Adaptive explanations for sensitive windows in development.

Published onlineREVIEWThis is the final version of the article. It first appeared from BioMed Central via http://dx.doi.org/10.1186/1742-9994-12-S1-S3Development in many organisms appears to show evidence of sensitive windows-periods or stages in ontogeny in which individual experience has a particularly strong influence on the phenotype (compared to other periods or stages). Despite great interest in sensitive windows from both fundamental and applied perspectives, the functional (adaptive) reasons why they have evolved are unclear. Here we outline a conceptual framework for understanding when natural selection should favour changes in plasticity across development. Our approach builds on previous theory on the evolution of phenotypic plasticity, which relates individual and population differences in plasticity to two factors: the degree of uncertainty about the environmental conditions and the extent to which experiences during development ('cues') provide information about those conditions. We argue that systematic variation in these two factors often occurs within the lifetime of a single individual, which will select for developmental changes in plasticity. Of central importance is how informational properties of the environment interact with the life history of the organism. Phenotypes may be more or less sensitive to environmental cues at different points in development because of systematic changes in (i) the frequency of cues, (ii) the informativeness of cues, (iii) the fitness benefits of information and/or (iv) the constraints on plasticity. In relatively stable environments, a sensible null expectation is that plasticity will gradually decline with age as the developing individual gathers information. We review recent models on the evolution of developmental changes in plasticity and explain how they fit into our conceptual framework. Our aim is to encourage an adaptive perspective on sensitive windows in development.TWF was supported by the European Research Council (Advanced Grant 250209 to Alasdair Houston); WEF was supported by the Netherlands Organisation for Scientific Research (Veni Grant 016.155.195)

Comment on 'Are physicists afraid of mathematics?'

This is the final version of the article. Available from the publisher via the DOI in this record.In 2012, we showed that the citation count for articles in ecology and evolutionary biology declines with increasing density of equations. Kollmeret al (2015 New J. Phys. 17 013036) claim this effect is an artefact of the manner in which we plotted the data. They also present citation data from Physical Review Letters and argue, based on graphs, that citation counts are unrelated to equation density. Here we show that both claims are misguided. We identified the effects in biology not by visual means, but using the most appropriate statistical analysis. Since Kollmeret al did not carry out any statistical analysis, they cannot draw reliable inferences about the citation patterns in physics. We show that when statistically analysed their data actually do provide evidence that in physics, as in biology, citation counts are lower for articles with a high density of equations. This indicates that a negative relationship between equation density and citations may extend across the breadth of the sciences, even those in which researchers are well accustomed to mathematical descriptions of natural phenomena. We restate our assessment that this is a genuine problem and discuss what we think should be done about it.This work was supported by a European Research Council Advanced Grant (250209) awarded to Alasdair Houston and NERC Independent Research Fellowship (NE/L011921/1) awarded to ADH. We are indebted to the American Physical Society and Physical Review Letters for granting access to their article data and Jonathan Kollmer, Thorsten Pöschel and Jason Gallas for supplying it

Conflict between groups promotes later defense of a critical resource in a cooperatively breeding bird.

This is the author accepted manuscript. The final version is available on open access from Elsevier via http://dx.doi.org/10.1016/j.cub.2014.10.036Conflict between groups (intergroup conflict) is common in many social species and is widely discussed as an evolutionary driver of within-group dynamics and social structure. However, empirical studies investigating the impacts of intergroup conflict have focused on the immediate aftermath, when behavioral changes may be the direct result of elevated stress levels or territorial exclusions. Demonstrations of longer-term effects, with behavioral changes persisting once increases in stress have diminished and full access to resources is again possible, would support proposed links to individual fitness and social evolution. Here we show that conflicts between neighboring groups of cooperatively breeding green woodhoopoes (Phoeniculus purpureus) have a lasting influence on decisions concerning roost cavities, a limiting resource vital for survival and breeding. Groups involved in extended conflicts in the morning were more likely to return to the zone of conflict that evening, roosting closer to territorial borders, than when intergroup interactions were short or did not occur. Extended morning conflicts also increased the likelihood that groupmates roosted together and preened one another at the roost, suggesting that intergroup conflict promotes consensus decision-making, social bonding, and group cohesion. Border roost use and allopreening increased more following conflicts that were lost rather than won. By demonstrating that both the intensity and outcome of intergroup interactions affect resource defense and associated within-group behavior many hours later, our results begin to bridge the gap between the immediate impacts of intergroup conflict and its role in social evolution.This study complied with the laws of South Africa, where the data were collected, and was approved by the Science Faculty Animal Ethics Committee, University of Cape Town. We are grateful to Morné du Plessis for access to the study population he originally established and to Andrew Higginson, Christos Ioannou, and two anonymous referees for comments on the manuscript. The data were collected by A.N.R. while supported by a Natural Environment Research Council studentship

