How competition between overlapping generations can influence optimal egg-laying strategies in annual social insects.

Annual social insects are an integral functional group of organisms, particularly in temperate environments. An emblematic part of their annual cycle is the social phase, during which the colony-founding queen rears workers that later assist her in rearing sexual progeny (gynes and drones). In many annual social insects, such as species of bees, wasps, and other groups, developing larvae are provisioned gradually as they develop (progressive provisioning) leading to multiple larval generations being reared simultaneously. We present a model for how the queen in such cases should optimize her egg-laying rate throughout the social phase depending on number-size trade-offs, colony age-structure, and energy balance. Complementing previous theory on optimal allocation between workers vs. sexuals in annual social insects and on temporal egg-laying patterns in solitary insects, we elucidate how resource competition among overlapping larval generations can influence optimal egg-laying strategies. With model parameters informed by knowledge of a common bumblebee species, the optimal egg-laying schedule consists of two temporally separated early broods followed by a more continuous rearing phase, matching empirical observations. However, eggs should initially be laid continuously at a gradually increasing rate when resources are scarce or mortality risks high and in cases where larvae are fully supplied with resources at the egg-laying stage (mass-provisioning). These factors, alongside sexual:worker body size ratios, further determine the overall trend in egg-laying rates over the colony cycle. Our analysis provides an inroad to study and mechanistically understand variation in colony development strategies within and across species of annual social insects.

Carryover effects from natal habitat type upon competitive ability lead to trait divergence or source-sink dynamics.

Local adaptation to rare habitats is difficult due to gene flow, but can occur if the habitat has higher productivity. Differences in offspring phenotypes have attracted little attention in this context. We model a scenario where the rarer habitat improves offspring's later competitive ability - a carryover effect that operates on top of local adaptation to one or the other habitat type. Assuming localised dispersal, so the offspring tend to settle in similar habitat to the natal type, the superior competitive ability of offspring remaining in the rarer habitat hampers immigration from the majority habitat. This initiates a positive feedback between local adaptation and trait divergence, which can thereafter be reinforced by coevolution with dispersal traits that match ecotype to habitat type. Rarity strengthens selection on dispersal traits and promotes linkage disequilibrium between locally adapted traits and ecotype-habitat matching dispersal. We propose that carryover effects may initiate isolation by ecology.

Constrained growth flips the direction of optimal phenological responses among annual plants.

Phenological changes among plants due to climate change are well documented, but often hard to interpret. In order to assess the adaptive value of observed changes, we study how annual plants with and without growth constraints should optimize their flowering time when productivity and season length changes. We consider growth constraints that depend on the plant's vegetative mass: self-shading, costs for nonphotosynthetic structural tissue and sibling competition. We derive the optimal flowering time from a dynamic energy allocation model using optimal control theory. We prove that an immediate switch (bang-bang control) from vegetative to reproductive growth is optimal with constrained growth and constant mortality. Increasing mean productivity, while keeping season length constant and growth unconstrained, delayed the optimal flowering time. When growth was constrained and productivity was relatively high, the optimal flowering time advanced instead. When the growth season was extended equally at both ends, the optimal flowering time was advanced under constrained growth and delayed under unconstrained growth. Our results suggests that growth constraints are key factors to consider when interpreting phenological flowering responses. It can help to explain phenological patterns along productivity gradients, and links empirical observations made on calendar scales with life-history theory.

The canonical equation of adaptive dynamics for life histories: from fitness-returns to selection gradients and Pontryagin's maximum principle.

This paper should be read as addendum to Dieckmann et al. (J Theor Biol 241:370-389, 2006) and Parvinen et al. (J Math Biol 67: 509-533, 2013). Our goal is, using little more than high-school calculus, to (1) exhibit the form of the canonical equation of adaptive dynamics for classical life history problems, where the examples in Dieckmann et al. (J Theor Biol 241:370-389, 2006) and Parvinen et al. (J Math Biol 67: 509-533, 2013) are chosen such that they avoid a number of the problems that one gets in this most relevant of applications, (2) derive the fitness gradient occurring in the CE from simple fitness return arguments, (3) show explicitly that setting said fitness gradient equal to zero results in the classical marginal value principle from evolutionary ecology, (4) show that the latter in turn is equivalent to Pontryagin's maximum principle, a well known equivalence that however in the literature is given either ex cathedra or is proven with more advanced tools, (5) connect the classical optimisation arguments of life history theory a little better to real biology (Mendelian populations with separate sexes subject to an environmental feedback loop), (6) make a minor improvement to the form of the CE for the examples in Dieckmann et al. and Parvinen et al.

