Integrating animal behaviour into research on multiple environmental stressors: a conceptual framework.

While a large body of research has focused on the physiological effects of multiple environmental stressors, how behavioural and life-history plasticity mediate multiple-stressor effects remains underexplored. Behavioural plasticity can not only drive organism-level responses to stressors directly but can also mediate physiological responses. Here, we provide a conceptual framework incorporating four fundamental trade-offs that explicitly link animal behaviour to life-history-based pathways for energy allocation, shaping the impact of multiple stressors on fitness. We first address how small-scale behavioural changes can either mediate or drive conflicts between the effects of multiple stressors and alternative physiological responses. We then discuss how animal behaviour gives rise to three additional understudied and interrelated trade-offs: balancing the benefits and risks of obtaining the energy needed to cope with stressors, allocation of energy between life-history traits and stressor responses, and larger-scale escape from stressors in space or time via large-scale movement or dormancy. Finally, we outline how these trade-offs interactively affect fitness and qualitative ecological outcomes resulting from multiple stressors. Our framework suggests that explicitly considering animal behaviour should enrich our mechanistic understanding of stressor effects, help explain extensive context dependence observed in these effects, and highlight promising avenues for future empirical and theoretical research.

Polyandry as a Male Strategy? A Game between Aggressive and Tolerant Males, Arbitrated by Females.

AbstractUnrelated males sometimes share their nests and their mates, an example of male-male cooperation that calls for an evolutionary explanation. We developed a game-theoretic model of this situation under the assumption that males could be either "aggressors," attempting to drive off any other arriving male, or "tolerators," willing to share a nest and mates with another tolerator male. We modeled nest dynamics by changing the frequency of the two types in the population and determined how this affected their fitness. We use the sea lamprey as a case study to generate a plausible array of behavioral traits and ecological conditions for the model. Under these conditions, only aggressors or only tolerators could persist, not both, but we also show how exceptions can arise. Aggressors predominated for the standard conditions we chose, but tolerators could take over when females favored them through nest choice or increased mating rate. High nesting densities and high fighting costs also tended to favor tolerators. At moderate to low densities of individuals in the nesting area, female behavior, based on their own costs and benefits, should determine the outcome.

Resolving conflict over within-pair mating rate in external fertilizers.

Besides egg fertilization, females of many taxa obtain direct fitness benefits from male mates, such as food, protection or paternal care. But males often increase their own fitness by mating with several females, among which they distribute sperm along with the above-mentioned benefits, reducing the benefits to individual females. These diverging interests lead to a conflict in which each female may try to ensure male fidelity and get exclusive access to male-provided benefits. Here, we use a theoretical model to show how a female of an externally fertilizing species may achieve mate fidelity by soliciting copulations at such a rate that the male has insufficient sperm left to increase his fitness with additional females. We show that three alternative condition-dependent evolutionarily stable mating relationships emerge in this scenario, based on whether one mate's preference for mating rate dominates, or the conflict is resolved by what amounts to negotiation. We demonstrate how these outcomes depend on some features of physiology, ecology, and behavior. In particular, a greater reproductive benefit to a female from exclusive access to a male partner-or the occasional tendency of females to withhold eggs during mating-can increase male fidelity; and continuous sperm regeneration rather than an initially-set stock of sperm allows for multiple within-pair mating across all three mating patterns.

Theory of environmental sex determination: Trending populations in stressful environments.

Species that have sex determined by environmental conditions during development (i.e., environmental sex determination [ESD]) are especially vulnerable to environmental change, including altered stress levels, habitat loss, and species translocations. These factors can produce multigenerational trends in population size and eco-evolutionary dynamics not captured by existing theory based on lifetime reproductive success (R0 ). Here, we extend ESD theory to use per capita growth rate r as a more appropriate measure of evolutionary success (fitness), and we demonstrate the importance of this change when males and females can differ in maturation times and when maturation times vary with local conditions (plasticity). In these cases, we show that primary and secondary sex ratios may be strongly biased; that optimal maturation times, when locally plastic, depend on the balance between mortality and growth effects; and that plasticity of maturation times can ameliorate fitness costs of increasing environmental stress.

Model and Data Concur and Explain the Coexistence of Two Very Distinct Animal Behavioral Types.

