The repeatability of adaptive radiation during long-term experimental evolution of Escherichia coli in a multiple nutrient environment

Adaptive radiations occur when a species diversifies into different ecological specialists due to competition for resources and trade-offs associated with the specialization. The evolutionary outcome of an instance of adaptive radiation cannot generally be predicted because chance (stochastic events) and necessity (deterministic events) contribute to the evolution of diversity. With increasing contributions of chance, the degree of parallelism among different instances of adaptive radiations and the predictability of an outcome will decrease. To assess the relative contributions of chance and necessity during adaptive radiation, we performed a selection experiment by evolving twelve independent microcosms of Escherichia coli for 1000 generations in an environment that contained two distinct resources. Specialization to either of these resources involves strong trade-offs in the ability to use the other resource. After selection, we measured three phenotypic traits: 1) fitness, 2) mean colony size, and 3) colony size diversity. We used fitness relative to the ancestor as a measure of adaptation to the selective environment; changes in colony size as a measure of the evolution of new resource specialists because colony size has been shown to correlate with resource specialization; and colony size diversity as a measure of the evolved ecological diversity. Resource competition led to the rapid evolution of phenotypic diversity within microcosms. Measurements of fitness, colony size, and colony size diversity within and among microcosms showed that the repeatability of adaptive radiation was high, despite the evolution of genetic variation within microcosms. Consistent with the observation of parallel evolution, we show that the relative contributions of chance are far smaller and less important than effects due to adaptation for the traits investigated. The two-resource environment imposed similar selection pressures in independent populations and promoted parallel phenotypic adaptive radiations in all independently evolved microcosms.     

The Links Between Parent Behaviors and Boys' and Girls' Science Achievement Beliefs

This study examined whether parental involvement in children's science schoolwork (i.e., discussions about science, homework helping and encouragement of science interest) varies for boys and girls, and how these behaviors relate to children's science achievement beliefs (i.e., ability perceptions and task-value) at the end of a school year. We analyzed these links both for fathers and mothers and examined whether child gender moderates how parental behaviors relate to children's beliefs over time. Data were gathered over a span of a school year from 114 middle-school students (50% girls, 81% European American) and their parents (mothers: n = 103, fathers: n = 90). We found support for the moderating effect of gender. Specifically, the findings indicated that only parents' encouragement of science interest varied by child gender; mothers' encouragement positively predicted girls' self-assessments of science ability at the end of the year, but was a negative estimator of boys' self-assessments. Additionally, mothers' discussions about science showed similar findings with respect to girls' and boys' utility beliefs about science.     

History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection

Introduced species often exhibit changes in genetic variation, population structure, selection regime and phenotypic traits as they colonize and expand into new ranges. For these reasons, species invasions are increasingly recognized as promising systems for studying adaptive evolution over contemporary time scales. However, changes in phenotypic traits during invasion occur under non-equilibrium demographic conditions and may reflect the influences of prior evolutionary history and chance events, as well as selection. We briefly review the evidence for phenotypic evolution and the role of selection during invasion. While there is ample evidence for evolutionary change, it is less clear if selection is the primary mechanism. We then discuss the likelihood that stochastic events shift phenotypic distributions during invasion, and argue that hypotheses of adaptation should be tested against appropriate null models. We suggest two experimental frameworks for separating stochastic evolution from adaptation: statistically accounting for phenotypic variation among putative invasion sources identified by using phylogenetic or assignment methods and by comparing estimates of differentiation within and among ranges for both traits and neutral markers ( Q _ST vs. F _ST). Designs that incorporate a null expectation can reveal the role of history and chance in the evolutionary process, and provide greater insights into evolution during species invasions.     

Newly evolved genes: Moving from comparative genomics to functional studies in model systems

Genes are gained and lost over the course of evolution. A recent study found that over 1,800 new genes have appeared during primate evolution and that an unexpectedly high proportion of these genes are expressed in the human brain. But what are the molecular functions of newly evolved genes and what is their impact on an organism's fitness? The acquisition of new genes may provide a rich source of genetic diversity that fuels evolutionary innovation. Although gene manipulation experiments are not feasible in humans, studies in model organisms, such as Drosophila melanogaster, have shown that new genes can quickly become integrated into genetic networks and become essential for survival or fertility. Future studies of new genes, especially chimeric genes, and their functions will help determine the role of genetic novelty in the adaptation and diversification of species.     