Information-Mediated Allee Effects in Breeding Habitat Selection.

Social information is used widely in breeding habitat selection and provides an efficient means for individuals to select habitat, but the population-level consequences of this process are not well explored. At low population densities, efficiencies may be reduced because there are insufficient information providers to cue high-quality habitat. This constitutes what we call an information-mediated Allee effect. We present the first general model for an information-mediated Allee effect applied to breeding habitat selection and unify personal and social information, Allee effects, and ecological traps into a common framework. In a second model, we consider an explicit mechanism of social information gathering through prospecting on conspecific breeding performance. In each model, we independently vary personal and social information use to demonstrate how dependency on social information may result in either weak or strong Allee effects that, in turn, affect population extinction risk. Abrupt transitions between outcomes can occur through reduced information transfer or small changes in habitat composition. Overall, information-mediated Allee effects may produce positive feedbacks that amplify population declines in species that are already experiencing environmentally driven stressors, such as habitat loss and degradation. Alternatively, social information has the capacity to rescue populations from ecological traps.

Phenology of two interdependent traits in migratory birds in response to climate change.

In migratory birds, arrival date and hatching date are two key phenological markers that have responded to global warming. A body of knowledge exists relating these traits to evolutionary pressures. In this study, we formalize this knowledge into general mathematical assumptions, and use them in an ecoevolutionary model. In contrast to previous models, this study novelty accounts for both traits-arrival date and hatching date-and the interdependence between them, revealing when one, the other or both will respond to climate. For all models sharing the assumptions, the following phenological responses will occur. First, if the nestling-prey peak is late enough, hatching is synchronous with, and arrival date evolves independently of, prey phenology. Second, when resource availability constrains the length of the pre-laying period, hatching is adaptively asynchronous with prey phenology. Predictions for both traits compare well with empirical observations. In response to advancing prey phenology, arrival date may advance, remain unchanged, or even become delayed; the latter occurring when egg-laying resources are only available relatively late in the season. The model shows that asynchronous hatching and unresponsive arrival date are not sufficient evidence that phenological adaptation is constrained. The work provides a framework for exploring microevolution of interdependent phenological traits.

Enhanced science-stakeholder communication to improve ecosystem model performances for climate change impact assessments.

In recent years, climate impact assessments of relevance to the agricultural and forestry sectors have received considerable attention. Current ecosystem models commonly capture the effect of a warmer climate on biomass production, but they rarely sufficiently capture potential losses caused by pests, pathogens and extreme weather events. In addition, alternative management regimes may not be integrated in the models. A way to improve the quality of climate impact assessments is to increase the science-stakeholder collaboration, and in a two-way dialog link empirical experience and impact modelling with policy and strategies for sustainable management. In this paper we give a brief overview of different ecosystem modelling methods, discuss how to include ecological and management aspects, and highlight the importance of science-stakeholder communication. By this, we hope to stimulate a discussion among the science-stakeholder communities on how to quantify the potential for climate change adaptation by improving the realism in the models.

Life-history differences favor evolution of male dimorphism in competitive games.

Many species exhibit two discrete male morphs: fighters and sneakers. Fighters are large and possess weapons but may mature slowly. Sneakers are small and have no weapons but can sneak matings and may mature quickly to start mating earlier in life than fighters. However, how differences in competitive ability and life history interact to determine male morph coexistence has not yet been investigated within a single framework. Here we integrate demography and game theory into a two-sex population model to study the evolution of strategies that result in the coexistence of fighters and sneakers. We incorporate differences in maturation time between the morphs and use a mating-probability matrix analogous to the classic hawk-dove game. Using adaptive dynamics, we show that male dimorphism evolves more easily in our model than in classic game theory approaches. Our results also revealed an interaction between life-history differences and sneaker competitiveness, which shows that demography and competitive games should be treated as interlinked mechanisms to understand the evolution of male dimorphism. Applying our approach to empirical data on bulb mites (Rhizoglyphus robini), coho salmon (Oncorhynchus kisutch), and bullhorned dung beetles (Onthophagus taurus) indicates that observed occurrences of male dimorphism are in general agreement with model predictions.

Adaptation of reproductive phenology to climate change with ecological feedback via dominance hierarchies.

