the theorems can be used to draw conclusions about any intelligent design inference, but in the sense that it helps us to interpret computer simulations of evolutionary processes. As a result of this discussion, I will argue that from simulations, we do not learn much about how complexity arises in the universe. This position is in contrast with certain claims in the literature that I will discuss.     

How to write consistently boring scientific literature

Although scientists typically insist that their research is very exciting and adventurous when they talk to laymen and prospective students, the allure of this enthusiasm is too often lost in the predictable, stilted structure and language of their scientific publications. I present here, a top-10 list of recommendations for how to write consistently boring scientific publications. I then discuss why we should and how we could make these contributions more accessible and exciting.     

A review of the evolutionary causes of rodent group-living

I analyze and summarize the empirical evidence supporting alternative hypotheses posed to explain the evolution of rodent group-living. Eight hypotheses are considered: two rely on net fitness benefits to individuals, five rely on ecological and life-history constraints, and one uses elements of both. I expose the logic behind each hypothesis, identify its key predictions, examine how the available evidence on rodent socioecology supports or rejects its predictions, and identify some priorities for future research. I show that empirical support for most hypotheses is meager due to a lack of relevant studies. Also, empirical support for a particular hypothesis, when it exists, comes from studies of the same species used to formulate the original hypothesis. Two exceptions are the hypothesis that individual rodents live in groups to reduce their predation risk and the hypothesis that group-living was adopted by individuals to reduce their cost of thermoregulation. Finally, most hypotheses have been examined without regard to competing hypotheses and often in a restricted taxonomic context. This is clearly an unfortunate situation given that most competing hypotheses are not mutually exclusive. I suggest that in the future comparative approaches should be used. These studies should examine simultaneously the relevance of different benefits and constraints hypothesized to explain the evolution of rodent sociality.     

The effectiveness and limitations of immune memory: understanding protective immune responses

Immune memory is the foundation of the practise of vaccination. Research on the molecular and cellular events leading to generation and development of memory T and B lymphocytes explain why there are heightened secondary immune responses after an initial encounter with antigen. In this review, we discuss how clonal expansion, targeted tissue localisation, more efficient antigen recognition and more proficient effector functions contribute to the improved effectiveness of memory cells. Despite the enhanced efficacy of memory cells and the recall immune response, there are numerous experimental and empirical examples in which protection provided by vaccines are short-lived, particularly against pathogens that replicate and cause pathology at their site of entry. In the absence of active immune effector activities, the ability of memory cells to respond quickly enough to control this type of infection is limited. The protective efficacy of bovine herpes virus-1 vaccines in experimental and field challenge conditions are used to illustrate the concept that full protection from disease conferred by vaccination requires the presence of active immune effector mechanisms. Thus, regardless of the many successful technological advances in vaccine design and better understanding of mechanisms underlining induction of memory responses by vaccination, we should recognise that vaccine immunoprophylaxis has limitations. Expectations for vaccines should be realistic and linked to the understanding of host immune responses and knowledge regarding the pathogen and disease pathogenesis.     

Individual differences in behavioural plasticities

Interest in individual differences in animal behavioural plasticities has surged in recent years, but research in this area has been hampered by semantic confusion as different investigators use the same terms (e.g. plasticity, flexibility, responsiveness) to refer to different phenomena. The first goal of this review is to suggest a framework for categorizing the many different types of behavioural plasticities, describe examples of each, and indicate why using reversibility as a criterion for categorizing behavioural plasticities is problematic. This framework is then used to address a number of timely questions about individual differences in behavioural plasticities. One set of questions concerns the experimental designs that can be used to study individual differences in various types of behavioural plasticities. Although within‐individual designs are the default option for empirical studies of many types of behavioural plasticities, in some situations (e.g. when experience at an early age affects the behaviour expressed at subsequent ages), ‘replicate individual’ designs can provide useful insights into individual differences in behavioural plasticities. To date, researchers using within‐individual and replicate individual designs have documented individual differences in all of the major categories of behavioural plasticities described herein. Another important question is whether and how different types of behavioural plasticities are related to one another. Currently there is empirical evidence that many behavioural plasticities [e.g. contextual plasticity, learning rates, IIV (intra‐individual variability), endogenous plasticities, ontogenetic plasticities) can themselves vary as a function of experiences earlier in life, that is, many types of behavioural plasticity are themselves developmentally plastic. These findings support the assumption that differences among individuals in prior experiences may contribute to individual differences in behavioural plasticities observed at a given age. Several authors have predicted correlations across individuals between different types of behavioural plasticities, i.e. that some individuals will be generally more plastic than others. However, empirical support for most of these predictions, including indirect evidence from studies of relationships between personality traits and plasticities, is currently sparse and equivocal. The final section of this review suggests how an appreciation of the similarities and differences between different types of behavioural plasticities may help theoreticians formulate testable models to explain the evolution of individual differences in behavioural plasticities and the evolutionary and ecological consequences of individual differences in behavioural plasticities.     

