Toward improved conservation management: a consideration of sensory ecology

All organisms rely on sensory systems to obtain, interpret, and respond to information available in their environment. With rapid alterations of ecosystems occurring across the globe, organisms are being faced with sensory challenges that result in behavioural changes and disruptions with potential population-level consequences. Through a consideration of sensory ecology, it is possible to identify the underlying causes of disturbances at the individual level and use this information to develop better-informed, highly targeted, and more effective management strategies. Indeed, sensory-based approaches have already been successful in response to a variety of conservation issues. This article provides a general discussion of how a consideration of sensory ecology can benefit conservation biology and proceeds to describe three areas of rapid growth and potential for expansion: (1) mitigation of anthropogenic noise disturbance; (2) prevention and amelioration of ecological and other evolutionary traps; (3) targeted population control with special attention to aquatic invasive species. I conclude with general recommendations on how sensory ecologists and conservation biologists can mutually benefit from integrated endeavours.     

Multicellular organization in bacteria as a target for drug therapy

Antibiotic treatments are now reaching the limit of their efficiency, especially in hospitals where certain bacteria are resistant to all available drugs. The development of new drugs against which resistance would be slower to evolve is an important challenge. Recent advances have shown that a potential strategy is to target global properties of infections instead of harming each individual bacterium. Consider an analogy with multicellular organisms. In order to kill an animal two strategies are possible. One can kill each of its cells individually. This is what antibiotics do to get rid of bacterial infections. An alternate way, for instance, is to disorganize the hormonal system of animal's body, leading eventually to its death. This second strategy could also be employed against infections, in place of antibiotics. Bacteria are indeed often involved into coordinated activities within a group, and certain drugs are able to disorganize these activities by blocking bacterial communication. In other words, these drugs are able to target infections as a whole, rather than individuals within infections. The present paper aims at analysing the consequence of this peculiarity on the evolution of bacterial resistance. We use a mathematical model, based on branching process, to calculate the fixation probability of a mutant resistant to this type of drug, and finally to predict the speed of resistance evolution. We show that this evolution is several orders of magnitude slower than in the case of antibiotic resistance. The explanation is as follows. By targeting treatments against adaptive properties of groups instead of individuals, we shift one level up the relevant unit of organization generating resistance. Instead of facing billions of bacteria with a very rapid evolutionary rate, these alternate treatments face a reduced number of larger organisms with lower evolutionary potential. In conclusion, this result leads us to emphasize the strong potential of anti‐bacterial treatments aiming at disorganizing social traits of microbes rather than at killing every individual.     

以发育模块重复征用和整合为基础的进化创新机制

进化新征的起源和分化是进化发育生物学研究的核心问题。通过对多细胞生物早期发育调控机制的比较分析,发现亲缘关系较远的生物所共有的一些形态特征受保守的发育调控程序调节（深同源性）。许多创新性状的发生是基于对预先存在的基因或发育调控模块的重复利用和整合。发育基因调控网络在结构和功能上高度模块化,因此不仅可以通过模块拆分和重复征用改变发育程式,而且也增强了调控网络自身的进化力。研究基因调控网络和发育系统的进化动态将有助于更深入地认识生物演化过程中创新性状发生和表型进化的分子机制。     

Ecological aspects of the evolutionary processes

Darwin in his On the Origin of species made it clear that evolutionary change depends on the combined action of two different causes, the first being the origin of genetically based phenotypic variation in the individual organisms comprising the population and the second being the action of selective agents of the external environment placing demands on the individual organisms. For over a century following Darwin, most evolutionists focused on the origin of inherited variation and its transmission; many workers continue to regard genetics to be the core of evolutionary theory. Far less attention has been given to the exact nature of the selective agents with most evolutionists still treating this cause imprecisely to the detriment of our understanding of both nomological and historical evolutionary theory. Darwin was vague in the meaning of his new concept of "Natural Selection," using it interchangeably as one of the causes for evolutionary change and as the final outcome (= evolutionary change). In 1930, natural selection was defined clearly as "non-random, differential reproduction of genes" by R. Fisher and J.B.S. Haldane which is a statement of the outcome of evolutionary process and which omits mention of the causes bringing about this change. Evolutionists quickly accepted this outcome definition of natural selection, and have used interchangeably selection both as a cause and as the result of evolutionary change, causing great confusion. Herein, the details will be discussed of how the external environment (i.e., the environment-phenotype interaction) serves as selective agents and exerts demands on the phenotypic organisms. Included are the concepts of fitness and of the components of fitness (= adaptations) which are respectively (a) survival, (b) direct reproductive and (c) indirect reproductive features. Finally, it will be argued that historical-narrative analyses of organisms, including classification and phylogenetic history, are possible only with a full understanding of nomological evolutionary theory and with functional/adaptive studies of the employed taxonomic features in addition to the standard comparative investigations.     