Phenological shifts belong to the most commonly observed biological responses to recent climate change. It is, however, often unclear how these shifts are linked to demography and competitive interactions. We develop an eco-evolutionary model to study adaptation of timing of reproduction in organisms with social dominance hierarchies. We focus on residential birds with winter flocks, where success in competition for territories among offspring depends on ranking given by prior residence. We study the effects of environmental change on breeding population densities, ensuing selection pressures and long-term evolutionary equilibria. We consider changes in food peak date, in winter survival, in total reproductive output and in the width of the food distribution. We show that the evolutionarily stable hatching date will advance with increasing winter survival and reproductive output since these parameters increase habitat saturation and post-fledging competition. Increasing the length of the breeding season also selects for earlier hatching date due to the reduced costs for producing offspring with high ranking. Our analysis shows that there is little correlation between short-term and long-term population responses across different scenarios of environmental change. However, short-term population growth consistently predicts selection for earlier reproduction. Hence, the model identifies changed breeding population density as a key factor to understanding phenological adaptation in systems with prior residence advantages. While selection for change in reproductive phenology is often explained by changed seasonal variation in environmental variables, such as food abundance, we show that environmental change without apparent effects on seasonality can critically affect phenological adaptation. Such factors can mask or even override influences of changed seasonality on phenology. The model thus offers a conceptually new set of explanations for understanding phenological and demographic trends in a changing climate.

Phenological evolution in annual plants under light competition, changes in the growth season and mass loss.

Flowering time is an important phenological trait in plants and a critical determinant of the success of pollination and fruit or seed development, with immense significance for agriculture as it directly affects crop yield and overall food production. Shifts in the growth season, changes in the growth season duration and changes in the production rate are environmental processes (potentially linked to climate change) that can lead to changes in flowering time in the long-term due to selection. In contrast, biomass loss (due to, for example, herbivory or diseases) can have profound consequences for plant mass production and food security. We model the effects of these environmental processes on the flowering time evolutionarily stable strategy (ESS) of annual plants and the potential consequences for reproductive output. Our model recapitulates previous theoretical results linked to climate change and light competition and makes novel predictions about the effects of biomass loss on the evolution of flowering time. Our analysis elucidates how both the magnitude and direction of the evolutionary response can depend on whether biomass loss occurs during the earlier vegetative phase or during the later reproductive phase and on whether or not plants are adapted to grow in dense, competitive environments. Specifically, light competition generates an asymetric effect of mass loss on flowering time even when loss is indiscriminate (equal rates), with vegetative mass loss having a stronger effect on flowering time (resulting in greater ESS change) and final reproductive output.

Game theory sheds new light on ecological responses to current climate change when phenology is historically mismatched.

Phenological changes are well documented biological effects of current climate change but their adaptive value and demographic consequences are poorly known. Game theoretical models have shown that deviating from the fitness-maximising phenology can be evolutionary stable under frequency-dependent selection. We study eco-evolutionary responses to climate change when the historical phenology is mismatched in this way. For illustration we model adaptation of arrival dates in migratory birds that compete for territories at their breeding grounds. We simulate climate change by shifting the timing and the length of the favourable season for breeding. We show that initial trends in changes of population densities can be either reinforced or counteracted during the ensuing evolutionary adaptation. We find in total seven qualitatively different population trajectories during the transition to a new evolutionary equilibrium. This surprising diversity of eco-evolutionary responses provides adaptive explanations to the observed variation in phenological responses to recent climate change.

Effects of territory competition and climate change on timing of arrival to breeding grounds: a game-theory approach.

Phenology is an important part of life history that is gaining increased attention because of recent climate change. We use game theory to model phenological adaptation in migratory birds that compete for territories at their breeding grounds. We investigate how the evolutionarily stable strategy (ESS) for the timing of arrival is affected by changes in the onset of spring, the timing of the resource peak, and the season length. We compare the ESS mean arrival date with the environmental optimum, that is, the mean arrival date that maximizes fitness in the absence of competition. When competition is strong, the ESS mean arrival date responds less than the environmental optimum to shifts in the resource peak but more to changes in the onset of spring. Increased season length may not necessarily affect the environmental optimum but can still advance the ESS mean arrival date. Conversely, shifting a narrow resource distribution may change the environmental optimum without affecting the ESS mean arrival date. The ESS mean arrival date and the environmental optimum may even shift in different directions. Hence, treating phenology as an evolutionary game rather than an optimization problem fundamentally changes what we predict to be an adaptive response to environmental changes.