Effects of adaptation, chance, and history on the evolution of the toxic dinoflagellate Alexandrium minutum under selection of increased temperature and acidification

The roles of adaptation, chance, and history on evolution of the toxic dinoflagellate Alexandrium minutum Halim, under selective conditions simulating global change, have been addressed. Two toxic strains (AL1V and AL2V), previously acclimated for two years at pH 8.0 and 20°C, were transferred to selective conditions: pH 7.5 to simulate acidification and 25°C. Cultures under selective conditions were propagated until growth rate and toxin cell quota achieved an invariant mean value at 720 days (ca. 250 and ca. 180 generations for strains AL1V and AL2V, respectively). Historical contingencies strongly constrained the evolution of growth rate and toxin cell quota, but the forces involved in the evolution were not the same for both traits. Growth rate was 1.5-1.6 times higher than the one measured in ancestral conditions. Genetic adaptation explained two-thirds of total adaptation while one-third was a consequence of physiological adaptation. On the other hand, the evolution of toxin cell quota showed a pattern attributable to neutral mutations because the final variances were significantly higher than those measured at the start of the experiment. It has been hypothesized that harmful algal blooms will increase under the future scenario of global change. Although this study might be considered an oversimplification of the reality, it can be hypothesized that toxic blooms will increase but no predictions can be advanced about toxicity.     

The beak of the other finch: coevolution of genetic covariance structure and developmental modularity during adaptive evolution

The link between adaptation and evolutionary change remains the most central and least understood evolutionary problem. Rapid evolution and diversification of avian beaks is a textbook example of such a link, yet the mechanisms that enable beak''s precise adaptation and extensive adaptability are poorly understood. Often observed rapid evolutionary change in beaks is particularly puzzling in light of the neo-Darwinian model that necessitates coordinated changes in developmentally distinct precursors and correspondence between functional and genetic modularity, which should preclude evolutionary diversification. I show that during first 19 generations after colonization of a novel environment, house finches (Carpodacus mexicanus) express an array of distinct, but adaptively equivalent beak morphologies—a result of compensatory developmental interactions between beak length and width in accommodating microevolutionary change in beak depth. Directional selection was largely confined to the elimination of extremes formed by these developmental interactions, while long-term stabilizing selection along a single axis—beak depth—was mirrored in the structure of beak''s additive genetic covariance. These results emphasize three principal points. First, additive genetic covariance structure may represent a historical record of the most recurrent developmental and functional interactions. Second, adaptive equivalence of beak configurations shields genetic and developmental variation in individual components from depletion by natural selection. Third, compensatory developmental interactions among beak components can generate rapid reorganization of beak morphology under novel conditions and thus greatly facilitate both the evolution of precise adaptation and extensive diversification, thereby linking adaptation and adaptability in this classic example of Darwinian evolution.     

The evolution of coexistence: Reciprocal adaptation promotes the assembly of a simple community

Species coexistence may result by chance when co‐occurring species do not strongly interact or it may be an evolutionary outcome of strongly interacting species adapting to each other. Although patterns like character displacement indicate that coexistence has often been an evolutionary outcome, it is unclear how often the evolution of coexistence represents adaptation in only one species or reciprocal adaptation among all interacting species. Here, we demonstrate a strong role for evolution in the coexistence of guppies and killifish in Trinidadian streams. We experimentally recreated the temporal stages in the invasion and establishment of guppies into communities that previously contained only killifish. We combined demographic responses of guppies and killifish with a size‐based integral projection model to calculate the fitness of the phenotypes of each species in each of the stages of community assembly. We show that guppies from locally adapted populations that are sympatric with killifish have higher fitness when paired with killifish than guppies from allopatric populations. This elevated fitness involves effects traceable to both guppy and killifish evolution. We discuss the implications of our results to the study of species coexistence and how it may be mediated through eco‐evolutionary feedbacks.     

