Empirical tests of "Take-the-Best" with non-human subjects

The fast and frugal heuristics of ABC and rules of thumb of behavioural biologists represent strategies that humans and other animals might use to make decisions under time constraints and with a minimum of information. If experimental psychologists could demonstrate use of simple heuristics by non-humans in experimental settings, quantitative and empirical evaluation of those heuristics would benefit from additional formal, controlled avenues of study.     

The assembly and disassembly of ecological networks

Global change has created a severe biodiversity crisis. Species are driven extinct at an increasing rate, and this has the potential to cause further coextinction cascades. The rate and shape of these coextinction cascades depend very much on the structure of the networks of interactions across species. Understanding network structure and how it relates to network disassembly, therefore, is a priority for system-level conservation biology. This process of network collapse may indeed be related to the process of network build-up, although very little is known about both processes and even less about their relationship. Here we review recent work that provides some preliminary answers to these questions. First, we focus on network assembly by emphasizing temporal processes at the species level, as well as the structural building blocks of complex ecological networks. Second, we focus on network disassembly as a consequence of species extinctions or habitat loss. We conclude by emphasizing some general rules of thumb that can help in building a comprehensive framework to understand the responses of ecological networks to global change.     

Connecting behavioural biologists and psychologists: Clarifying distinctions and suggestions for further work

This article is a reply to the commentaries on our target article, which relates our group's work on simple heuristics to biological research on rules of thumb. Several commentators contrasted both these approaches with behaviour analysis, in which the patterns of behaviour investigated in the laboratory are claimed to be near-universal attributes, rather than specific to particular appropriate environments. We question this universality. For instance, learning phenomena such Pavlovian or operant conditioning have mostly been studied only in a few generalist species that learn easily; in many natural situations the environment hinders learning as an adaptive strategy. Other supposedly general phenomena such as impulsiveness and matching are outcome models, which several different models of simple cognitive processes might explain. We clarify some confusions about optimisation, optima and optimality modelling. Lastly, we say a little more about how heuristics might be selected, learnt and tuned to suit the current environment.     

Vervet monkeys use paths consistent with context‐specific spatial movement heuristics

Animal foraging routes are analogous to the computationally demanding “traveling salesman problem” (TSP), where individuals must find the shortest path among several locations before returning to the start. Humans approximate solutions to TSPs using simple heuristics or “rules of thumb,” but our knowledge of how other animals solve multidestination routing problems is incomplete. Most nonhuman primate species have shown limited ability to route plan. However, captive vervets were shown to solve a TSP for six sites. These results were consistent with either planning three steps ahead or a risk‐avoidance strategy. I investigated how wild vervet monkeys (Chlorocebus pygerythrus) solved a path problem with six, equally rewarding food sites; where site arrangement allowed assessment of whether vervets found the shortest route and/or used paths consistent with one of three simple heuristics to navigate. Single vervets took the shortest possible path in fewer than half of the trials, usually in ways consistent with the most efficient heuristic (the convex hull). When in competition, vervets' paths were consistent with different, more efficient heuristics dependent on their dominance rank (a cluster strategy for dominants and the nearest neighbor rule for subordinates). These results suggest that, like humans, vervets may solve multidestination routing problems by applying simple, adaptive, context‐specific “rules of thumb.” The heuristics that were consistent with vervet paths in this study are the same as some of those asserted to be used by humans. These spatial movement strategies may have common evolutionary roots and be part of a universal mental navigational toolkit. Alternatively, they may have emerged through convergent evolution as the optimal way to solve multidestination routing problems.     

Speciation reversal and biodiversity dynamics with hybridization in changing environments

A considerable fraction of the world's biodiversity is of recent evolutionary origin and has evolved as a by-product of, and is maintained by, divergent adaptation in heterogeneous environments. Conservationists have paid attention to genetic homogenization caused by human-induced translocations (e.g. biological invasions and stocking), and to the importance of environmental heterogeneity for the ecological coexistence of species. However, far less attention has been paid to the consequences of loss of environmental heterogeneity to the genetic coexistence of sympatric species. Our review of empirical observations and our theoretical considerations on the causes and consequences of interspecific hybridization suggest that a loss of environmental heterogeneity causes a loss of biodiversity through increased genetic admixture, effectively reversing speciation. Loss of heterogeneity relaxes divergent selection and removes ecological barriers to gene flow between divergently adapted species, promoting interspecific introgressive hybridization. Since heterogeneity of natural environments is rapidly deteriorating in most biomes, the evolutionary ecology of speciation reversal ought to be fully integrated into conservation biology.     

