The microbial environment modulates non-genetic maternal effects on egg immunity.

BACKGROUND: In a diverse microbial world immune function of animals is essential. Diverse microbial environments may contribute to extensive variation in immunological phenotypes of vertebrates, among and within species and individuals. As maternal effects benefit offspring development and survival, whether females use cues about their microbial environment to prime offspring immune function is unclear. To provide microbial environmental context to maternal effects, we asked if the bacterial diversity of the living environment of female zebra finches Taeniopygia guttata shapes maternal effects on egg immune function. We manipulated environmental bacterial diversity of birds and tested if females increased immunological investment in eggs in an environment with high bacterial diversity (untreated soil) versus low (gamma-sterilized soil). We quantified lysozyme and ovotransferrin in egg albumen and IgY in egg yolk and in female blood, and we used 16S rRNA gene sequencing to profile maternal cloacal and eggshell microbiotas. RESULTS: We found a maternal effect on egg IgY concentration that reflected environmental microbial diversity: females who experienced high diversity deposited more IgY in their eggs, but only if maternal plasma IgY levels were relatively high. We found no effects on lysozyme and ovotransferrin concentrations in albumen. Moreover, we uncovered that variation in egg immune traits could be significantly attributed to differences among females: for IgY concentration in yolk repeatability R = 0.80; for lysozyme concentration in albumen R = 0.27. Furthermore, a partial least squares path model (PLS-PM) linking immune parameters of females and eggs, which included maternal and eggshell microbiota structures and female body condition, recapitulated the treatment-dependent yolk IgY response. The PLS-PM additionally suggested that the microbiota and physical condition of females contributed to shaping maternal effects on egg immune function, and that (non-specific) innate egg immunity was prioritized in the environment with low bacterial diversity. CONCLUSIONS: The microbial environment of birds can shape maternal effects on egg immune function. Since immunological priming of eggs benefits offspring, we highlight that non-genetic maternal effects on yolk IgY levels based on cues from the parental microbial environment may prove important for offspring to thrive in the microbial environment that they are expected to face.

Evolution of parasitoid host preference and performance in response to an invasive host acting as evolutionary trap.

The invasion of a novel host species can create a mismatch in host choice and offspring survival (performance) when native parasitoids attempt to exploit the invasive host without being able to circumvent its resistance mechanisms. Invasive hosts can therefore act as evolutionary trap reducing parasitoids' fitness and this may eventually lead to their extinction. Yet, escape from the trap can occur when parasitoids evolve behavioral avoidance or a physiological strategy compatible with the trap host, resulting in either host-range expansion or a complete host-shift. We developed an individual based model to investigate which conditions promote parasitoids to evolve behavioral preference that matches their performance, including host-trap avoidance, and which conditions lead to adaptations to the unsuitable hosts. The model was inspired by solitary endo-parasitoids attacking larval host stages. One important aspect of these conditions was reduced host survival during incompatible interaction, where a failed parasitization attempt by a parasitoid resulted not only in death of her offspring but also in host killing. This non-reproductive host mortality had a strong influence on the likelihood of establishment of novel host-parasitoid relationship, in some cases constraining adaptation to the trap host species. Moreover, our model revealed that host-search efficiency and genetic variation in host-preference play a key role in the likelihood that parasitoids will include the suboptimal host in their host range, or will evolve behavioral avoidance resulting in specialization and host-range conservation, respectively. Hence, invasive species might change the evolutionary trajectory of native parasitoid species, which is important for predicting biocontrol ability of native parasitoids towards novel hosts.

Trade-offs predicted by metabolic network structure give rise to evolutionary specialization and phenotypic diversification.