The evolutionary ecology of individual phenotypic plasticity in wild populations

The ability of individual organisms to alter morphological and life-history traits in response to the conditions they experience is an example of phenotypic plasticity which is fundamental to any population's ability to deal with short-term environmental change. We currently know little about the prevalence, and evolutionary and ecological causes and consequences of variation in life history plasticity in the wild. Here we outline an analytical framework, utilizing the reaction norm concept and random regression statistical models, to assess the between-individual variation in life history plasticity that may underlie population level responses to the environment at both phenotypic and genetic levels. We discuss applications of this framework to date in wild vertebrate populations, and illustrate how natural selection and ecological constraint may alter a population's response to the environment through their effects at the individual level. Finally, we present future directions and challenges for research into individual plasticity.     

Individuality in seaweeds and why we need to care

Documenting the causes and consequences of intraspecific variation forms the foundation of much of evolutionary ecology. In this Perspectives piece, we review the importance of individual variation in ecology and evolution, argue that contemporary phycology often overlooks this foundational biological unit, and highlight how this lack of attention has potentially constrained our understanding of seaweeds. We then provide some suggestions of promising but underrepresented approaches, for instance: conducting more studies and analyses at the level of the individual; designing studies to evaluate heritability and genetic regulation of traits; and measuring associations between individual variation in functional traits and ecological outcomes. We close by highlighting areas of phycological research (e.g., population biology, ecology, aquaculture, climate change management) that could benefit immediately from including a focus on individual variation. Algae, for their part, provide us with a powerful and diverse set of ecological and evolutionary traits to explore these topics. There is much to be discovered.     

Evolutionary dynamics of pathogen resistance and tolerance

Abstract.— Host organisms can respond to the threat of disease either through resistance defenses (which inhibit or limit infection) or through tolerance strategies (which do not limit infection, but reduce or offset its fitness consequences). Here we show that resistance and tolerance can have fundamentally different evolutionary outcomes, even when they have equivalent short-term benefit for the host. As a gene conferring disease resistance spreads through a population, the incidence of infection declines, reducing the fitness advantage of carrying the resistance gene. Thus genes conferring complete resistance cannot become fixed (i.e., universal) by selection in a host population, and diseases cannot be eliminated solely by natural selection for host resistance. By contrast, as a gene conferring disease tolerance spreads through a population, disease incidence rises, increasing the evolutionary advantage of carrying the tolerance gene. Therefore, any tolerance gene that can invade a host population will tend to be driven to fixation by selection. As predicted, field studies of diverse plant species infected by rust fungi confirm that resistance traits tend to be polymorphic and tolerance traits tend to be fixed. These observations suggest a new mechanism for the evolution of mutualism from parasitism, and they help to explain the ubiquity of disease.     

