Applying population-genetic models in theoretical evolutionary epidemiology

Much of the existing theory for the evolutionary biology of infectious diseases uses an invasion analysis approach. In this Ideas and Perspectives article, we suggest that techniques from theoretical population genetics can also be profitably used to study the evolutionary epidemiology of infectious diseases. We highlight four ways in which population-genetic models provide benefits beyond those provided by most invasion analyses: (i) they can make predictions about the rate of pathogen evolution; (ii) they explicitly draw out the mechanistic way in which the epidemiological dynamics feed into evolutionary change, and thereby provide new insights into pathogen evolution; (iii) they can make predictions about the evolutionary consequences of non-equilibrium epidemiological dynamics; (iv) they can readily incorporate the effects of multiple host dynamics, and thereby account for phenomena such as immunological history and/or host co-evolution.     

Exploring the hidden landscape of female preferences for complex signals

A major challenge in evolutionary biology is explaining the origins of complex phenotypic diversity. In animal communication, complex signals may evolve from simpler signals because novel signal elements exploit preexisting biases in receivers’ sensory systems. Investigating the shape of female preference functions for novel signal characteristics is a powerful, but underutilized, method to describe the adaptive landscape potentially guiding complex signal evolution. We measured female preference functions for characteristics of acoustic appendages added to male calling songs in the grasshopper Chorthippus biguttulus, which naturally produces only simple songs. We discovered both hidden preferences for and biases against novel complex songs, and identified rules governing song attractiveness based on multiple characteristics of both the base song and appendage. The appendage's temporal position and duration were especially important: long appendages preceding the song often made songs less attractive, while following appendages were neutral or weakly attractive. Appendages had stronger effects on songs of shorter duration, but did not restore the attractiveness of very unattractive songs. We conclude that sensory biases favor, within predictable limits, the evolution of complex songs in grasshoppers. The function‐valued approach is an important tool in determining the generality of these limits in other taxa and signaling modalities.     

Behavioral drive versus behavioral inertia in evolution: a null model approach

Some biologists embrace the classical view that changes in behavior inevitably initiate or drive evolutionary changes in other traits, yet others note that behavior sometimes inhibits evolutionary changes. Here we develop a null model that quantifies the impact of regulatory behaviors (specifically, thermoregulatory behaviors) on body temperature and on performance of ectotherms. We apply the model to data on a lizard (Anolis cristatellus) and show that thermoregulatory behaviors likely inhibit selection for evolutionary shifts in thermal physiology with altitude. Because behavioral adjustments are commonly used by ectotherms to regulate physiological performance, regulatory behaviors should generally constrain rather than drive evolution, a phenomenon we call the "Bogert effect." We briefly review a few other examples that contradict the classical view of behavior as the inevitable driving force in evolution. Overall, our analysis and brief review challenge the classical view that behavior is invariably the driving force in evolution, and instead our work supports the alternative view that behavior has diverse--and sometimes conflicting--effects on the directions and rates at which other traits evolve.     

Artificial evolution of life history and behavior

We present an individual-based model that uses artificial evolution to predict fit behavior and life-history traits on the basis of environmental data and organism physiology. Our main purpose is to investigate whether artificial evolution is a suitable tool for studying life history and behavior of real biological organisms. The evolutionary adaptation is founded on a genetic algorithm that searches for improved solutions to the traits under scrutiny. From the genetic algorithm's "genetic code," behavior is determined using an artificial neural network. The marine planktivorous fish Müller's pearlside (Maurolicus muelleri) is used as the model organism because of the broad knowledge of its behavior and life history, by which the model's performance is evaluated. The model adapts three traits: habitat choice, energy allocation, and spawning strategy. We present one simulation with, and one without, stochastic juvenile survival. Spawning pattern, longevity, and energy allocation are the life-history traits most affected by stochastic juvenile survival. Predicted behavior is in good agreement with field observations and with previous modeling results, validating the usefulness of the presented model in particular and artificial evolution in ecological modeling in general. The advantages, possibilities, and limitations of this modeling approach are further discussed.     