Why join a neighbour: fitness consequences of colony fusions in termites

The evolution of life is characterized by major evolutionary transitions during which independent units cooperated and formed a new level of selection. Relatedness is a common mechanism that reduces conflict in such cooperative associations. One of the latest transitions is the evolution of social insect colonies. As expected, they are composed of kin and mechanisms have evolved that prevent the intrusion of nonrelatives. Yet, there are exceptions an extreme case is the fusion of unrelated colonies. What are the advantages of fusions that have colonies with a high potential for conflict as a consequence? Here, we investigated fitness costs and benefits of colony fusions in a lower termite species, Cryptotermes secundus, in which more than 25% of all colonies in the field are fused. We found two benefits of colony fusion depending on colony size: very small colonies had an increased probability of survival when they fused, yet for most colony sizes mainly a few workers profit from colony fusions as their chance to become reproductives increased. This individual benefit was often costly for other colony members: colony growth was reduced and the current reproductives had an increased chance of dying when fusions were aggressive. Our study suggests that fusion of colonies often is the result of ‘selfish’ worker interests to become reproductives, and this might have been important for the termites' social evolution. Our results uniquely shows that selfish interests among related colony members can lead to the formation of groups with increased potential for conflict among less related members.     

Evolutionary Changes in Growth Rate and Toxin Production in the Cyanobacterium <Emphasis Type="Italic">Microcystis aeruginosa</Emphasis> Under a Scenario of Eutrophication and Temperature Increase

Toxic blooms of the cyanobacterium Microcystis aeruginosa affect humans and animals in inland water systems worldwide, and it has been hypothesized that the development of these blooms will increase under the future scenario of global change, considering eutrophication and temperature increase as two important consequences. The importance of genetic adaptation, chance and history on evolution of growth rate, and toxin production of M. aeruginosa was studied under these new conditions. The experiment followed the idea of “replaying life’s tape” by means of the simultaneous propagation of 15 independent isolates of three M. aeruginosa strains, which were grown under doubled nutrient concentration and temperature during c. 87 generations. Adaptation by new mutations that resulted in the enhancement of growth rate arose during propagation of derived cultures under the new environmental conditions was the main component of evolution; however, chance also contributed in a lesser extension to evolution of growth rate. Mutations were selected, displacing the wild-type ancestral genotypes. In contrast, the effect of selection on mutations affecting microcystin production was neutral. Chance and history were the pacemakers in evolution of toxin production. Although this study might be considered an oversimplification of the reality, it suggest that a future scenario of global change might lead to an increase in M. aeruginosa bloom frequency, but no predictions about the frequency of toxicity can be made.     

The genetic basis of thermal reaction norm evolution in lab and natural phage populations

Two major goals of laboratory evolution experiments are to integrate from genotype to phenotype to fitness, and to understand the genetic basis of adaptation in natural populations. Here we demonstrate that both goals are possible by re-examining the outcome of a previous laboratory evolution experiment in which the bacteriophage G4 was adapted to high temperatures. We quantified the evolutionary changes in the thermal reaction norms—the curves that describe the effect of temperature on the growth rate of the phages—and decomposed the changes into modes of biological interest. Our analysis indicated that changes in optimal temperature accounted for almost half of the evolutionary changes in thermal reaction norm shape, and made the largest contribution toward adaptation at high temperatures. Genome sequencing allowed us to associate reaction norm shape changes with particular nucleotide mutations, and several of the identified mutations were found to be polymorphic in natural populations. Growth rate measures of natural phage that differed at a site that contributed substantially to adaptation in the lab indicated that this mutation also underlies thermal reaction norm shape variation in nature. In combination, our results suggest that laboratory evolution experiments may successfully predict the genetic bases of evolutionary responses to temperature in nature. The implications of this work for viral evolution arise from the fact that shifts in the thermal optimum are characterized by tradeoffs in performance between high and low temperatures. Optimum shifts, if characteristic of viral adaptation to novel temperatures, would ensure the success of vaccine development strategies that adapt viruses to low temperatures in an attempt to reduce virulence at higher (body) temperatures.     

Emergent neutrality in adaptive asexual evolution

In nonrecombining genomes, genetic linkage can be an important evolutionary force. Linkage generates interference interactions, by which simultaneously occurring mutations affect each other's chance of fixation. Here, we develop a comprehensive model of adaptive evolution in linked genomes, which integrates interference interactions between multiple beneficial and deleterious mutations into a unified framework. By an approximate analytical solution, we predict the fixation rates of these mutations, as well as the probabilities of beneficial and deleterious alleles at fixed genomic sites. We find that interference interactions generate a regime of emergent neutrality: all genomic sites with selection coefficients smaller in magnitude than a characteristic threshold have nearly random fixed alleles, and both beneficial and deleterious mutations at these sites have nearly neutral fixation rates. We show that this dynamic limits not only the speed of adaptation, but also a population's degree of adaptation in its current environment. We apply the model to different scenarios: stationary adaptation in a time-dependent environment and approach to equilibrium in a fixed environment. In both cases, the analytical predictions are in good agreement with numerical simulations. Our results suggest that interference can severely compromise biological functions in an adapting population, which sets viability limits on adaptive evolution under linkage.     