DNA barcoding Central Asian butterflies: increasing geographical dimension does not significantly reduce the success of species identification

DNA barcoding employs short, standardized gene regions (5' segment of mitochondrial cytochrome oxidase subunit I for animals) as an internal tag to enable species identification. Prior studies have indicated that it performs this task well, because interspecific variation at cytochrome oxidase subunit I is typically much greater than intraspecific variation. However, most previous studies have focused on local faunas only, and critics have suggested two reasons why barcoding should be less effective in species identification when the geographical coverage is expanded. They suggested that many recently diverged taxa will be excluded from local analyses because they are allopatric. Second, intraspecific variation may be seriously underestimated by local studies, because geographical variation in the barcode region is not considered. In this paper, we analyse how adding a geographical dimension affects barcode resolution, examining 353 butterfly species from Central Asia. Despite predictions, we found that geographically separated and recently diverged allopatric species did not show, on average, less sequence differentiation than recently diverged sympatric taxa. Although expanded geographical coverage did substantially increase intraspecific variation reducing the barcoding gap between species, this did not decrease species identification using neighbour-joining clustering. The inclusion of additional populations increased the number of paraphyletic entities, but did not impede species-level identification, because paraphyletic species were separated from their monophyletic relatives by substantial sequence divergence. Thus, this study demonstrates that DNA barcoding remains an effective identification tool even when taxa are sampled from a large geographical area.     

Animal dissection and evidence-based life-science and health-professions education

Cambridge mathematician and philosopher W. K. Clifford (1879/1999) con-cluded his famous essay, "The Ethics of Belief" with the bold claim that "it is wrong always, everywhere, and for anyone to believe anything upon insufficient evidence" (p.77). Clifford's enthusiasm for evidentialism-the principle that one should proportion one's belief to the strength of the evidence-may have been overzealous, but a plausible interpretation of his view is this: Because beliefs of-ten have serious moral consequences, one should base one's beliefs on the evi-dence, and it is intellectually and morally irresponsible not to do so. This per-spective motivates recent so-called "evidence-based" methods in the fields of medicine and education. Balcombe's (2000, 2001) case for replacing learning methods that require pain, suffering, and death for animals with methods that do not (computer-assisted learning, three-dimensional models, videotapes, and other alternatives) can be seen as motivated by this evidentialist perspective. Balcombe provided a wealth of empirical evidence from educational studies to show that in most contexts animal dissection is not necessary-and even counterproductive-to achieve valid educa-tional goals, especially higher order goals (concept learning and problem solving). He demonstrated that no sound defense of dissection has been given. Can we learn as effectively without hurting or killing another being? If so, why do we not try? Many of the studies Balcombe cites have supported sufficiently the adequacy and, often, superiority of learning methods that do not harm animals or students. The first of the aforementioned questions is being answered; we can learn effectively with these non-detrimental methods. Those who seek to educate (and accept the prin-ciple of "do no harm") must seize the second question because they see, in the big pic-ture, the benefit for themselves, their students, their society, and other sentient beings. (p. 132)     

The minimum endpoint variance trajectory depends on the profile of the signal-dependent noise

It has been proposed that the central nervous system determines reaching movement trajectories so as to minimize the positional variance of the endpoint in the presence of signal-dependent noise. The hypothesis well reproduces the empirical movement trajectories for noise to the control signal whose variance is proportional to the second power of the amplitude of the control signal. However, empirical studies do not necessarily exhibit such a simple signal-noise relationship. The studies exhibit a wide distribution of estimates of the value of the exponent. This discrepancy raises the question of how the minimum endpoint variance trajectory depends on the value of the exponent. To address this question, we calculated minimum endpoint variance trajectories in simulations in which the value of the exponent was varied from 0 to 3. We found that the optimal trajectories differed according to the value of the exponent, and the profiles of optimal trajectories gradually diverged from the empirical ones as the value approached 0, though this change was not remarkable for larger values. Moreover, the optimal trajectories failed to replicate Fitts' law when the value was not equal to 2. These results suggest that the acceptability of the minimum endpoint variance theory depends on the value of the exponent in our motor system.     