A novel meta‐analytical approach to improve systematic review of rates and patterns of microevolution

A classic topic in ecology and evolution, phenotypic microevolution of quantitative traits has received renewed attention in the face of rapid global environmental change. However, for plants, synthesis has been hampered by the limited use of standard metrics, which makes it difficult to systematize empirical information. Here we demonstrate the advantages of incorporating meta‐analysis tools to the review of microevolutionary rates. We perform a systematic survey of the plant literature on microevolution of quantitative traits over known periods of time, based on the scopus database. We quantify the amount of change by standard mean difference and develop a set of effect sizes to analyze such data. We show that applying meta‐analysis tools to a systematic literature review allows the extraction of a much larger volume of information than directly calculating microevolutionary rates. We also propose derived meta‐analysis effect sizes (h, LG and LR) which are appropriate for the study of evolutionary patterns, the first being similar to haldanes, the second and third allowing the application of a preexisting analytical framework for the inference of evolutionary mechanisms. This novel methodological development is applicable to the study of microevolution in any taxa. To pilot test it, we built an open‐access database of 1,711 microevolutionary rates of 152 angiosperm species from 128 studies documenting population changes in quantitative traits following an environmental novelty with a known elapsed time (<260 years). The performance of the metrics proposed (h, LG and LR) is similar to that of preexisting ones, and at the same time they bring the advantages of lower estimation bias and higher number of usable observations typical of meta‐analysis.     

The effect of historical legacy on adaptation: do closely related species respond to the environment in the same way?

The many documented examples of parallel and convergent evolution in similar environments are strong evidence for the role of natural selection in the evolution of trait variation. However, species may respond to selection in different ways; idiosyncrasies of their evolutionary history may affect how different species respond to the same selective pressure. To determine whether evolutionary history affects trait-environment associations in a recently diverged lineage, we investigated within-species trait-environment associations in the white proteas, a closely related monophyletic group. We first used manovas to determine the relative importance of shared response to selection, evolutionary history and unique responses to selection on trait variation. We found that on average, similar associations to the environment across species explained trait variation, but that the species had different mean trait values. We also detected species-specific associations of traits with the environmental gradients. To identify the traits associated uniquely with the environment, we used a structural equation model. Our analysis showed that the species differed in how their traits were associated with each of the environmental variables. Further, in the cases of two root traits (root mass and root length/mass ratio), two species differed in the direction of their associations (e.g. populations in one species had heavier roots in warmer areas, and populations in the other species had lighter roots in warmer areas). Our study shows that even in a closely related group of species, evolutionary history may have an effect on both the size and direction of adaptations to the environment.     

Robustness and evolution: concepts, insights and challenges from a developmental model system

Robustness, the persistence of an organismal trait under perturbations, is a ubiquitous property of complex living systems. We here discuss key concepts related to robustness with examples from vulva development in the nematode Caenorhabditis elegans. We emphasize the need to be clear about the perturbations a trait is (or is not) robust to. We discuss two prominent mechanistic causes of robustness, namely redundancy and distributed robustness. We also discuss possible evolutionary causes of robustness, one of which does not involve natural selection. To better understand robustness is of paramount importance for understanding organismal evolution. Part of the reason is that highly robust systems can accumulate cryptic variation that can serve as a source of new adaptations and evolutionary innovations. We point to some key challenges in improving our understanding of robustness.     

The importance of mechanisms for the evolution of cooperation

Studies aimed at explaining the evolution of phenotypic traits have often solely focused on fitness considerations, ignoring underlying mechanisms. In recent years, there has been an increasing call for integrating mechanistic perspectives in evolutionary considerations, but it is not clear whether and how mechanisms affect the course and outcome of evolution. To study this, we compare four mechanistic implementations of two well-studied models for the evolution of cooperation, the Iterated Prisoner''s Dilemma (IPD) game and the Iterated Snowdrift (ISD) game. Behavioural strategies are either implemented by a 1 : 1 genotype–phenotype mapping or by a simple neural network. Moreover, we consider two different scenarios for the effect of mutations. The same set of strategies is feasible in all four implementations, but the probability that a given strategy arises owing to mutation is largely dependent on the behavioural and genetic architecture. Our individual-based simulations show that this has major implications for the evolutionary outcome. In the ISD, different evolutionarily stable strategies are predominant in the four implementations, while in the IPD each implementation creates a characteristic dynamical pattern. As a consequence, the evolved average level of cooperation is also strongly dependent on the underlying mechanism. We argue that our findings are of general relevance for the evolution of social behaviour, pleading for the integration of a mechanistic perspective in models of social evolution.     