Mitigating trade-offs between different resource-utilization functions is key to an organism's ecological and evolutionary success. These trade-offs often reflect metabolic constraints with a complex molecular underpinning; therefore, their consequences for evolutionary processes have remained elusive. Here, we investigate how metabolic architecture induces resource utilization constraints and how these constraints, in turn, elicit evolutionary specialization and diversification. Guided by the metabolic network structure of the bacterium Lactococcus cremoris, we selected two carbon sources (fructose and galactose) with predicted co-utilization constraints. By evolving L. cremoris on either fructose, galactose or a mix of both sugars, we imposed selection favoring divergent metabolic specializations or co-utilization of both resources, respectively. Phenotypic characterization revealed the evolution of either fructose or galactose specialists in the single-sugar treatments. In the mixed sugar regime, we observed adaptive diversification: both specialists coexisted, and no generalist evolved. Divergence from the ancestral phenotype occurred at key pathway junctions in the central carbon metabolism. Fructose specialists evolved mutations in the fbp and pfk genes that appear to balance anabolic and catabolic carbon fluxes. Galactose specialists evolved increased expression of pgmA (the primary metabolic bottleneck of galactose metabolism) and silencing of ptnABCD (the main glucose transporter) and ldh (regulator/enzyme of downstream carbon metabolism). Overall, our study shows how metabolic network architecture and historical contingency serve to predict targets of selection and inform the functional interpretation of evolved mutations. The elucidation of the relationship between molecular constraints and phenotypic trade-offs contributes to an integrative understanding of evolutionary specialization and diversification.

Eusociality and the Evolution of Aging in Superorganisms.

AbstractEusocial insects-ants, bees, wasps, and termites-are being recognized as model organisms to unravel the evolutionary paradox of aging for two reasons: (1) queens (and kings, in termites) of social insects outlive similarly sized solitary insects by up to several orders of magnitude and (2) all eusocial taxa show a divergence of long queen and shorter worker life spans, despite their shared genomes and even under risk-free laboratory environments. Traditionally, these observations have been explained by invoking the classical evolutionary aging theory: well-protected inside their nests, queens are much less exposed to external hazards than foraging workers, and this provides natural selection the opportunity to favor queens that perform well at advanced ages. Although quite plausible, these verbal arguments have not been backed up by mathematical analysis. Here, for the first time, we provide quantitative models for the evolution of caste-specific aging patterns. We show that caste-specific mortality risks are in general neither sufficient nor necessary to explain the evolutionary divergence in life span between queens and workers and the extraordinary queen life spans. Reproductive monopolization and the delayed production of sexual offspring in highly social colonies lead natural selection to inherently favor queens that live much longer than workers, even when exposed to the same external hazards. Factors that reduce a colony's reproductive skew, such as polygyny and worker reproduction, tend to reduce the evolutionary divergence in life span between queens and workers. Caste-specific extrinsic hazards also affect life span divergence, but to a much smaller extent than reproductive monopolization.

Selection for rapid uptake of scarce or fluctuating resource explains vulnerability of glycolysis to imbalance.

Glycolysis is a conserved central pathway in energy metabolism that converts glucose to pyruvate with net production of two ATP molecules. Because ATP is produced only in the lower part of glycolysis (LG), preceded by an initial investment of ATP in the upper glycolysis (UG), achieving robust start-up of the pathway upon activation presents a challenge: a sudden increase in glucose concentration can throw a cell into a self-sustaining imbalanced state in which UG outpaces LG, glycolytic intermediates accumulate and the cell is unable to maintain high ATP concentration needed to support cellular functions. Such metabolic imbalance can result in "substrate-accelerated death", a phenomenon observed in prokaryotes and eukaryotes when cells are exposed to an excess of substrate that previously limited growth. Here, we address why evolution has apparently not eliminated such a costly vulnerability and propose that it is a manifestation of an evolutionary trade-off, whereby the glycolysis pathway is adapted to quickly secure scarce or fluctuating resource at the expense of vulnerability in an environment with ample resource. To corroborate this idea, we perform individual-based eco-evolutionary simulations of a simplified yeast glycolysis pathway consisting of UG, LG, phosphate transport between a vacuole and a cytosol, and a general ATP demand reaction. The pathway is evolved in constant or fluctuating resource environments by allowing mutations that affect the (maximum) reaction rate constants, reflecting changing expression levels of different glycolytic enzymes. We demonstrate that under limited constant resource, populations evolve to a genotype that exhibits balanced dynamics in the environment it evolved in, but strongly imbalanced dynamics under ample resource conditions. Furthermore, when resource availability is fluctuating, imbalanced dynamics confers a fitness advantage over balanced dynamics: when glucose is abundant, imbalanced pathways can quickly accumulate the glycolytic intermediate FBP as intracellular storage that is used during periods of starvation to maintain high ATP concentration needed for growth. Our model further predicts that in fluctuating environments, competition for glucose can result in stable coexistence of balanced and imbalanced cells, as well as repeated cycles of population crashes and recoveries that depend on such polymorphism. Overall, we demonstrate the importance of ecological and evolutionary arguments for understanding seemingly maladaptive aspects of cellular metabolism.