The dynamics of diversification in evolving Pseudomonas populations

Determining the mechanisms that promote the evolution of diversity is a central problem in evolutionary biology. Previous studies have demonstrated that diversification occurs in complex environments and that genotypes specialized on alternative resources can be maintained over short time scales. Here, we describe a selection experiment that has tracked the dynamics of adaptive diversification within selection lines of the asexual bacteria Pseudomonas fluorescens over about 900 generations. We cultured experimental populations from the same two isogenic ancestral strains in simple, single-substrate environments or in complex, four-substrate environments. Following selection we assayed the growth of genotypes from each population on each substrate individually. We estimated mutational heritability, Vm/VE, as 1 x 10(-3) per generation in simple environments and 3 x 10(-3) per generation in complex environments. These values are roughly consistent with estimates reported in other systems. Populations selected in complex environments evolved into genetically diverse communities. Genotypes exhibited greater metabolic differentiation from other genotypes in their own population than to genotypes evolving in other populations, presumably as a result of resource competition. In populations selected in simple environments, little genetic diversity evolved, and genotypes shared very similar phenotypes. Our findings suggest that ecological opportunity provided by environmental complexity plays a major role in the evolution and maintenance of diversity.     

Ten Heuristics for Interdisciplinary Modeling Projects

Complex environmental and ecological problems require collaborative, interdisciplinary efforts. A common approach to integrating disciplinary perspectives on these problems is to develop simulation models in which the linkages between system components are explicitly represented. There is, however, little guidance in the literature on how such models should be developed through collaborative teamwork. In this paper, we offer a set of heuristics (rules of thumb) that address a range of challenges associated with this enterprise, including the selection of team members, negotiating a consensus view of the research problem, prototyping and refining models, the role of sensitivity analysis, and the importance of team communication. These heuristics arose from a comparison of our experiences with several interdisciplinary modeling projects. We use one such experience—a project in which natural scientists, social scientists, and local residents came together to investigate the sustainability of small indigenous communities in the Arctic—to illustrate the heuristics. Received 27 April 2001; accepted 12 November 2001.     

Constraints on adaptation of Escherichia coli to mixed‐resource environments increase over time

Can a population evolved in two resources reach the same fitness in both as specialist populations evolved in each of the individual resources? This question is central to theories of ecological specialization, the maintenance of genetic variation, and sympatric speciation, yet relatively few experiments have examined costs of generalism over long‐term adaptation. We tested whether selection in environments containing two resources limits a population's ability to adapt to the individual resources by comparing the fitness of replicate Escherichia coli populations evolved for 6000 generations in the presence of glucose or lactose alone (specialists), or in varying presentations of glucose and lactose together (generalists). We found that all populations had significant fitness increases in both resources, though the magnitude and rate of these increases differed. For the first 4000 generations, most generalist populations increased in fitness as quickly in the individual resources as the corresponding specialist populations. From 5000 generations, however, a widespread cost of adaptation affected all generalists, indicating a growing constraint on their abilities to adapt to two resources simultaneously. Our results indicate that costs of generalism are prevalent, but may influence evolutionary trajectories only after a period of cost‐free adaptation.     

Many Possible Worlds: Expanding the Ecological Scenarios in Experimental Evolution

Experimental microbial evolution has focused on the particular ecological scenario where a population is placed suddenly in an environment where its fitness is low, and then adapts while the environment remains stable. In line with this, most microbial evolution studies use fitness measures that report how evolved genotypes fare when competed directly against their own distant ancestor while other studies compare life history traits (such as growth rates) of ancestral and evolved genotypes. This standard way of measuring and reporting changes in fitness has resulted in a consistent body of literature that explains adaptation when populations evolve in this “standard ecological scenario.” Here, I suggest that for experimental evolution to investigate adaptation in other ecological scenarios, such as fluctuating or persistently changing environments, measures of fitness must be expanded such that they not only continue to be comparable between experiments, but also account for evolution and demographic effects in all environments that an evolving lineage experiences. I examine two non-standard measures of fitness—fitness flux and the total number of reproductive events—as potential ways to quantify adaptation by integrating historical information about selection over many environments. This approach could allow us to make quantitative and biologically-meaningful comparisons of adaptation across diverse ecological scenarios. I use the case study of understanding how phytoplankton communities may respond to global change, where environmental variables change continuously, to explore concrete ways of using non-standard fitness measures that consider both demographic effects and selection in changing, rather than in changed, environments.     