Strengthening the evidence base for temperature-mediated phenological asynchrony and its impacts.

Climate warming has caused the seasonal timing of many components of ecological food chains to advance. In the context of trophic interactions, the match-mismatch hypothesis postulates that differential shifts can lead to phenological asynchrony with negative impacts for consumers. However, at present there has been no consistent analysis of the links between temperature change, phenological asynchrony and individual-to-population-level impacts across taxa, trophic levels and biomes at a global scale. Here, we propose five criteria that all need to be met to demonstrate that temperature-mediated trophic asynchrony poses a growing risk to consumers. We conduct a literature review of 109 papers studying 129 taxa, and find that all five criteria are assessed for only two taxa, with the majority of taxa only having one or two criteria assessed. Crucially, nearly every study was conducted in Europe or North America, and most studies were on terrestrial secondary consumers. We thus lack a robust evidence base from which to draw general conclusions about the risk that climate-mediated trophic asynchrony may pose to populations worldwide.

The risk of competitive exclusion during evolutionary branching: effects of resource variability, correlation and autocorrelation.

Evolutionary branching has been suggested as a mechanism to explain ecological speciation processes. Recent studies indicate however that demographic stochasticity and environmental fluctuations may prevent branching through stochastic competitive exclusion. Here we extend previous theory in several ways; we use a more mechanistic ecological model, we incorporate environmental fluctuations in a more realistic way and we include environmental autocorrelation in the analysis. We present a single, comprehensible analytical result which summarizes most effects of environmental fluctuations on evolutionary branching driven by resource competition. Corroborating earlier findings, we show that branching may be delayed or impeded if the underlying resources have uncorrelated or negatively correlated responses to environmental fluctuations. There is also a strong impeding effect of positive environmental autocorrelation, which can be related to results from recent experiments on adaptive radiation in bacterial microcosms. In addition, we find that environmental fluctuations can lead to cycles of repeated branching and extinction.

Is timing of reproduction according to temperature sums an optimal strategy?

Temperature sums are widely used to predict the seasonal timing of yearly recurring biological events, such as flowering, budburst, and hatching. We use a classic energy allocation model for annual plants to compare a strategy for reproductive timing that follows a temperature sum rule (TSR) with a strategy that follows an optimal control rule (OCR) maximizing reproductive output. We show that the OCR corresponds to a certain TSR regardless of how temperature is distributed over the growing season as long as the total temperature sum over the whole growing season is constant between years. We discuss such scenarios, thus outlining under which type of variable growth conditions TSR maximizes reproductive output and should be favored by natural selection. By providing an ultimate explanation for a well-documented empirical pattern this finding enhances the credibility of temperature sums as predictors of the timing of biological events. However, TSR and OCR respond in opposite directions when the total yearly temperature sum changes between years, representing, for example, variation in the length of the growing season. Our findings have implications for predicting optimal responses of organisms to climatic changes and suggest under which conditions natural selection should favor photoperiod versus temperature control.

Evolutionary responses to environmental changes: how does competition affect adaptation?

The role and importance of ecological interactions for evolutionary responses to environmental changes is to large extent unknown. Here it is shown that interspecific competition may slow down rates of adaptation substantially and fundamentally change patterns of adaptation to long-term environmental changes. In the model investigated here, species compete for resources distributed along an ecological niche space. Environmental change is represented by a slowly moving resource maximum and evolutionary responses of single species are compared with responses of coalitions of two and three competing species. In scenarios with two and three species, species that are favored by increasing resource availability increase in equilibrium population size whereas disfavored species decline in size. Increased competition makes it less favorable for individuals of a disfavored species to occupy a niche close to the maximum and reduces the selection pressure for tracking the moving resource distribution. Individual-based simulations and an analysis using adaptive dynamics show that the combination of weaker selection pressure and reduced population size reduces the evolutionary rate of the disfavored species considerably. If the resource landscape moves stochastically, weak evolutionary responses cause large fluctuations in population size and thereby large extinction risk for competing species, whereas a single species subject to the same environmental variability may track the resource maximum closely and maintain a much more stable population size. Other studies have shown that competitive interactions may amplify changes in mean population sizes due to environmental changes and thereby increase extinction risks. This study accentuates the harmful role of competitive interactions by illustrating that they may also decrease rates of adaptation. The slowdown in evolutionary rates caused by competition may also contribute to explain low rates of morphological change in spite of large environmental fluctuations found in fossil records.