Avian distraction displays: a review

Distraction displays are conspicuous behaviours functioning to distract a predator's attention away from the displayer's nest or young, thereby reducing the chance of offspring being discovered and predated. Distraction is one of the riskier parental care tactics, as its success derives from the displaying parent becoming the focus of a predator's attention. Such displays are prominent in birds, primarily shorebirds, but the last comprehensive review of distraction was in 1984. Our review aims to provide an updated synthesis of what is known about distraction displays in birds, and to open up new areas of study by highlighting some of the key avenues to explore and the broadened ecological perspectives that could be adopted in future research. We begin by drawing attention to the flexibility of form that distraction displays can take and providing an overview of the different avian taxa known to use anti-predator distraction displays, also examining species-specific sex differences in use. We then explore the adaptive value and evolution of distraction displays, before considering the variation seen in the timing of their use over a reproductive cycle. An evaluation of the efficacy of distraction compared with alternative anti-predator tactics is then conducted via a cost–benefit analysis. Distraction displays are also found in a handful of non-avian taxa, and we briefly consider these unusual cases. We conclude by postulating why distraction is primarily an avian behaviour and set out our suggestions for future research into the evolution and ecology of avian distraction displays.     

The standard genetic code enhances adaptive evolution of proteins

The standard genetic code, by which most organisms translate genetic material into protein metabolism, is non-randomly organized. The Error Minimization hypothesis interprets this non-randomness as an adaptation, proposing that natural selection produced a pattern of codon assignments that buffers genomes against the impact of mutations. Indeed, on the average any given point mutation has a lesser effect on the chemical properties of the utilized amino acid than expected by chance. Might it also, however, be the case that the non-random nature of the code effects the rate of adaptive evolution? To investigate this, here we develop population genetic simulations to test the rate of adaptive gene evolution under different genetic codes. We identify two independent properties of a genetic code that profoundly influence the speed of adaptive evolution. Noting that the standard genetic code exhibits both, we offer a new insight into the effects of the "error minimizing" code: such a code enhances the efficacy of adaptive sequence evolution.     

Trade‐offs and evolution of thermal adaptation in the Irish potato famine pathogen Phytophthora infestans

Temperature is one of the most important environmental parameters with crucial impacts on nearly all biological processes. Due to anthropogenic activity, average air temperatures are expected to increase by a few degrees in coming decades, accompanied by an increased occurrence of extreme temperature events. Such global trends are likely to have various major impacts on human society through their influence on natural ecosystems, food production and biotic interactions, including diseases. In this study, we used a combination of statistical genetics, experimental evolution and common garden experiments to investigate the evolutionary potential for thermal adaptation in the potato late blight pathogen, Phytophthora infestans, and infer its likely response to changing temperatures. We found a trade‐off associated with thermal adaptation to heterogeneous environments in P. infestans, with the degree of the trade‐off peaking approximately at the pathogen's optimum growth temperature. A genetic trade‐off in thermal adaptation was also evidenced by the negative association between a strain's growth rate and its thermal range for growth, and warm climates selecting for a low pathogen growth rate. We also found a mirror effect of phenotypic plasticity and genetic adaptation on growth rate. At below the optimum, phenotypic plasticity enhances pathogen's growth rate but nature selects for slower growing genotypes when temperature increases. At above the optimum, phenotypic plasticity reduces pathogen's growth rate but natural selection favours for faster growing genotypes when temperature increases further. We conclude from these findings that the growth rate of P. infestans will only be marginally affected by global warming.     