When is it adaptive to be patient? A general framework for evaluating delayed rewards

This is the author accepted manuscript. The final version is available from Elsevier via the DOI in this record.The tendency of animals to seek instant gratification instead of waiting for greater long-term benefits has been described as impatient, impulsive or lacking in self-control. How can we explain the evolution of such seemingly irrational behaviour? Here we analyse optimal behaviour in a variety of simple choice situations involving delayed rewards. We show that preferences for more immediate rewards should depend on a variety of factors, including whether the choice is a one-off or is likely to be repeated, the information the animal has about the continuing availability of the rewards and the opportunity to gain rewards through alternative activities. In contrast to the common assertion that rational animals should devalue delayed rewards exponentially, we find that this pattern of discounting is optimal only under restricted circumstances. We predict preference reversal whenever waiting for delayed rewards entails loss of opportunities elsewhere, but the direction of this reversal depends on whether the animal will face the same choice repeatedly. Finally, we question the ecological relevance of standard laboratory tests for impulsive behaviour, arguing that animals rarely face situations analogous to the self-control paradigm in their natural environment. To understand the evolution of impulsiveness, a more promising strategy would be to identify decision rules that are adaptive in a realistic ecological setting, and examine how these rules determine patterns of behaviour in simultaneous choice tests.We thank the European Research Council for financial support (Advanced Grant 250209 to A.I.H.)

Evolution of a flexible rule for foraging that copes with environmental variation

PublishedThis is the final version of the article. It first appeared from Oxford University Press via http://www.currentzoology.org/paperdetail.asp?id=12437Models of adaptive behaviour typically assume that animals behave as though they have highly complex, detailed strategies for making decisions. In reality, selection favours the optimal balance between the costs and benefits of complexity. Here we investigate this trade-off for an animal that has to decide whether or not to forage for food - and so how much energy reserves to store - depending on the food availability in its environment. We evolve a decision rule that controls the target reserve level for different ranges of food availability, but where increasing complexity is costly in that metabolic rate increases with the sensitivity of the rule. The evolved rule tends to be much less complex than the optimal strategy but performs almost as well, while being less costly to implement. It achieves this by being highly sensitive to changing food availability at low food abun-dance - where it provides a close fit to the optimal strategy - but insensitive when food is plentiful. When food availability is high, the target reserve level that evolves is much higher than under the optimal strategy, which has implications for our under-standing of obesity. Our work highlights the important principle of generalisability of simple decision-making mechanisms, which enables animals to respond reasonably well to conditions not directly experienced by themselves or their ancestors.This work was supported by the European Research Council (Advanced Grant 250209 to A.I.H.) and a College for Life Sciences Fellowship at the Wissenschaftskolleg zu Berlin awarded to A.D.H

The evolution of mechanisms underlying behaviour

This is the final version of the article. It first appeared from Oxford University press via http://www.scopus.com/record/display.uri?eid=2-s2.0-84925394342&origin=inward&txGid=0-This work was funded by the European Research Council (Advanced Grant 250209 to Alasdair Houston)

Clarifying the relationship between prospect theory and risk-sensitive foraging theory

This is the author accepted manuscript. The final version is available from Elsevier via the DOI in this record.When given a choice between options with uncertain outcomes, people tend to be loss averse and risk averse regarding potential gains and risk prone regarding potential losses. These features of human decision making are captured by prospect theory (PT)-a hugely influential descriptive model of choice, but one which lacks any unifying principle that might explain why such preferences exist. Recently there have been several attempts to connect PT with risk-sensitive foraging theory (RSFT), a normative framework developed by evolutionary biologists to explain how animals should choose optimally when faced with uncertain foraging options. Although this seems a promising direction, here we show that current approaches are overly simplistic, and, despite their claims, they leave key features of PT unaccounted for. A common problem is the failure to appreciate the central concept of reproductive value in RSFT, which depends on the decision maker's current state and the particular situation it faces. Reproductive value provides a common currency in which decisions can be compared in a logical way. In contrast, existing models provide no rational justification for the reference state in PT. Evolutionary approaches to understanding PT preferences must confront this basic problem.This work was supported by the European Research Council (ERC Advanced Grant 250209 to AIH)