Divergent adaptation promotes reproductive isolation among experimental populations of the filamentous fungus <Emphasis Type="Italic">Neurospora</Emphasis>

Background  

An open, focal issue in evolutionary biology is how reproductive isolation and speciation are initiated; elucidation of mechanisms with empirical evidence has lagged behind theory. Under ecological speciation, reproductive isolation between populations is predicted to evolve incidentally as a by-product of adaptation to divergent environments. The increased genetic diversity associated with interspecific hybridization has also been theorized to promote the development of reproductive isolation among independent populations. Using the fungal model Neurospora, we founded experimental lineages from both intra- and interspecific crosses, and evolved them in one of two sub-optimal, selective environments. We then measured the influence that initial genetic diversity and the direction of selection (parallel versus divergent) had on the evolution of reproductive isolation.     

Assessing predation risk: optimal behaviour and rules of thumb

We look at a simple model in which an animal makes behavioural decisions over time in an environment in which all parameters are known to the animal except predation risk. In the model there is a trade-off between gaining information about predation risk and anti-predator behaviour. All predator attacks lead to death for the prey, so that the prey learns about predation risk by virtue of the fact that it is still alive. We show that it is not usually optimal to behave as if the current unbiased estimate of the predation risk is its true value. We consider two different ways to model reproduction; in the first scenario the animal reproduces throughout its life until it dies, and in the second scenario expected reproductive success depends on the level of energy reserves the animal has gained by some point in time. For both of these scenarios we find results on the form of the optimal strategy and give numerical examples which compare optimal behaviour with behaviour under simple rules of thumb. The numerical examples suggest that the value of the optimal strategy over the rules of thumb is greatest when there is little current information about predation risk, learning is not too costly in terms of predation, and it is energetically advantageous to learn about predation. We find that for the model and parameters investigated, a very simple rule of thumb such as 'use the best constant control' performs well.     

Biologically inspired strategy for programmed assembly of viral building blocks with controlled dimensions

Facile fabrication of building blocks with precisely controlled dimensions is imperative in the development of functional devices and materials. We demonstrate the assembly of nanoscale viral building blocks of controlled lengths using a biologically motivated strategy. To achieve this we exploit the simple self-assembly mechanism of Tobacco mosaic virus (TMV), whose length is solely governed by the length of its genomic mRNA. We synthesize viral mRNA of desired lengths using simple molecular biology techniques, and in vitro assemble the mRNA with viral coat proteins to yield viral building blocks of controlled lengths. The results indicate that the assembly of the viral building blocks is consistent and reproducible, and can be readily extended to assemble building blocks with genetically modified coat proteins (TMV1cys). Additionally, we confirm the potential utility of the TMV1cys viral building blocks with controlled dimensions via covalent and quantitative conjugation of fluorescent markers. We envision that our biologically inspired assembly strategy to design and construct viral building blocks of controlled dimensions could be employed to fabricate well-controlled nanoarchitectures and hybrid nanomaterials for a wide variety of applications including nanoelectronics and nanocatalysis.     

The cell and developmental biology of alkaloid biosynthesis

Plants produce unique natural products as a result of gene mutation and subsequent adaptation of metabolic pathways to create new secondary metabolites. However, their biosynthesis and accumulation remains remarkably under the control of the biotic and abiotic environments. Alkaloid biosynthesis, which requires the adaptation of cellular activities to perform specialized metabolism without compromising general homeostasis, is accomplished by restricting product biosynthesis and accumulation to particular cells and to defined times of plant development. The cell and developmental biology of alkaloid biosynthesis, which is remarkably complex, evolved in part by recruiting pre-existing enzymes to perform new functions.     

Renewal ecology: conservation for the Anthropocene

The global scale and rapidity of environmental change is challenging ecologists to reimagine their theoretical principles and management practices. Increasingly, historical ecological conditions are inadequate targets for restoration ecology, geographically circumscribed nature reserves are incapable of protecting all biodiversity, and the precautionary principle applied to management interventions no longer ensures avoidance of ecological harm. In addition, human responses to global environmental changes, such as migration, building of protective infrastructures, and land use change, are having their own negative environmental impacts. We use examples from wildlands, urban, and degraded environments, as well as marine and freshwater ecosystems, to show that human adaptation responses to rapid ecological change can be explicitly designed to benefit biodiversity. This approach, which we call “renewal ecology,” is based on acceptance that environmental change will have transformative effects on coupled human and natural systems and recognizes the need to harmonize biodiversity with human infrastructure, for the benefit of both.     