The causes of repeated genetic evolution

A general understanding of the evolutionary process is limited by the contingency of each evolutionary event, making it difficult, even retrospectively, to explain why things have unfolded the way they have. The repeated evolution of similar traits in organisms facing similar environmental conditions is a pervasive phenomenon, including for animal morphology, and is considered a strong evidence for adaptive evolution. Examples of repeated evolution of particular traits offer a unique opportunity to ask whether evolution has followed similar or different genetic paths. Case studies reveal that although multiple genetic paths were often possible to evolve a morphological trait, similar evolutionary trajectories have been followed repeatedly in independent lineages, suggesting that biases influence the course of genetic evolution. In the light of these examples we examine several factors influencing the genetic paths of adaptive evolution and in particular how the interplay between natural selection and genetic variations carves out predictable genetic trajectories of morphological evolution.     

New challenges in the study of the evolution of wild animals and their gut microbiome

In this viewpoint, by reviewing the recent findings on wild animals and their gut microbiomes, we found some potential new insights and challenges in the study of the evolution of wild animals and their gut microbiome. We suggested that wild animal gut microbiomes may come from microbiomes in the animals'' living habitats along with animals'' special behavior, and that the study of long‐term changes in gut microbiomes should consider both habitat and special behaviors. Also, host behavior would facilitate the gut microbiome transmission between individuals. We suggested that research should integrate the evolutionary history and physiological systems of wild animals to understand the evolution of animals and their gut microbiomes. Finally, we proposed the Noncultured‐Cultured‐Fermentation‐Model Animal pipeline to determine the function (diet digestion, physiology, and behavior) of these target strains in the wild animal gut.     

MOLECULAR PALAEOBIOLOGY

Abstract:  For more than a generation, molecular biology has been used to approach palaeontological problems, and yet only recently have attempts been made to integrate research utilizing the geological and genomic records in uncovering evolutionary history. We codify this approach as Molecular Palaeobiology for which we provide a synthetic framework for studying the interplay among genotype, phenotype and the environment, within the context of deep time. We provide examples of existing studies where molecular and morphological data have been integrated to provide novel insights within each of these variables, and an account of a case study where each variable has been tackled to understand better a single macroevolutionary event: the diversification of metazoan phyla. We show that the promise of this approach extends well beyond research into the evolutionary history of animals and, in particular, we single out plant evolution as the single greatest opportunity waiting to be exploited by molecular palaeobiology. Although most of our examples consider how novel molecular data and techniques have breathed new life into long-standing palaeontological controversies, we argue that this asymmetry in the balance of molecular and morphological evidence is an artefact of the relative 'newness' of molecular data. In particular, palaeontological data provide unique and crucial roles in unravelling evolutionary history given that extinct taxa reveal patterns of character evolution invisible to molecular biology. Finally, we argue that palaeobiologists, rather than molecular biologists, are best placed to exploit the opportunity afforded by molecular palaeobiology, though this will require incorporating the techniques and approaches of molecular biology into their skill-set.     

The evolutionary impacts of conservation actions

Conservation management for environmental sustainability is now ubiquitous. The ecological effects of these actions are well-intentioned and well-known. Although conservation biologists and managers increasingly incorporate evolutionary considerations into management plans, the evolutionary consequences of management strategies have remained relatively unexplored and unconsidered. But what are the evolutionary consequences? Here, we advocate a new research agenda focused on identifying, predicting, and countering the evolutionary consequences of conservation management. We showcase the examples of park creation and invasive species management, and speculate further on five other major methods of management. Park creation may cause selection for altered dispersal and behavior that utilizes human foods and structures. Management of invasive species may favor the evolution of resistance to or tolerance of control methods. In these and other cases, evolution may cause deviations from the predicted consequences of management strategies optimized without considering evolution, particularly when management results in or coincides with major environmental change, if population size change strongly, or if life histories are short enough to allow more rapid evolution. We call for research focused on: (1) experimental predictions and tests of evolution under particular management strategies, (2) widespread monitoring of managed populations and communities, and (3) meta-analysis and theoretical study aimed at simplifying the process of evolutionary prediction, particularly at systematizing a means of identifying traits likely to evolve due to likely existing genetic variance or high mutation rates. Ultimately, conservation biologists should incorporate evolutionary prediction into management planning to prevent the evolutionary domestication of the species that they are trying to protect.     