How scientists perceive the evolutionary origin of human traits: Results of a survey study

Various hypotheses have been proposed for why the traits distinguishing humans from other primates originally evolved, and any given trait may have been explained both as an adaptation to different environments and as a result of demands from social organization or sexual selection. To find out how popular the different explanations are among scientists, we carried out an online survey among authors of recent scientific papers in journals covering relevant fields of science (paleoanthropology, paleontology, ecology, evolution, human biology). Some of the hypotheses were clearly more popular among the 1,266 respondents than others, but none was universally accepted or rejected. Even the most popular of the hypotheses were assessed “very likely” by <50% of the respondents, but many traits had 1–3 hypotheses that were found at least moderately likely by >70% of the respondents. An ordination of the hypotheses identified two strong gradients. Along one gradient, the hypotheses were sorted by their popularity, measured by the average credibility score given by the respondents. The second gradient separated all hypotheses postulating adaptation to swimming or diving into their own group. The average credibility scores given for different subgroups of the hypotheses were not related to respondent's age or number of publications authored. However, (paleo)anthropologists were more critical of all hypotheses, and much more critical of the water‐related ones, than were respondents representing other fields of expertise. Although most respondents did not find the water‐related hypotheses likely, only a small minority found them unscientific. The most popular hypotheses were based on inherent drivers; that is, they assumed the evolution of a trait to have been triggered by the prior emergence of another human‐specific behavioral or morphological trait, but opinions differed as to which of the traits came first.     

Occurrence data uncover patterns of allopatric divergence and interspecies interactions in the evolutionary history of Sceloporus lizards

As shown from several long‐term and time‐intensive studies, closely related, sympatric species can impose strong selection on one another, leading to dramatic examples of phenotypic evolution. Here, we use occurrence data to identify clusters of sympatric Sceloporus lizard species and to test whether Sceloporus species tend to coexist with other species that differ in body size, as we would expect when there is competition between sympatric congeners. We found that Sceloporus species can be grouped into 16 unique bioregions. Bioregions that are located at higher latitudes tend to be larger and have fewer species, following Rapoport''s rule and the latitudinal diversity gradient. Species richness was positively correlated with the number of biomes and elevation heterogeneity of each bioregion. Additionally, most bioregions show signs of phylogenetic underdispersion, meaning closely related species tend to occur in close geographic proximity. Finally, we found that although Sceloporus species that are similar in body size tend to cluster geographically, small‐bodied Sceloporus species are more often in sympatry with larger‐bodied Sceloporus species than expected by chance alone, whereas large‐bodied species cluster with each other geographically and phylogenetically. These results suggest that community composition in extant Sceloporus species is the result of allopatric evolution, as closely related species move into different biomes, and interspecies interactions, with sympatry between species of different body sizes. Our phyloinformatic approach offers unique and detailed insights into how a clade composed of ecologically and morphologically disparate species are distributed over large geographic space and evolutionary time.     

Microbial laboratory evolution in the era of genome‐scale science

Laboratory evolution studies provide fundamental biological insight through direct observation of the evolution process. They not only enable testing of evolutionary theory and principles, but also have applications to metabolic engineering and human health. Genome‐scale tools are revolutionizing studies of laboratory evolution by providing complete determination of the genetic basis of adaptation and the changes in the organism's gene expression state. Here, we review studies centered on four central themes of laboratory evolution studies: (1) the genetic basis of adaptation; (2) the importance of mutations to genes that encode regulatory hubs; (3) the view of adaptive evolution as an optimization process; and (4) the dynamics with which laboratory populations evolve.     

The evolution of climate tolerance in conifer‐feeding aphids in relation to their host's climatic niche

Climate adaptation has major consequences in the evolution and ecology of all living organisms. Though phytophagous insects are an important component of Earth's biodiversity, there are few studies investigating the evolution of their climatic preferences. This lack of research is probably because their evolutionary ecology is thought to be primarily driven by their interactions with their host plants. Here, we use a robust phylogenetic framework and species‐level distribution data for the conifer‐feeding aphid genus Cinara to investigate the role of climatic adaptation in the diversity and distribution patterns of these host‐specialized insects. Insect climate niches were reconstructed at a macroevolutionary scale, highlighting that climate niche tolerance is evolutionarily labile, with closely related species exhibiting strong climatic disparities. This result may suggest repeated climate niche differentiation during the evolutionary diversification of Cinara. Alternatively, it may merely reflect the use of host plants that occur in disparate climatic zones, and thus, in reality the aphid species' fundamental climate niches may actually be similar but broad. Comparisons of the aphids' current climate niches with those of their hosts show that most Cinara species occupy the full range of the climatic tolerance exhibited by their set of host plants, corroborating the hypothesis that the observed disparity in Cinara species' climate niches can simply mirror that of their hosts. However, 29% of the studied species only occupy a subset of their hosts' climatic zone, suggesting that some aphid species do indeed have their own climatic limitations. Our results suggest that in host‐specialized phytophagous insects, host associations cannot always adequately describe insect niches and abiotic factors must be taken into account.