Behaviors may enhance fitness in some situations while being detrimental in others. Linked behaviors (behavioral syndromes) may be central to understanding the maintenance of behavioral variability in natural populations. The spillover hypothesis of premating sexual cannibalism by females explains genetically determined female aggression towards both prey and males: growth to a larger size translates into higher fecundity, but at the risk of insufficient sperm acquisition. Here, we use an individual-based model to determine the ecological scenarios under which this spillover strategy is more likely to evolve over a strategy in which females attack approaching males only once the female has previously secured sperm. We found that a classic spillover strategy could never prevail. However, a more realistic early-spillover strategy, in which females become adults earlier in addition to reaching a larger size, could be maintained in some ecological scenarios and even invade a population of females following the other strategy. We also found under some ecological scenarios that both behavioral types coexist through frequency-dependent selection. Additionally, using data from the spider Lycosa hispanica, we provide strong support for the prediction that the two strategies may coexist in the wild. Our results clarify how animal personalities evolve and are maintained in nature.

Nonconsumptive predator effects modify crayfish-induced bioturbation as mediated by limb loss: Field and mesocosm experiments.

We addressed the implications of limb loss and regeneration for multispecies interactions and their impacts on ecosystem engineering in freshwater stream environments.We included regenerative and nonregenerative crayfish as well as fish predators in a 2 × 2 factorial design to assess the effects on water turbidity of interactions between crayfish ecosystem engineers differing in regenerative status and their fish predators.We demonstrated that crayfish limb loss and predation risks lead to more turbidity in field and mesocosm conditions. Moreover, ongoing regeneration of crayfish increased turbidity, while fish presence seemed to hinder crayfish turbidity-inducing behaviors (such as tail-flipping and burrowing) in the mesocosm experiment.We confirmed that greater numbers of crayfish produce a greater amount of turbidity in situ in streams.Although mechanical burrowing crayfish capacities may depend on crayfish burrowing classification (primary, secondary, or tertiary), our work emphasizes the implication for turbidity levels of crayfish autotomy in freshwater streams.

Self-Deception about Fecundity in Women : Modeling the Burley Hypothesis.

Concealed fecundity and extended female sexual receptivity have evolved in some primates, including humans, conferring advantages both within primarily monogamous relationships (e.g., benefits from paternity assurance) and from extrapair liaisons (e.g., better access to good genes). As humans evolved the intellectual capacity for decision-making, women became capable of altering their own fertility. In some circumstances, they may choose to ameliorate risks and responsibilities associated with pregnancy by reducing sexual motivation near the perceived most fecund time of their menstrual cycle. But three findings-a general inability of women to accurately recognize their own intervals of fecundity, high variability in ovulation timing, and unconscious transmission and reception of cues associated with fecundity-constitute a physiological and behavioral syndrome that can be considered self-deception. In this study, I develop a descriptive model to determine implications of the hypothesis that these features of female and male physiology and behavior have been shaped by natural selection in response to female decision-making. My analysis shows that consensus motivation for coitus between partners influences both the importance of variable ovulation date and the probability of conception, under the influence of self-deception. It also identifies priorities for future empirical work.

Predicting Habitat Choice after Rapid Environmental Change.

Decisions made while searching for settlement sites (e.g., nesting, oviposition) often have major fitness implications. Despite numerous case studies, we lack theory to explain why some species are thriving while others are making poor habitat choices after environmental change. We develop a model to predict (1) which kinds of environmental change have larger, negative effects on fitness, (2) how evolutionary history affects susceptibility to environmental change, and (3) how much lost fitness can be recovered via readjustment after environmental change. We model the common scenario where animals search an otherwise inhospitable matrix, encountering habitats of varying quality and settling when finding a habitat better than a threshold quality level. We consider decisions and fitness before environmental change, immediately following change (assuming that animals continue to use their previously adaptive decision rules), and after optimal readjustment (e.g., via learning or evolution). We find that decreases in survival per time step searching and declines in habitat quality or availability generally have stronger negative effects than reduced season duration. Animals that were adapted to good conditions remained choosy after conditions declined and thus suffered more from environmental change than those adapted to poor conditions. Readjustment recovered much of the fitness lost through a reduction in average habitat quality but recovered much less following reductions in habitat availability or survival while searching. Our model offers novel predictions for empiricists to test as well as suggestions for prioritizing alternative mitigation steps.

Maintenance of brucellosis in Yellowstone bison: linking seasonal food resources, host-pathogen interaction, and life-history trade-offs.