Tolerance traits and the stability of mutualism

Identifying factors which allow the evolution and persistence of cooperative interactions between species is a fundamental issue in evolutionary ecology. Various hypotheses have been suggested which generally focus on mechanisms that allow cooperative genotypes in different species to maintain interactions over space and time. Here, we emphasise the fact that even within mutualisms (interactions with net positive fitness effects for both partners), there may still be inherent costs, such as the occasional predation by ants upon aphids. Individuals engaged in mutualisms benefit from minimising these costs as long as it is not at the expense of breaking the interspecific interaction, which offers a net positive benefit. The most common and obvious defence traits to minimise interspecific interaction costs are resistance traits, which act to reduce encounter rate between two organisms. Tolerance traits, in contrast, minimise fitness costs to the actor, but without reducing encounter rate. Given that, by definition, it is beneficial to remain in mutualistic interactions, the only viable traits to minimise costs are tolerance-based 'defence' strategies. Thus, we propose that tolerance traits are an important factor promoting stability in mutualisms. Furthermore, because resistance traits tend to propagate coevolutionary arms races between antagonists, whilst tolerance traits do not, we also suggest that tolerance-based defence strategies may be important in facilitating the transition from antagonistic interactions into mutualisms. For example, the mutualism between ants and aphids has been suggested to have evolved from parasitism. We describe how phenotypic plasticity in honeydew production may be a tolerance trait that has prevented escalation into an antagonistic arms race and instead led to mutualistic coevolution.     

HOW TO MEASURE INDIRECT GENETIC EFFECTS: THE CONGRUENCE OF TRAIT-BASED AND VARIANCE-PARTITIONING APPROACHES

Indirect genetic effects (IGEs), which occur when phenotypic expression in one individual is influenced by genes in another conspecific individual, may have a drastic effect on evolutionary response to selection. General evolutionary models of IGEs have been developed using two distinct theoretical frameworks derived from maternal effects theory. The first framework is trait-based and focuses on how phenotypes are influenced by specific traits in a social partner, with the strength of interactions defined by the matrix Ψ. The second framework partitions total genetic variance into components representing direct effects, indirect effects, and the covariance between them, without identifying specific social traits responsible for IGEs. The latter framework has been employed more commonly by empiricists because the methods for estimating variance components are relatively straightforward. Here, we show how these two theoretical frameworks are related to each other and derive equations that can be used to translate between them. This translation leads to a generalized method that can be used to estimate Ψ via standard quantitative genetic breeding designs or pedigrees from natural populations. This method can be used in a very general set of circumstances and is widely applicable to all IGEs, including maternal effects and other interactions among relatives.     

INTERPRETING REJECTIONS OF THE BENEFICIAL ACCLIMATION HYPOTHESIS: WHEN IS PHYSIOLOGICAL PLASTICITY ADAPTIVE?

Abstract.— Although many studies testing the beneficial acclimation hypothesis have rejected it, what these rejections imply about the adaptive value of physiological change remains unclear. Uncertainty arises because the hypothesis focuses on the relative performance of organisms exposed to one environment versus another, whereas the raw material available to evolution is variation in acclimation responses of individual traits. This mismatch is problematic when organisms are exposed to poor environments. In poor environments, the adaptive or maladaptive value of changes in individual traits may be obscured by long-term decrements in organismal condition. A better match between the evolutionary pressures shaping acclimation and the tests used to examine them can be achieved by focusing on the fitness consequences of acclimation changes in individual traits.     

VARIATION IN SEED CHARACTERS IN NEMOPHILA MENZIESII: EVIDENCE OF A GENETIC BASIS FOR MATERNAL EFFECT

A growing body of evidence indicates that phenotypic selection on juvenile traits of both plants and animals may be considerable. Because juvenile traits are typically subject to maternal effects and often have low heritabilities, adaptive responses to natural selection on these traits may seem unlikely. To determine the potential for evolutionary response to selection on juvenile traits of Nemophila menziesii (Hydrophyllaceae), we conducted two quantitative genetic studies. A reciprocal factorial cross, involving 16 parents and 1960 progeny, demonstrated a significant maternal component of variance in seed mass and additive genetic component of variance in germination time. This experiment also suggested that interaction between parents, though small, provides highly significant contributions to the variance of both traits. Such a parental interaction could arise by diverse mechanisms, including dependence of nuclear gene expression on cytoplasmic genotype, but the design of this experiment could not distinguish this from other possible causes, such as effects on progeny phenotype of interaction between the environmental conditions of both parents. The second experiment, spanning three generations with over 11,000 observations, was designed for investigation of the additive genetic variance in maternal effect, assessment of paternal effects, as well as further partitioning of the parental interaction identified in the reciprocal factorial experiment. It yielded no consistent evidence of paternal effects on seed mass, nor of parental interactions. Our inference of such interaction effects from the first experiment was evidently an artifact of failing to account for the substantial variance among fruits within crosses. The maternal effect was found to have a large additive genetic component, accounting for at least 20% of the variation in individual seed mass. This result suggests that there is appreciable potential for response to selection on seed mass through evolution of the maternal effect. We discuss aspects that may nevertheless limit response to individual selection on seed mass, including trade-offs between the size of individual seeds and germination time and between the number of seeds a maternal plant can mature and their mean size.     