Twelve fundamental life histories evolving through allocation-dependent fecundity and survival.

An organism's life history is closely interlinked with its allocation of energy between growth and reproduction at different life stages. Theoretical models have established that diminishing returns from reproductive investment promote strategies with simultaneous investment into growth and reproduction (indeterminate growth) over strategies with distinct phases of growth and reproduction (determinate growth). We extend this traditional, binary classification by showing that allocation-dependent fecundity and mortality rates allow for a large diversity of optimal allocation schedules. By analyzing a model of organisms that allocate energy between growth and reproduction, we find twelve types of optimal allocation schedules, differing qualitatively in how reproductive allocation increases with body mass. These twelve optimal allocation schedules include types with different combinations of continuous and discontinuous increase in reproduction allocation, in which phases of continuous increase can be decelerating or accelerating. We furthermore investigate how this variation influences growth curves and the expected maximum life span and body size. Our study thus reveals new links between eco-physiological constraints and life-history evolution and underscores how allocation-dependent fitness components may underlie biological diversity.

Will sympatric speciation fail due to stochastic competitive exclusion?

Sympatric speciation requires coexistence of the newly formed species. If divergence proceeds by small mutational steps, the new species utilize almost the same resources initially, and full speciation may be impeded by competitive exclusion in stochastic environments. We investigate this primarily ecological problem of sympatric speciation by studying the population dynamics of a diverging asexual population in a fluctuating environment. Correlation between species responses to environmental fluctuation is assumed to decrease with distance in trait space. Rapidly declining correlation in combination with high environmental variability may delay full speciation or even render it impossible. Stochastic extinctions impeding speciation are most likely when correlation decays faster than competition, for example, when demographic stochasticity is strong or when divergence is not accompanied by niche separation, such as in speciation driven entirely by sexual selection. Our general theoretical results show an interesting connection between short-term ecological dynamics and long-term, large-scale evolution.

Climate change and the optimal flowering time of annual plants in seasonal environments.

Long-term phenology monitoring has documented numerous examples of changing flowering dates during the last century. A pivotal question is whether these phenological responses are adaptive or not under directionally changing climatic conditions. We use a classic dynamic growth model for annual plants, based on optimal control theory, to find the fitness-maximizing flowering time, defined as the switching time from vegetative to reproductive growth. In a typical scenario of global warming, with advanced growing season and increased productivity, optimal flowering time advances less than the start of the growing season. Interestingly, increased temporal spread in production over the season may either advance or delay the optimal flowering time depending on overall productivity or season length. We identify situations where large phenological changes are necessary for flowering time to remain optimal. Such changes also indicate changed selection pressures. In other situations, the model predicts advanced phenology on a calendar scale, but no selection for early flowering in relation to the start of the season. We also show that the optimum is more sensitive to increased productivity when productivity is low than when productivity is high. All our results are derived using a general, graphical method to calculate the optimal flowering time applicable for a large range of shapes of the seasonal production curve. The model can thus explain apparent maladaptation in phenological responses in a multitude of scenarios of climate change. We conclude that taking energy allocation trade-offs and appropriate time scales into account is critical when interpreting phenological patterns.

An eco-evolutionary model for demographic and phenological responses in migratory birds.

Many migratory birds have changed their timing of arrival at breeding grounds in response to recent climate change. Understanding the adaptive value and the demographic consequences of these shifts are key challenges. To address these questions we extend previous models of phenological adaptation to climate change under territory competition to include feedback from population dynamics, winter survival and habitat productivity. We study effects of improved pre-breeding survival and of earlier food abundance peak. We show that phenological responses depend strongly on equilibrium population density via effects on territory competition. When density is high, improved pre-breeding survival affects selection pressures more than shifts of the resource peak. Under certain conditions, an advanced food peak can even select for later arrival due to competitive release. Improved pre-breeding survival has positive effects on population density that in many cases is stronger than negative effects of an advanced food peak. The fraction of young in the population decreases in all scenarios of change, but food peak shifts only affect population structure marginally unless population density is low. This work thus provides several missing links between phenological adaptation and demographic responses, and augments the toolbox for interpreting ongoing phenological shifts in migratory birds. We illustrate the utility of our model by explaining different patterns in demographic trends and phenological shifts in populations of Pied flycatchers (Ficedula hypoleuca) across Western Europe.