The omnistat: A flexible continuous-culture system for prolonged experimental evolution.

Microbial evolution experiments provide a powerful tool to unravel the molecular basis of adaptive evolution but their outcomes can be difficult to interpret, unless the selective forces that are applied during the experiment are carefully controlled. In this respect, experimental evolution in continuous cultures provides advantages over commonly used sequential batch-culture protocols because continuous cultures allow for more accurate control over the induced selective environment. However, commercial continuous-culture systems are large and expensive, while available DIY continuous-culture systems are not versatile enough to allow for multiple sensors and rigorous stirring.We present a modular continuous-culture system that adopts the commonly used GL45 glass laboratory bottle as a bioreactor vessel. Our design offers three advantages: first, it is equipped with a large head plate, fitting two sensors and seven input/output ports, enabling the customization of the system for many running modes (chemostat, auxostat, etc.). Second, the bioreactor is small (25-250 ml), which makes it feasible to run many replicates in parallel. Third, bioreactor modules can be coupled by uni- or bi-directional flows to induce spatiotemporal variation in selection. These features result in a particularly flexible culturing platform that facilitates the investigation of a broad range of evolutionary and ecological questions.To illustrate the versatility of our culturing system, we outline two evolution experiments that impose a temporally or spatially variable regime of selection. The first experiment illustrates how controlled temporal variation in resource availability can be utilized to select for anticipatory switching. The second experiment illustrates a spatially structured morbidostat setup that is designed to probe epistatic interactions between adaptive mutations. Furthermore, we demonstrate how sensor data can be used to stabilize selection pressures or track evolutionary adaptation.Evolution experiments in which populations are exposed to controlled spatiotemporal variation, are essential to gain insight into the process of adaptation and the mechanisms that constrain evolution. Continuous-culture systems, like the one presented here, offer control over key environmental parameters and establish a well-defined regime of selection. As such, they create the opportunity to expose evolutionary constraints in the form of phenotypic trade-offs, contributing to a mechanistic understanding of adaptive evolution.

Wide lag time distributions break a trade-off between reproduction and survival in bacteria.

Many microorganisms face a fundamental trade-off between reproduction and survival: Rapid growth boosts population size but makes microorganisms sensitive to external stressors. Here, we show that starved bacteria encountering new resources can break this trade-off by evolving phenotypic heterogeneity in lag time. We quantify the distribution of single-cell lag times of populations of starved Escherichia coli and show that population growth after starvation is primarily determined by the cells with shortest lag due to the exponential nature of bacterial population dynamics. As a consequence, cells with long lag times have no substantial effect on population growth resumption. However, we observe that these cells provide tolerance to stressors such as antibiotics. This allows an isogenic population to break the trade-off between reproduction and survival. We support this argument with an evolutionary model which shows that bacteria evolve wide lag time distributions when both rapid growth resumption and survival under stressful conditions are under selection. Our results can explain the prevalence of antibiotic tolerance by lag and demonstrate that the benefits of phenotypic heterogeneity in fluctuating environments are particularly high when minorities with extreme phenotypes dominate population dynamics.