Inducible defence and the social evolution of herd immunity.

Many organisms vary their level of investment in defensive characters. Protective traits may be induced upon exposure to predators or parasites. In a similar way, humans vaccinate in response to threatening epidemics. When most group members defend themselves, epidemics die out quickly because parasites cannot spread. A high level of group (herd) immunity is therefore beneficial to the group. There is, however, a well-known divergence between the optimum degree of induction for selfish individuals and the level of induction that maximizes group benefit. I develop two optimality models for the frequency of induction. The first model shows that higher relatedness favours more induction and a smaller difference between selfish and cooperative optima. The second model assumes variation in the vigour of individuals and therefore differences in the relative cost for induction. The model predicts that strong individuals induce more easily than weak individuals. Small differences in vigour cause a large divergence in the optimal levels of induction for strong and weak individuals. The concept of genetic relatedness in an evolutionary model is analogous to correlated interests and correlated strategies in an economic model of human behaviour. The evolutionary models presented here therefore provide a basis for further study of human vaccination.     

A case for evolutionary genomics and the comprehensive examination of sequence biodiversity

Comparative analysis is one of the most powerful methods available for understanding the diverse and complex systems found in biology, but it is often limited by a lack of comprehensive taxonomic sampling. Despite the recent development of powerful genome technologies capable of producing sequence data in large quantities (witness the recently completed first draft of the human genome), there has been relatively little change in how evolutionary studies are conducted. The application of genomic methods to evolutionary biology is a challenge, in part because gene segments from different organisms are manipulated separately, requiring individual purification, cloning, and sequencing. We suggest that a feasible approach to collecting genome-scale data sets for evolutionary biology (i.e., evolutionary genomics) may consist of combination of DNA samples prior to cloning and sequencing, followed by computational reconstruction of the original sequences. This approach will allow the full benefit of automated protocols developed by genome projects to be realized; taxon sampling levels can easily increase to thousands for targeted genomes and genomic regions. Sequence diversity at this level will dramatically improve the quality and accuracy of phylogenetic inference, as well as the accuracy and resolution of comparative evolutionary studies. In particular, it will be possible to make accurate estimates of normal evolution in the context of constant structural and functional constraints (i.e., site-specific substitution probabilities), along with accurate estimates of changes in evolutionary patterns, including pairwise coevolution between sites, adaptive bursts, and changes in selective constraints. These estimates can then be used to understand and predict the effects of protein structure and function on sequence evolution and to predict unknown details of protein structure, function, and functional divergence. In order to demonstrate the practicality of these ideas and the potential benefit for functional genomic analysis, we describe a pilot project we are conducting to simultaneously sequence large numbers of vertebrate mitochondrial genomes.     

Adaptive developmental plasticity: Compartmentalized responses to environmental cues and to corresponding internal signals provide phenotypic flexibility

Background

The environmental regulation of development can result in the production of distinct phenotypes from the same genotype and provide the means for organisms to cope with environmental heterogeneity. The effect of the environment on developmental outcomes is typically mediated by hormonal signals which convey information about external cues to the developing tissues. While such plasticity is a wide-spread property of development, not all developing tissues are equally plastic. To understand how organisms integrate environmental input into coherent adult phenotypes, we must know how different body parts respond, independently or in concert, to external cues and to the corresponding internal signals.