Social intelligence in the spotted hyena (Crocuta crocuta)

If the large brains and great intelligence characteristic of primates were favoured by selection pressures associated with life in complex societies, then cognitive abilities and nervous systems with primate-like attributes should have evolved convergently in non-primate mammals living in large, elaborate societies in which social dexterity enhances individual fitness. The societies of spotted hyenas are remarkably like those of cercopithecine primates with respect to size, structure and patterns of competition and cooperation. These similarities set an ideal stage for comparative analysis of social intelligence and nervous system organization. As in cercopithecine primates, spotted hyenas use multiple sensory modalities to recognize their kin and other conspecifics as individuals, they recognize third-party kin and rank relationships among their clan mates, and they use this knowledge adaptively during social decision making. However, hyenas appear to rely more intensively than primates on social facilitation and simple rules of thumb in social decision making. No evidence to date suggests that hyenas are capable of true imitation. Finally, it appears that the gross anatomy of the brain in spotted hyenas might resemble that in primates with respect to expansion of frontal cortex, presumed to be involved in the mediation of social behaviour.     

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

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

Shedding light on the evolution of plasticity in natural populations

Plasticity allows for changes in phenotype in response to environmental cues, often facilitating local adaptation to seasonal environments. Phenotypic plasticity alone, however, may not always be sufficient to ensure adaptation to new localities. In particular, changing cues associated with shifting seasonal regimes may no longer induce appropriate phenotypic responses in new environments ( Nicotra et al. 2010 ). Plastic responses must thus evolve to avoid being maladaptive. To date, the extent to which plastic responses can change and the genetic mechanisms by which this can happen have remained elusive. In this issue of Molecular Ecology, Blackman et al. (2011a) harness natural variation in flowering time among populations of the wild sunflower, Helianthus annuus, to demonstrate that plasticity has indeed evolved in this species. Remarkably, they are able to detect changes in gene expression that are associated with both a loss of plasticity and a reversal of the plastic response. These changes occur in two separate, but integrated, regulatory pathways controlling the transition to flowering, suggesting that complex regulatory networks that incorporate multiple environmental and developmental cues may facilitate the evolution of plastic responses. This study leverages knowledge from plant genetic models to provide a surprising level of insight into the evolution of an adaptive trait in a non‐model species. Through discoveries of the roles of gene duplication and network modularity in the evolution of plastic responses, the study raises questions about the degree to which species‐specific network architectures may act as a constraint to the potential of adaptation.     

Synthetic biology with RNA: progress report

One of the long-term goals in synthetic biology is the construction of large-scale gene networks to control and manipulate cells. Such networks often tweak natural regulatory mechanisms, or 'switches', in order to achieve the desired function. Regulatory mechanisms that involve RNA building blocks such as messenger RNA, microRNA and riboswitches have become increasingly prominent in this regard. Recent achievements include prototype mRNA sensors, logic circuits that respond to small molecule cues to affect cell fate, and cell-state classifier networks that identify physiological states using multiple microRNA inputs. This Review describes these and other results in RNA-based synthetic biology.     

Natural hybridization and conservation

This review deals with natural hybridization, an important subject in conservation biology. Natural hybridization is defined as the secondary contact between two populations that have evolved separately over a long period of time. This process is uncommon in terms of the total number of individuals involved, but is much less unusual if we consider the number of species that hybridize. Thus, natural hybridization may be an important process in the shaping of the evolutionary trajectories of many plant and animal species. The possible consequences of natural hybridization, which can either promote or prevent evolutionary divergence between taxa and will involve many ecological factors, are analysed here. I question whether natural hybridization poses always a problem in conservation and try to answer when conservation biologists and managers do have a responsibility to take decisions. Several examples of hybridization related to management strategies are also discussed. In conclusion, I believe that it is impossible to provide conservation managers with a simple handbook explaining how to proceed in cases of hybridization––each case is unique and should be analyzed individually. The only advice is that the more we know about hybridization and the factors involved, the better we will be able to assess each situation, to establish the possible consequences and even to estimate the probability of success of any particular conservation strategy.