Alternative male morphs solve sperm performance/longevity trade-off in opposite directions.

Males pursuing alternative reproductive tactics have been predicted to face a trade-off between maximizing either swimming performance or endurance of their sperm. However, empirical evidence for this trade-off is equivocal, which may be due to simplistic assumptions. In the shell-brooding cichlid fish Lamprologus callipterus, two Mendelian male morphs compete for fertilization by divergent means: Bourgeois nest males ejaculate sperm, on average, about six times farther from the unfertilized ova than do parasitic dwarf males. This asymmetry is opposite to the usual situation, in which bourgeois males typically benefit from superior fertilization opportunities, suggesting that nest males' sperm should persist longer than dwarf male sperm. The assumed trade-off between sperm swimming performance and longevity predicts that, in turn, sperm of dwarf males should outperform that of nest males in swimming efficiency. Measurement of sperm performance and endurance reveals that dwarf male spermatozoa swim straighter initially than those of nest males, but their motility declines earlier and their velocity slows down more abruptly. Nest male sperm survives longer, which relates to a larger sperm head plus midpiece, implying more mitochondria. Thus, the trade-off between sperm performance and endurance is optimized in opposite directions by alternative male morphs. We argue that the relative success of alternative sperm performance strategies can be influenced strongly by environmental factors such as the time window between gamete release and fertilization, and the position of gamete release. This is an important yet little understood aspect of gametic adaptations to sperm competition.

Mechanisms of Assortative Mating in Speciation with Gene Flow: Connecting Theory and Empirical Research.

The large body of theory on speciation with gene flow has brought to light fundamental differences in the effects of two types of mating rules on speciation: preference/trait rules, in which divergence in both (female) preferences and (male) mating traits is necessary for assortment, and matching rules, in which individuals mate with like individuals on the basis of the presence of traits or alleles that they have in common. These rules can emerge from a variety of behavioral or other mechanisms in ways that are not always obvious. We discuss the theoretical properties of both types of rules and explain why speciation is generally thought to be more likely under matching rather than preference/trait rules. We furthermore discuss whether specific assortative mating mechanisms fall under a preference/trait or matching rule, present empirical evidence for these mechanisms, and propose empirical tests that could distinguish between them. The synthesis of the theoretical literature on these assortative mating rules with empirical studies of the mechanisms by which they act can provide important insights into the occurrence of speciation with gene flow. Finally, by providing a clear framework we hope to inspire greater alignment in the ways that both theoreticians and empiricists study mating rules and how these rules affect speciation through maintaining or eroding barriers to gene flow among closely related species or populations.

Quorum sensing integrates environmental cues, cell density and cell history to control bacterial competence.

Streptococcus pneumoniae becomes competent for genetic transformation when exposed to an autoinducer peptide known as competence-stimulating peptide (CSP). This peptide was originally described as a quorum-sensing signal, enabling individual cells to regulate competence in response to population density. However, recent studies suggest that CSP may instead serve as a probe for sensing environmental cues, such as antibiotic stress or environmental diffusion. Here, we show that competence induction can be simultaneously influenced by cell density, external pH, antibiotic-induced stress, and cell history. Our experimental data is explained by a mathematical model where the environment and cell history modify the rate at which cells produce or sense CSP. Taken together, model and experiments indicate that autoinducer concentration can function as an indicator of cell density across environmental conditions, while also incorporating information on environmental factors or cell history, allowing cells to integrate cues such as antibiotic stress into their quorum-sensing response. This unifying perspective may apply to other debated quorum-sensing systems.Peptide CSP regulates natural competence in pneumococci and has been proposed as a quorum-sensing signal or a probe for sensing environmental cues. Here, the authors show that CSP levels can indeed act as an indicator of cell density and also incorporate information on environmental factors or cell history.