The seasonal availability of food resources is an important factor shaping the life-history strategies of organisms. During times of nutritional restriction, physiological trade-offs can induce periods of immune suppression, thereby increasing susceptibility to infectious disease. Our goal was to provide a conceptual framework describing how the endemic level bovine brucellosis (Brucella abortus) may be maintained in Yellowstone bison based on the seasonality of food resources and the life-history strategies of the host and pathogen. Our analysis was based on active B. abortus infection (measured via bacterial culture), nutritional indicators (measured as metabolites and hormones in plasma), and carcass measurements of 402 slaughtered bison. Data from Yellowstone bison were used to investigate (1) whether seasonal changes in diet quality affect nutritional condition and coincide with the reproductive needs of female bison; (2) whether active B. abortus infection and infection intensities vary with host nutrition and nutritional condition; and (3) the evidence for seasonal changes in immune responses, which may offer protection against B. abortus, in relation to nutritional condition. Female bison experienced a decline in nutritional condition during winter as reproductive demands of late gestation increased while forage quality and availability declined. Active B. abortus infection was negatively associated with bison age and nutritional condition, with the intensity of infection negatively associated with indicators of nutrition (e.g., dietary protein and energy) and body weight. Data suggest that protective cell-mediated immune responses may be reduced during the B. abortus transmission period, which coincides with nutritional insufficiencies and elevated reproductive demands during spring. Our results illustrate how seasonal food restriction can drive physiological trade-offs that suppress immune function and create infection and transmission opportunities for pathogens.

An insect-feeding guild of carnivorous plants and spiders: does optimal foraging lead to competition or facilitation?

Carnivorous plants and spiders, along with their prey, are main players in an insect-feeding guild found on acidic, poorly drained soils in disturbed habitat. Darwin's notion that these plants must actively attract the insects they capture raises the possibility that spiders could benefit from proximity to prey hotspots created by the plants. Alternatively, carnivorous plants and spiders may deplete prey locally or (through insect redistribution) more widely, reducing each other's gain rates from predation. Here, we formulate and analyze a model of this guild, parameterized for carnivorous sundews and lycosid spiders, under assumptions of random movement by insects and optimal foraging by predators. Optimal foraging here involves gain maximization via trap investment (optimal web sizes and sundew trichome densities) and an ideal free distribution of spiders between areas with and without sundews. We find no facilitation: spiders and sundews engage in intense exploitation competition. Insect attraction by plants modestly increases sundew gain rates but slightly decreases spider gain rates. In the absence of population size structure, optimal spider redistribution between areas with and without sundews yields web sizes that are identical for all spiders, regardless of proximity to sundews. Web-building spiders have higher gain rates than wandering spiders in this system at high insect densities, but wandering spiders have the advantage at low insect densities. Results are complex, indicating that predictions to be tested empirically must be based on careful quantitative assessment.

Wolbachia re-replacement without incompatibility: potential for intended and unintended consequences.

Recent releases of mosquitoes infected with different Wolbachia types into Australia have led to conditions that have not been observed naturally and that have not been considered theoretically. In an ongoing public health campaign, two Wolbachia infection types have been introduced, and the infections differ in their fitness cost imposed on the host mosquito. The dynamics of each infection type as it interacts with the indigenous uninfected host population have been previously examined via models and empirical tests. Here we conduct a modeling analysis to predict the dynamics when the two infection types do not remain geographically isolated. The results demonstrate the potential replacement and loss of the more costly infection type, which may not be the desired public health outcome.

Wolbachia infections that reduce immature insect survival: predicted impacts on population replacement.

BACKGROUND: The evolutionary success of Wolbachia bacteria, infections of which are widespread in invertebrates, is largely attributed to an ability to manipulate host reproduction without imposing substantial fitness costs. Here, we describe a stage-structured model with deterministic immature lifestages and a stochastic adult female lifestage. Simulations were conducted to better understand Wolbachia invasions into uninfected host populations. The model includes conventional Wolbachia parameters (the level of cytoplasmic incompatibility, maternal inheritance, the relative fecundity of infected females, and the initial Wolbachia infection frequency) and a new parameter termed relative larval viability (RLV), which is the survival of infected larvae relative to uninfected larvae. RESULTS: The results predict the RLV parameter to be the most important determinant for Wolbachia invasion and establishment. Specifically, the fitness of infected immature hosts must be close to equal to that of uninfected hosts before population replacement can occur. Furthermore, minute decreases in RLV inhibit the invasion of Wolbachia despite high levels of cytoplasmic incompatibility, maternal inheritance, and low adult fitness costs. CONCLUSIONS: The model described here takes a novel approach to understanding the spread of Wolbachia through a population with explicit dynamics. By combining a stochastic female adult lifestage and deterministic immature/adult male lifestages, the model predicts that even those Wolbachia infections that cause minor decreases in immature survival are unlikely to invade and spread within the host population. The results are discussed in relation to recent theoretical and empirical studies of natural population replacement events and proposed applied research, which would use Wolbachia as a tool to manipulate insect populations.