Phenotypic and genetic integration of personality and growth under competition in the sheepshead swordtail,Xiphophorus birchmanni

Competition for resources including food, physical space, and potential mates is a fundamental ecological process shaping variation in individual phenotype and fitness. The evolution of competitive ability, in particular social dominance, depends on genetic (co)variation among traits causal (e.g., behavior) or consequent (e.g., growth) to competitive outcomes. If dominance is heritable, it will generate both direct and indirect genetic effects (IGE) on resource‐dependent traits. The latter are expected to impose evolutionary constraint because winners necessarily gain resources at the expense of losers. We varied competition in a population of sheepshead swordtails, Xiphophorus birchmanni, to investigate effects on behavior, size, growth, and survival. We then applied quantitative genetic analyses to determine (i) whether competition leads to phenotypic and/or genetic integration of behavior with life history and (ii) the potential for IGE to constrain life history evolution. Size, growth, and survival were reduced at high competition. Male dominance was repeatable and dominant individuals show higher growth and survival. Additive genetic contributions to phenotypic covariance were significant, with the G matrix largely recapitulating phenotypic relationships. Social dominance has a low but significant heritability and is strongly genetically correlated with size and growth. Assuming causal dependence of growth on dominance, hidden IGE will therefore reduce evolutionary potential.     

When water interacts with temperature: Ecological and evolutionary implications of thermo‐hydroregulation in terrestrial ectotherms

The regulation of body temperature (thermoregulation) and of water balance (defined here as hydroregulation) are key processes underlying ecological and evolutionary responses to climate fluctuations in wild animal populations. In terrestrial (or semiterrestrial) ectotherms, thermoregulation and hydroregulation closely interact and combined temperature and water constraints should directly influence individual performances. Although comparative physiologists traditionally investigate jointly water and temperature regulation, the ecological and evolutionary implications of these coupled processes have so far mostly been studied independently. Here, we revisit the concept of thermo‐hydroregulation to address the functional integration of body temperature and water balance regulation in terrestrial ectotherms. We demonstrate how thermo‐hydroregulation provides a framework to investigate functional adaptations to joint environmental variation in temperature and water availability, and potential physiological and/or behavioral conflicts between thermoregulation and hydroregulation. We extend the classical cost–benefit model of thermoregulation in ectotherms to highlight the adaptive evolution of optimal thermo‐hydroregulation strategies. Critical gaps in the parameterization of this conceptual optimality model and guidelines for future empirical research are discussed. We show that studies of thermo‐hydroregulation refine our mechanistic understanding of physiological and behavioral plasticity, and of the fundamental niche of the species. This is illustrated with relevant and recent examples of space use and dispersal, resource‐based trade‐offs, and life‐history tactics in insects, amphibians, and nonavian reptiles.     

Why the short face? Developmental disintegration of the neurocranium drives convergent evolution in neotropical electric fishes

Convergent evolution is widely viewed as strong evidence for the influence of natural selection on the origin of phenotypic design. However, the emerging evo‐devo synthesis has highlighted other processes that may bias and direct phenotypic evolution in the presence of environmental and genetic variation. Developmental biases on the production of phenotypic variation may channel the evolution of convergent forms by limiting the range of phenotypes produced during ontogeny. Here, we study the evolution and convergence of brachycephalic and dolichocephalic skull shapes among 133 species of Neotropical electric fishes (Gymnotiformes: Teleostei) and identify potential developmental biases on phenotypic evolution. We plot the ontogenetic trajectories of neurocranial phenotypes in 17 species and document developmental modularity between the face and braincase regions of the skull. We recover a significant relationship between developmental covariation and relative skull length and a significant relationship between developmental covariation and ontogenetic disparity. We demonstrate that modularity and integration bias the production of phenotypes along the brachycephalic and dolichocephalic skull axis and contribute to multiple, independent evolutionary transformations to highly brachycephalic and dolichocephalic skull morphologies.     