Reconstructing the genotype-to-fitness map for the bacterial chemotaxis network and its emergent behavioural phenotypes.

The signal-transduction network responsible for chemotaxis in Escherichia coli has been characterised in extraordinary detail. Yet, relatively little is known about eco-evolutionary aspects of chemotaxis, such as how the network has been shaped by selection and to what extent natural populations may fine-tune their chemotactic behaviour to the ecological conditions. To address these questions, we here develop an evolutionary-systems-biology model of the chemotaxis network of E. coli, which we apply to estimate the resource accumulation rate (here used as a proxy for fitness) of wildtype and a large number of potential mutant genotypes. Mutant genotypes differ from the wildtype in the concentrations of one or more constituent proteins of the chemotaxis signalling network or in one or more of its kinetic parameters. To guarantee model consistency across the genotype space, we explicitly incorporated biochemical constraints that underly observed phenotypic trade-offs. The model was validated by reconstructing the phenotypic properties of several known mutant genotypes. We also characterised differences in the fitness distribution between genotypes, and reconstructed adaptive walks in genotype space for populations exposed to different environmental conditions. We found that the local fitness landscape is rugged, due to non-additive interactions between mutations. When selection has a consistent direction, just a few adaptive mutations are required to reach a local peak, and different local peaks can be reached by adaptive walks starting from the same initial genotype. However, when the direction of selection is fluctuating, evolutionary paths are much longer and genotype space is explored further. Longer adaptive walks were also observed when evolution was started from a low-fitness genotype such as a CheZ knockout mutant. In line with empirical observations, the initial ΔcheZ mutant did not respond to a step-down stimulus, but a dynamic response similar to the wildtype was recovered following the fixation of compensatory mutations.

Collective Resistance in Microbial Communities by Intracellular Antibiotic Deactivation.

The structure and composition of bacterial communities can compromise antibiotic efficacy. For example, the secretion of ß-lactamase by individual bacteria provides passive resistance for all residents within a polymicrobial environment. Here, we uncover that collective resistance can also develop via intracellular antibiotic deactivation. Real-time luminescence measurements and single-cell analysis demonstrate that the opportunistic human pathogen Streptococcus pneumoniae grows in medium supplemented with chloramphenicol (Cm) when resistant bacteria expressing Cm acetyltransferase (CAT) are present. We show that CAT processes Cm intracellularly but not extracellularly. In a mouse pneumonia model, more susceptible pneumococci survive Cm treatment when coinfected with a CAT-expressing strain. Mathematical modeling predicts that stable coexistence is only possible when antibiotic resistance comes at a fitness cost. Strikingly, CAT-expressing pneumococci in mouse lungs were outcompeted by susceptible cells even during Cm treatment. Our results highlight the importance of the microbial context during infectious disease as a potential complicating factor to antibiotic therapy.

Lifespan divergence between social insect castes: challenges and opportunities for evolutionary theories of aging.

The extraordinarily long lifespans of queens (and kings) in eusocial insects and the strikingly large differences in life expectancy between workers and queens challenge our understanding of the evolution of aging and provide unique opportunities for studying the causes underlying adaptive variation in lifespan within species. Here we review the major evolutionary theories of aging, focusing on their scope and limitations when applied to social insects. We show that reproductive division of labor, interactions between kin, caste-specific gene regulation networks, and the integration of colony-level trade-offs with individual-level trade-offs provide challenges to the classical theories We briefly indicate how these challenges could be met in future models of adaptive phenotypic plasticity in lifespan between and within different castes.

Coevolutionary feedback elevates constitutive immune defence: a protein network model.