Attractiveness is positively related to World Cup performance in male, but not female, biathletes

This is the author accepted manuscript. The final version is available from Oxford University Press via the DOI in this record.Whole-organism performance capacity is thought to play a key role in sexual selection,through its impacts on both intrasexual competition and intersexual mate choice. Based on data from elite sports, several studies have reported a positive association between facial attractiveness and athletic performance in humans, leading to claims that facial correlates of sporting prowess in men reveal heritable or non-heritable mate quality. However, for most of the sports studied (soccer, ice hockey, American football and cycling) it is not possible to separate individual performance from team performance. Here, using photographs of athletes who compete annually in a multi-event World Cup,we examine the relationship between facial attractiveness and individual career-best performance metrics in the biathlon, a multidisciplinary sport that combines target shooting and cross-country skiing. Unlike all previous studies, which considered only male athletes, we report relationships for both sportsmen and sportswomen. As predicted by evolutionary arguments, we found that male biathletes were judged more attractive if (unknown to the raters) they had achieved a higher peak performance (World Cup points score) in their career, whereas there was no significant relationship for female biathletes. Our findings show that elite male athletes display visible, attractive cues that reliably reflect their athletic performance

Conflict over resources generates conflict over mate choice: Reply to Smaldino and Newson

This is the author accepted manuscript. The final version is available from Elsevier via http://dx.doi.org/doi:10.1016/j.evolhumbehav.2013.12.004Evolutionary computer simulations are an important part of the theoretical biologist's toolkit (Peck, 2004; DeAngelis & Mooij, 2005; Kokko, 2007), offering insights into a range of fundamental evolutionary processes, not least sexual selection (e.g. van Doorn & Weissing 2004, 2006; Fawcett et al., 2007, 2011; van Doorn et al., 2009; reviewed in Kuijper et al., 2012). Like all theoretical tools, they must be used with care (Hamblin, 2012). Smaldino & Newson (2013, henceforth S&N) have challenged our recent work on parent–offspring conflict over mate choice (Van den Berg et al., 2013), arguing that our simulations rely on unrealistic assumptions and that our conclusions are not supported. But all four points of criticism they present are misguided. (1) The accusation that the handicap principle cannot work in our model is wrong; Fig. 1a in Van den Berg et al. (2013) clearly demonstrates that a costly preference for a signal of male quality does evolve. (2) The assertion that mutation bias drove male quality close to zero in our model is wrong; in fact, male quality reached very high, stable levels in our simulations. (3) The assertion that overcompensation was responsible for our results is wrong; parent and offspring preferences also diverge in the absence of overcompensation. (4) The alternative explanation offered for our results is wrong, because it predicts the opposite pattern to that we actually observed in our simulations. Below we address each of these misunderstandings and consider two alternative hypotheses suggested by S&

Adaptive Use of Information during Growth Can Explain Long-Term Effects of Early Life Experiences.

Development is a continuous process during which individuals gain information about their environment and adjust their phenotype accordingly. In many natural systems, individuals are particularly sensitive to early life experiences, even in the absence of later constraints on plasticity. Recent models have highlighted how the adaptive use of information can explain age-dependent plasticity. These models assume that information gain and phenotypic adjustments either cannot occur simultaneously or are completely independent. This assumption is not valid in the context of growth, where finding food results both in a size increase and learning about food availability. Here, we describe a simple model of growth to provide proof of principle that long-term effects of early life experiences can arise through the coupled dynamics of information acquisition and phenotypic change in the absence of direct constraints on plasticity. The increase in reproductive value from gaining information and sensitivity of behavior to experiences declines across development. Early life experiences have long-term impacts on age of maturity, yet-due to compensatory changes in behavior-our model predicts no substantial effects on reproductive success. We discuss how the evolution of sensitive windows can be explained by experiences having short-term effects on informational and phenotypic states, which generate long-term effects on life-history decisions.This research was funded by the European Union’s Seventh Framework Programme (FP7/2007-2011) under grant 259679 (IDEAL) awarded to T.U. T.W.F., A.D.H., and P.C.T. were supported by the European Research Council (ERC Advanced Grant 250209 Evomech to A. Houston). T.U. was supported by the Royal Society of London and the Knut and Alice Wallenberg Foundation. A.D.H. was supported by fellowships from the Wissenschaftskolleg zu Berlin and the Natural Environment Research Council (grant NE/L011921/1)