Intraguild mutualism.

Although studies of species linked by a common resource (i.e. ecological guilds) have so far mainly focused on competition and predation, guilds are also good places to find mutualism. In this review we consider some three- and four-species community modules to illustrate examples of wide relevance. Mutualism arises from various direct and indirect trophic and non-trophic interactions between species--and within modules both with and without intraguild predation. Species removal and augmentation experiments, other manipulations, direct measurements, and path-analytic methods can determine the presence and intensity of mutualism within guilds. Such studies, particularly when associated with existing theory and new theoretical development, can help advance an interaction-based approach to community analysis that recognizes linkages among mutualism, predation and competition in natural systems.

Effect of variable transmission rate on the dynamics of HIV in sub-Saharan Africa.

BACKGROUND: The cause of the high HIV prevalence in sub-Saharan Africa is incompletely understood, with heterosexual penile-vaginal transmission proposed as the main mechanism. Heterosexual HIV transmission has been estimated to have a very low probability; but effects of cofactors that vary in space and time may substantially alter this pattern. METHODS: To test the effect of individual variation in the HIV infectiousness generated by co-infection, we developed and analyzed a mathematical sexual network model that simulates the behavioral components of a population from Malawi, as well as the dynamics of HIV and the co-infection effect caused by other infectious diseases, including herpes simplex virus type-2, gonorrhea, syphilis and malaria. RESULTS: The analysis shows that without the amplification effect caused by co-infection, no epidemic is generated, and HIV prevalence decreases to extinction. But the model indicates that an epidemic can be generated by the amplification effect on HIV transmission caused by co-infection. CONCLUSION: The simulated sexual network demonstrated that a single value for HIV infectivity fails to describe the dynamics of the epidemic. Regardless of the low probability of heterosexual transmission per sexual contact, the inclusion of individual variation generated by transient but repeated increases in HIV viral load associated with co-infections may provide a biological basis for the accelerated spread of HIV in sub-Saharan Africa. Moreover, our work raises the possibility that the natural history of HIV in sub-Saharan Africa cannot be fully understood if individual variation in infectiousness is neglected.

HIV-malaria co-infection: effects of malaria on the prevalence of HIV in East sub-Saharan Africa.

OBJECTIVE: To examine the association between malaria and HIV prevalence in East sub-Saharan Africa. METHODS: Using large nationally representative samples of 19,735 sexually active adults from the 2003-04 HIV/AIDS indicator surveys conducted in Kenya, Malawi and Tanzania, and the atlas malaria project, we analysed the relationship between malaria and HIV prevalence adjusting for important socioeconomic and biological cofactors. RESULTS: In adjusted models, individuals who live in areas with high Plasmodium falciparum parasite rate (PfPR > 0.42) had increased estimated odds of being HIV positive than individuals who live in areas with low P. falciparum parasite rate (PfPR ≤ 0.10) [men: estimated odds ratio (OR) 2.24, 95% confidence interval (CI) 1.62-3.12; women: estimated OR 2.44, 95% CI 1.85-3.21]. CONCLUSION: This is the first study to report malaria as a risk factor of concurrent HIV infection at the population level. According to our results, individuals who live in areas with high P. falciparum parasite rate have about twice the risk of being HIV positive compared with individuals who live in areas with low P. falciparum parasite rate. Our work emphasizes the need for field studies focused on quantifying the interaction among parasitic infections and risk of HIV infection, and studies to explore the impact of control interventions. Programmes focused on reducing malaria transmission will be important to address, especially in HIV-infected individuals.

Effectiveness of a 'hunter' virus in controlling human immunodeficiency virus type 1 infection.