BACKGROUND: Organisms have evolved a variety of defence mechanisms against natural enemies, which are typically used at the expense of other life history components. Induced defence mechanisms impose minor costs when pathogens are absent, but mounting an induced response can be time-consuming. Therefore, to ensure timely protection, organisms may partly rely on constitutive defence despite its sustained cost that renders it less economical. Existing theoretical models addressing the optimal combination of constitutive versus induced defence focus solely on host adaptation and ignore the fact that the efficacy of protection depends on genotype-specific host-parasite interactions. Here, we develop a signal-transduction network model inspired by the invertebrate innate immune system, in order to address the effect of parasite coevolution on the optimal combination of constitutive and induced defence. RESULTS: Our analysis reveals that coevolution of parasites with specific immune components shifts the host's optimal allocation from induced towards constitutive immunity. This effect is dependent upon whether receptors (for detection) or effectors (for elimination) are subjected to parasite counter-evolution. A parasite population subjected to a specific immune receptor can evolve heightened genetic diversity, which makes parasite detection more difficult for the hosts. We show that this coevolutionary feedback renders the induced immune response less efficient, forcing the hosts to invest more heavily in constitutive immunity. Parasites diversify to escape elimination by a specific effector too. However, this diversification does not alter the optimal balance between constitutive and induced defence: the reliance on constitutive defence is promoted by the receptor's inability to detect, but not the effectors' inability to eliminate parasites. If effectors are useless, hosts simply adapt to tolerate, rather than to invest in any defence against parasites. These contrasting results indicate that evolutionary feedback between host and parasite populations is a key factor shaping the selection regime for immune networks facing antagonistic coevolution. CONCLUSION: Parasite coevolution against specific immune defence alters the prediction of the optimal use of defence, and the effect of parasite coevolution varies between different immune components.

Negotiation and appeasement can be more effective drivers of sociality than kin selection.

Two alternative frameworks explain the evolution of cooperation in the face of conflicting interests. Conflicts can be alleviated by kinship, the alignment of interests by virtue of shared genes, or by negotiation strategies, allowing mutually beneficial trading of services or commodities. Although negotiation often occurs in kin-structured populations, the interplay of kin- and negotiation-based mechanisms in the evolution of cooperation remains an unresolved issue. Inspired by the biology of a cooperatively breeding fish, we developed an individual-based simulation model to study the evolution of negotiation-based cooperation in relation to different levels of genetic relatedness. We show that the evolution of negotiation strategies leads to an equilibrium where subordinates appease dominants by conditional cooperation, resulting in high levels of help and low levels of aggression. This negotiation-based equilibrium can be reached both in the absence of relatedness and in a kin-structured population. However, when relatedness is high, evolution often ends up in an alternative equilibrium where subordinates help their kin unconditionally. The level of help at this kin-selected equilibrium is considerably lower than at the negotiation-based equilibrium, and it corresponds to a level reached when responsiveness is prevented from evolving in the simulations. A mathematical invasion analysis reveals that, quite generally, the alignment of payoffs due to the relatedness of interaction partners tends to impede selection for harsh but effective punishment of defectors. Hence kin structure will often hamper rather than facilitate the evolution of productive cooperation.

Contrasting effects of intralocus sexual conflict on sexually antagonistic coevolution.

Evolutionary conflict between the sexes can induce arms races in which males evolve traits that are detrimental to the fitness of their female partners, and vice versa. This interlocus sexual conflict (IRSC) has been proposed as a cause of perpetual intersexual antagonistic coevolution with wide-ranging evolutionary consequences. However, theory suggests that the scope for perpetual coevolution is limited, if traits involved in IRSC are subject to pleiotropic constraints. Here, we consider a biologically plausible form of pleiotropy that has hitherto been ignored in treatments of IRSC and arrive at drastically different conclusions. Our analysis is based on a quantitative genetic model of sexual conflict, in which genes controlling IRSC traits have side effects in the other sex, due to incompletely sex-limited gene expression. As a result, the genes are exposed to intralocus sexual conflict (IASC), a tug-of-war between opposing male- and female-specific selection pressures. We find that the interaction between the two forms of sexual conflict has contrasting effects on antagonistic coevolution: Pleiotropic constraints stabilize the dynamics of arms races if the mating traits are close to evolutionary equilibrium but can prevent populations from ever reaching such a state. Instead, the sexes are drawn into a continuous cycle of arms races, causing the buildup of IASC, alternated by phases of IASC resolution that trigger the next arms race. These results encourage an integrative perspective on the biology of sexual conflict and generally caution against relying exclusively on equilibrium stability analysis.