How phenological tracking shapes species and communities in non-stationary environments

Climate change alters the environments of all species. Predicting species responses requires understanding how species track environmental change, and how such tracking shapes communities. Growing empirical evidence suggests that how species track phenologically – how an organism shifts the timing of major biological events in response to the environment – is linked to species performance and community structure. Such research tantalizingly suggests a potential framework to predict the winners and losers of climate change, and the future communities we can expect. But developing this framework requires far greater efforts to ground empirical studies of phenological tracking in relevant ecological theory. Here we review the concept of phenological tracking in empirical studies and through the lens of coexistence theory to show why a community-level perspective is critical to accurate predictions with climate change. While much current theory for tracking ignores the importance of a multi-species context, basic community assembly theory predicts that competition will drive variation in tracking and trade-offs with other traits. We highlight how existing community assembly theory can help understand tracking in stationary and non-stationary systems. But major advances in predicting the species- and community-level consequences of climate change will require advances in theoretical and empirical studies. We outline a path forward built on greater efforts to integrate priority effects into modern coexistence theory, improved empirical estimates of multivariate environmental change, and clearly defined estimates of phenological tracking and its underlying environmental cues.     

Selection does not favor larger body size at lower temperature in a seed-feeding beetle

Body size of many animals increases with increasing latitude, a phenomenon known as Bergmann's rule (Bergmann clines). Latitudinal gradients in mean temperature are frequently assumed to be the underlying cause of this pattern because temperature covaries systematically with latitude, but whether and how temperature mediates selection on body size is unclear. To test the hypothesis that the "relative" advantage of being larger is greatest at cooler temperatures we compare the fitness of replicate lines of the seed beetle, Stator limbatus, for which body size was manipulated via artificial selection ("Large,"Control," and "Small" lines), when raised at low (22 degrees C) and high (34 degrees C) temperatures. Large-bodied beetles (Large lines) took the longest to develop but had the highest lifetime fecundity, and highest fitness (r(C)), at both low and high temperatures. However, the relative difference between the Large and Small lines did not change with temperature (replicate 2) or was greatest at high temperature (replicate 1), contrary to the prediction that the fitness advantage of being large relative to being small will decline with increasing temperature. Our results are consistent with two previous studies of this seed beetle, but inconsistent with prior studies that suggest that temperature-mediated selection on body size is a major contributor to the production of Bergmann clines. We conclude that other environmental and ecological variables that covary with latitude are more likely to produce the gradient in natural selection responsible for generating Bergmann clines.     

A Normalization Model of Attentional Modulation of Single Unit Responses

Although many studies have shown that attention to a stimulus can enhance the responses of individual cortical sensory neurons, little is known about how attention accomplishes this change in response. Here, we propose that attention-based changes in neuronal responses depend on the same response normalization mechanism that adjusts sensory responses whenever multiple stimuli are present. We have implemented a model of attention that assumes that attention works only through this normalization mechanism, and show that it can replicate key effects of attention. The model successfully explains how attention changes the gain of responses to individual stimuli and also why modulation by attention is more robust and not a simple gain change when multiple stimuli are present inside a neuron''s receptive field. Additionally, the model accounts well for physiological data that measure separately attentional modulation and sensory normalization of the responses of individual neurons in area MT in visual cortex. The proposal that attention works through a normalization mechanism sheds new light a broad range of observations on how attention alters the representation of sensory information in cerebral cortex.     

Six things Popper would like biologists not to ignore: In memoriam, Karl Raimund Popper, 1902–1994

To honour the memory of Sir Karl Popper, I put forward six elements of his philosophy which might be of particular interest to biologists and to philosophers of biology and which I think Popper would like them not to ignore, even if they disagree with him. They are: the primacy of problems; the criticizability of metaphysics (and thus the dubiousness of materialism); how downward causation might be real; how norms should matter to scientists; why dogmatism should be avoided; how genuine science is recognizable. I preface these six things with a brief discussion of Popper's early (but later recanted) mistakes concerning biology.