Engineered therapeutic viruses provide an alternative method for treating infectious diseases, and mathematical models can clarify the system's dynamics underlying this type of therapy. In particular, this study developed models to evaluate the potential to contain human immunodeficiency virus type 1 (HIV-1) infection using a genetically engineered 'hunter' virus that kills HIV-1-infected cells. First, we constructed a novel model for understanding the progression of HIV infection that predicted the loss of the immune system's CD4(+) T cells across time. Subsequently, it determined the effects of introducing hunter viruses in restoring cell population. The model implemented direct and indirect mechanisms by which HIV-1 may cause cell depletion and an immune response. Results suggest that the slow progression of HIV infection may result from a slowly decaying CTL immune response, leading to a limited but constant removal of uninfected CD4 resting cells through apoptosis - and from resting cell proliferation that reduces the rate of cell depletion over time. Importantly, results show that the hunter virus does restrain HIV infection and has the potential to allow major cell recovery to 'functional' levels. Further, the hunter virus persisted at a reduced HIV load and was effective either early or late in the infection. This study indicates that hunter viruses may halt the progression of the HIV infection by restoring and sustaining high CD4(+) T-cell levels.

Variable valuations and voluntarism under group selection: An evolutionary public goods game.

In biological systems, as in human society, competing social groups may depend heavily on a small number of volunteers to advance the group's prospects. This phenomenon can be understood as the solution to an evolutionary public goods game, in which a beneficent individual or a small number of individuals may place the highest value on group success and contribute the most to achieving it while profiting very little. Here we demonstrate that this type of solution, recently recognized in the social sciences, is evolutionarily stable and evolves in evolutionary simulations sensitive to alternative ways of gaining fitness beyond the present social group. The public goods mechanism may help explain biological voluntarism in cases like predator inspection and foraging on behalf of non-relatives and may determine the extent of commitment to group welfare at different intensities of group selection.

Vaccination strategies for managing brucellosis in Yellowstone bison.

Concerns over migratory bison (Bison bison) at Yellowstone National Park transmitting brucellosis (Brucella abortus) to cattle herds on adjacent lands led to proposals for bison vaccination. We developed an individual-based model to evaluate how brucellosis infection might respond under alternate vaccination strategies, including: (1) vaccination of female calves and yearlings captured at the park boundary when bison move outside the primary conservation area; (2) combining boundary vaccination with the remote delivery of vaccine to female calves and yearlings distributed throughout the park; and (3) vaccinating all female bison (including adults) during boundary capture and throughout the park using remote delivery of vaccine. Simulations suggested Alternative 3 would be most effective, with brucellosis seroprevalence decreasing by 66% (from 0.47 to 0.16) over a 30-year period resulting from 29% of the population receiving protection through vaccination. Under this alternative, bison would receive multiple vaccinations that extend the duration of vaccine protection and defend against recurring infection in latently infected animals. The initial decrease in population seroprevalence will likely be slow due to high initial seroprevalence (40-60%), long-lived antibodies, and the culling of some vaccinated bison that were subsequently exposed to field strain Brucella and reacted positively on serologic tests. Vaccination is unlikely to eradicate B. abortus from Yellowstone bison, but could be an effective tool for reducing the level of infection. Our approach and findings have applicability world-wide for managers dealing with intractable wildlife diseases that cross wildlife-livestock and wildlife-human interfaces and affect public health or economic well-being.

Sex-specific plant responses to light intensity and canopy openness: implications for spatial segregation of the sexes.

In seed plants, the proximate causes of spatial segregation of the sexes (SSS) and its association with environmental variation are thought to be linked to sex-specific morphological and physiological variation. To address the general question of linkage among SSS, plant traits and environmental gradients, Marchantia inflexa was used, for which male plants are found under more open tree canopy than females. We hypothesized that males are adapted to higher light intensity and are better able to tolerate water stress than females, as is the case with seed plants. We tested for sex-specific habitat and trait relationships by quantifying plant traits (morphological and physiological) and estimates of the light conditions (percent canopy openness and light intensity) in the field. Using path analysis, we found that edge pore density in both sexes was negatively correlated with canopy openness, while in males, edge pore density had a weak but positive relationship to light intensity. These responses suggest that canopy openness and light intensity have opposing effects on edge pore density in males and that males might be more responsive to water stress than females. Additionally, the greater importance of female support tissue, which functions as storage, in explaining and being explained by other variables in the path analysis, relative to male support tissue, may reflect sex-specific allocation differences related to resources needed for female function.