Coaction versus reciprocity in continuous-time models of cooperation.

Cooperating animals frequently show closely coordinated behaviours organized by a continuous flow of information between interacting partners. Such real-time coaction is not captured by the iterated prisoner's dilemma and other discrete-time reciprocal cooperation games, which inherently feature a delay in information exchange. Here, we study the evolution of cooperation when individuals can dynamically respond to each other's actions. We develop continuous-time analogues of iterated-game models and describe their dynamics in terms of two variables, the propensity of individuals to initiate cooperation (altruism) and their tendency to mirror their partner's actions (coordination). These components of cooperation stabilize at an evolutionary equilibrium or show oscillations, depending on the chosen payoff parameters. Unlike reciprocal altruism, cooperation by coaction does not require that those willing to initiate cooperation pay in advance for uncertain future benefits. Correspondingly, we show that introducing a delay to information transfer between players is equivalent to increasing the cost of cooperation. Cooperative coaction can therefore evolve much more easily than reciprocal cooperation. When delays entirely prevent coordination, we recover results from the discrete-time alternating prisoner's dilemma, indicating that coaction and reciprocity are connected by a continuum of opportunities for real-time information exchange.

The evolution of age-dependent plasticity.

When organisms encounter environments that are heterogeneous in time, phenotypic plasticity is often favored by selection. The degree of such plasticity can vary during an organism's lifetime, but the factors promoting differential plastic responses at different ages or life stages remain poorly understood. Here we develop and analyze an evolutionary model to investigate how environmental information is optimally collected and translated into phenotypic adjustments at different ages. We demonstrate that plasticity must often be expected to vary with age in a nonmonotonic fashion. Early in life, it is generally optimal to delay phenotypic adjustments until sufficient information has been collected about the state of the environment to warrant a costly phenotypic adjustment. Toward the end of life, phenotypic adjustments are disfavored as well because their beneficial effects can no longer be fully reaped before death. Our analysis clarifies how patterns of age-dependent plasticity are shaped by the interplay of environmental uncertainty, the accuracy of perceived information, and the costs of phenotypic adjustments with life-history determinants such as the relative strengths of fecundity and viability selection experienced by the organism over its lifetime. We conclude by comparing our results with expectations for alternative mechanisms, including developmental constraints, that promote age-dependent plasticity.

Environment-dependent selection on mate choice in a natural population of birds.

Female mate choice acts as an important evolutionary force, yet the influence of the environment on both its expression and the selective pressures acting upon it remains unknown. We found consistent heritable differences between females in their choice of mate based on ornament size during a 25-year study of a population of collared flycatchers. However, the fitness consequences of mate choice were dependent on environmental conditions experienced whilst breeding. Females breeding with highly ornamented males experienced high relative fitness during dry summer conditions, but low relative fitness during wetter years. Our results imply that sexual selection within a population can be highly variable and dependent upon the prevailing weather conditions experienced by individuals.

Magic traits in speciation: 'magic' but not rare?

Speciation with gene flow is greatly facilitated when traits subject to divergent selection also contribute to non-random mating. Such traits have been called 'magic traits', which could be interpreted to imply that they are rare, special, or unrealistic. Here, we question this assumption by illustrating that magic traits can be produced by a variety of mechanisms, including ones in which reproductive isolation arises as an automatic by-product of adaptive divergence. We also draw upon the theoretical literature to explore whether magic traits have a unique role in speciation or can be mimicked in their effects by physically linked trait-complexes. We conclude that magic traits are more frequent than previously perceived, but further work is needed to clarify their importance.