Results

We quantified the effect of temperature and ecdysone hormone manipulations on post-growth tissue patterning in an experimental model of adaptive developmental plasticity, the butterfly Bicyclus anynana. Following a suite of traits evolving by natural or sexual selection, we found that different groups of cells within the same tissue have sensitivities and patterns of response that are surprisingly distinct for the external environmental cue and for the internal hormonal signal. All but those wing traits presumably involved in mate choice responded to developmental temperature and, of those, all but the wing traits not exposed to predators responded to hormone manipulations. On the other hand, while patterns of significant response to temperature contrasted traits on autonomously-developing wings, significant response to hormone manipulations contrasted neighboring groups of cells with distinct color fates. We also showed that the spatial compartmentalization of these responses cannot be explained by the spatial or temporal compartmentalization of the hormone receptor protein.

Conclusions

Our results unravel the integration of different aspects of the adult phenotype into developmental and functional units which both reflect and impact evolutionary change. Importantly, our findings underscore the complexity of the interactions between environment and physiology in shaping the development of different body parts.

     

Impacts of sublethal insecticide exposure on insects — Facts and knowledge gaps

The biodiversity and biomass of insects is dramatically declining due to various anthropogenic factors. One of these factors is the use of insecticides to protect plants from pests. However, apart from the targeted pest insects, thousands of non-target organisms face traces of insecticides that are not lethal but can affect numerous traits of the individual, including development, physiology, behaviour and communication. In the present review, key facts on impacts of sublethal insecticide exposure on such traits are summarised. Attributable to various abiotic and biotic processes, insecticide concentrations may become sublethal in space and time. Nevertheless, these concentrations impede insect development, reducing growth and survival, but sometimes also enhance reproductive performance. The effects are species-specific, but sensitivity also differs within species depending on the developmental stage, sex and population. Furthermore, insecticide exposure influences several immunity pathways and causes changes in behaviour. Such changes are mostly studied on the level of behavioural traits. However, also effects on the consistency of overall individual behavioural phenotypes, i.e. personalities, should be investigated, which have consequences on individual fitness and on the effectiveness of biocontrol agents. Moreover, insecticides can act as info-disruptors, impeding signal production and perception during chemical communication at various levels. Finally, microbial symbionts may modify insect responses to insecticides, being of particular interest for biotechnological approaches. Here, methodological issues are discussed and knowledge gaps and potential future research directions are highlighted. Understanding the mechanisms of dose-dependent insecticide impacts on organisms and their cascading effects on higher levels of biological organisation and on subsequent generations are of utmost importance for proper insecticide use.     

Evolutionary adaptation to environmental stressors: a common response at the proteomic level

Mechanistic trade‐offs between traits under selection can shape and constrain evolutionary adaptation to environmental stressors. However, our knowledge of the quantitative and qualitative overlap in the molecular machinery among stress tolerance traits is highly restricted by the challenges of comparing and interpreting data between separate studies and laboratories, as well as to extrapolating between different levels of biological organization. We investigated the expression of the constitutive proteome (833 proteins) of 35 Drosophila melanogaster replicate populations artificially selected for increased resistance to six different environmental stressors. The evolved proteomes were significantly differentiated from replicated control lines. A targeted analysis of the constitutive proteomes revealed a regime‐specific selection response among heat‐shock proteins, which provides evidence that selection also adjusts the constitutive expression of these molecular chaperones. Although the selection response in some proteins was regime specific, the results were dominated by evidence for a “common stress response.” With the exception of high temperature survival, we found no evidence for negative correlations between environmental stress resistance traits, meaning that evolutionary adaptation is not constrained by mechanistic trade‐offs in regulation of functional important proteins. Instead, standing genetic variation and genetic trade‐offs outside regulatory domains likely constrain the evolutionary responses in natural populations.     