Cryptic sexual conflict in gift-giving insects: chasing the chase-away

The chase-away model of sexual selection posits that elaborate male sexual displays arise because they exploit preexisting biases in females' sensory systems and induce females to mate in a suboptimal manner. An essential element of this hypothesis is that such manipulation should quickly lead to female resistance to male displays. Nuptial food gifts may be a frequent conduit by which males attempt to influence the mating behavior of females against females' own reproductive interests. In decorated crickets Gryllodes sigillatus, such inducements come in the form of a spermatophylax, a gelatinous mass forming part of the male's spermatophore and consumed by the female after mating. We conducted experiments in which spermatophylaxes obtained from male G. sigillatus were offered as novel food gifts to females of a non-gift-giving species (Acheta domesticus) having no evolutionary history of spermatophylax consumption. Female A. domesticus that were allowed to consume the spermatophylax took significantly longer to remate than when given no such opportunity. In contrast, when female G. sigillatus were prevented from consuming their partners' nuptial gifts, there was no difference in their propensity to remate relative to females permitted to consume a food gift after mating. These results suggest that the spermatophylax synthesized by male G. sigillatus contains substances designed to inhibit the sexual receptivity of their mates but that female G. sigillatus have evolved reduced responsiveness to these substances.     

Summary and perspective on evolutionary ecology of fishes

This special issue of Evolutionary Ecology provides ten papers that have been presented at a conference on Evolutionary Ecology of Fishes in 2009. In addition to briefly summarizing the main content of the papers which is related to adaptive radiations, processes of ecological divergence, and fisheries-induced evolution, we review and synthesize in short the recent advance in studies on evolutionary ecology of fishes. We conclude that fishes are excellent model systems to study evolutionary ecology of animals, and suggest three promising new research avenues; (1) the contribution of behavioural processes to evolution, in particular the consideration of animal personalities and predator–prey interactions, (2) metabolic physiology and parasite-host interactions as new niche dimensions to be considered for adaptive diversification, and (3) the opportunities for mechanistic understanding of adaptation and speciation emerging from new genetic tools.     

Network design meets in silico evolutionary biology

Cell fate is programmed through gene regulatory networks that perform several calculations to take the appropriate decision. In silico evolutionary optimization mimics the way Nature has designed such gene regulatory networks. In this review we discuss the basic principles of these evolutionary approaches and how they can be applied to engineer synthetic networks. We summarize the basic guidelines to implement an in silico evolutionary design method, the operators for mutation and selection that iteratively drive the network architecture towards a specified dynamical behavior. Interestingly, as it happens in natural evolution, we show the existence of patterns of punctuated evolution. In addition, we highlight several examples of models that have been designed using automated procedures, together with different objective functions to select for the proper behavior. Finally, we briefly discuss the modular designability of gene regulatory networks and its potential application in biotechnology.     

Comprehensive splice-site analysis using comparative genomics

We have collected over half a million splice sites from five species-Homo sapiens, Mus musculus, Drosophila melanogaster, Caenorhabditis elegans and Arabidopsis thaliana-and classified them into four subtypes: U2-type GT-AG and GC-AG and U12-type GT-AG and AT-AC. We have also found new examples of rare splice-site categories, such as U12-type introns without canonical borders, and U2-dependent AT-AC introns. The splice-site sequences and several tools to explore them are available on a public website (SpliceRack). For the U12-type introns, we find several features conserved across species, as well as a clustering of these introns on genes. Using the information content of the splice-site motifs, and the phylogenetic distance between them, we identify: (i) a higher degree of conservation in the exonic portion of the U2-type splice sites in more complex organisms; (ii) conservation of exonic nucleotides for U12-type splice sites; (iii) divergent evolution of C.elegans 3' splice sites (3'ss) and (iv) distinct evolutionary histories of 5' and 3'ss. Our study proves that the identification of broad patterns in naturally-occurring splice sites, through the analysis of genomic datasets, provides mechanistic and evolutionary insights into pre-mRNA splicing.