Synergies and trade-offs between insect and pathogen resistance in maize leaves and roots

Determining links between plant defence strategies is important to understand plant evolution and to optimize crop breeding strategies. Although several examples of synergies and trade-offs between defence traits are known for plants that are under attack by multiple organisms, few studies have attempted to measure correlations of defensive strategies using specific single attackers. Such links are hard to detect in natural populations because they are inherently confounded by the evolutionary history of different ecotypes. We therefore used a range of 20 maize inbred lines with considerable differences in resistance traits to determine if correlations exist between leaf and root resistance against pathogens and insects. Aboveground resistance against insects was positively correlated with the plant's capacity to produce volatiles in response to insect attack. Resistance to herbivores and resistance to a pathogen, on the other hand, were negatively correlated. Our results also give first insights into the intraspecific variability of root volatiles release in maize and its positive correlation with leaf volatile production. We show that the breeding history of the different genotypes (dent versus flint) has influenced several defensive parameters. Taken together, our study demonstrates the importance of genetically determined synergies and trade-offs for plant resistance against insects and pathogens.     

QTL mapping and the genetic basis of adaptation: recent developments

Quantitative trait loci (QTL) mapping has been used in a number of evolutionary studies to study the genetic basis of adaptation by mapping individual QTL that explain the differences between differentiated populations and also estimating their effects and interaction in the mapping population. This analysis can provide clues about the evolutionary history of populations and causes of the population differentiation. QTL mapping analysis methods and associated computer programs provide us tools for such an inference on the genetic basis and architecture of quantitative trait variation in a mapping population. Current methods have the capability to separate and localize multiple QTL and estimate their effects and interaction on a quantitative trait. More recent methods have been targeted to provide a comprehensive inference on the overall genetic architecture of multiple traits in a number of environments. This development is important for evolutionary studies on the genetic basis of multiple trait variation, genotype by environment interaction, host–parasite interaction, and also microarray gene expression QTL analysis.     

Stochastic dynamics of leukemic cells under an intermittent targeted therapy

The evolutionary dynamics of cancerous cell populations in a model of Chronic Myeloid Leukemia (CML) is investigated in the presence of an intermittent targeted therapy. Cancer development and progression is modeled by simulating the stochastic evolution of initially healthy cells which can experience genetic mutations and modify their reproductive behavior, becoming leukemic clones. Front line therapy for the treatment of patients affected by CML is based on the administration of tyrosine kinase inhibitors, namely imatinib (Gleevec) or, more recently, dasatinib or nilotinib. Despite the fact that they represent the first example of a successful molecular targeted therapy, the development of resistance to these drugs is observed in a proportion of patients, especially those in advanced stages. In this study, we simulate an imatinib-like treatment of CML by modifying the fitness and the death rate of cancerous cells and describe the several scenarios in the evolutionary dynamics of white blood cells as a consequence of the efficacy of the different modeled therapies. The patient response to the therapy is investigated by simulating a drug administration following a continuous or pulsed time scheduling. A permanent disappearance of leukemic clones is achieved with a continuous therapy. This theoretical behavior is in a good agreement with that observed in previous clinical investigations. However, these findings demonstrate that an intermittent therapy could represent a valid alternative in patients with high risk of toxicity. A suitable tuned pulsed therapy can also reduce the probability of developing resistance.     

Co-niche construction between hosts and symbionts: ideas and evidence

Symbiosis is a process that can generate evolutionary novelties and can extend the phenotypic niche space of organisms. Symbionts can act together with their hosts to co-construct host organs, within which symbionts are housed. Once established within hosts, symbionts can also influence various aspects of host phenotype, such as resource acquisition, protection from predation by acquisition of toxicity, as well as behaviour. Once symbiosis is established, its fidelity between generations must be ensured. Hosts evolve various mechanisms to screen unwanted symbionts and to facilitate faithful transmission of mutualistic partners between generations. Microbes are the most important symbionts that have influenced plant and animal phenotypes; multicellular organisms engage in developmental symbioses with microbes at many stages in ontogeny. The co-construction of niches may result in composite organisms that are physically nested within each other. While it has been advocated that these composite organisms need new evolutionary theories and perspectives to describe their properties and evolutionary trajectories, it appears that standard evolutionary theories are adequate to explore selection pressures on their composite or individual traits. Recent advances in our understanding of composite organisms open up many important questions regarding the stability and transmission of these units.