Maintenance of Behavioral Variation under Predation Risk: Effects on Personality, Plasticity, and Predictability.

AbstractClassic evolutionary theory predicts that predation will shift trait means and erode variance within prey species; however, several studies indicate higher behavioral trait variance and trait integration in high-predation populations. These results come predominately from field-sampled animals comparing low- and high-predation sites and thus cannot isolate the role of predation from other ecological factors, including density effects arising from higher predation. Here, we study the role of predation on behavioral trait (co)variation in experimental populations of guppies (Poecilia reticulata) living with and without a benthic ambush predator (Jaguar cichlid) to better evaluate the role of predation and where density was equalized among replicates twice per year. At 2.5 years after introduction of the predators (∼10 overlapping generations), 40 males were sampled from each of the six replicate populations and extensively assayed for activity rates, water column use, and latency to feed following disturbance. Individual variation was pronounced in both treatments, with substantial individual variation in means, temporal plasticity, and predictability (inverse residual variance). Predators had little effect on mean behavior, although there was some evidence for greater use of the upper water column in predator-exposed fish. There was greater variance among individuals in water column use in predator-exposed fish, and they habituated more quickly over time; individuals higher in the water column fed slower and had a reduced positive correlation with activity, although again this effect was time specific. Predators also affected the integration of personality and plasticity-among-individual variances in water column use increased, and those in activity decreased, through time-which was absent in controls. Our results contrast with the extensive guppy literature showing rapid evolution in trait means, demonstrating either increases or maintenance of behavioral variance under predation.

The effect of mitochondrial recombination on fertilization success in blue mussels.

The presence of doubly uniparental inheritance (DUI) in bivalves represents a unique mode of mitochondrial transmission, whereby paternal (male-transmitted M-type) and maternal (female-transmitted F-type) haplotypes are transmitted to offspring separately. Male embryos retain both haplotypes, but the M-type is selectively removed from females. Due to the presence of heteroplasmy in males, mtDNA can recombine resulting in a 'masculinized' haplotype referred to as Mf-type. While mtDNA recombination is usually rare, it has been recorded in multiple mussel species across the Northern Hemisphere. Given that mitochondria are the powerhouse of the cell, different mtDNA haplotypes may have different selective advantages under diverse environmental conditions. This may be particularly important for sperm fitness and fertilization success. In this study we aimed to i) determine the presence, prevalence of the Mf-type in Australian blue mussels (Mytilus sp.) and ii) investigate the effect of Mf-mtDNA on sperm performance (a fitness correlate). We found a high prevalence of recombined mtDNA (≈35 %) located within the control region of the mitochondrial genome, which occurred only in specimens that contained Southern Hemisphere mtDNA. The presence of two female mitotypes were identified in the studied mussels, one likely originating from the Northern Hemisphere, and the other either representing the endemic M. planulatus species or introduced genotypes from the Southern Hemisphere. Despite having recombination events present in a third of the studied population, analysis of sperm performance indicated no difference in fertilization success related to mitotype.

The impact of food availability on tumorigenesis is evolutionarily conserved.

The inability to control cell proliferation results in the formation of tumors in many multicellular lineages. Nonetheless, little is known about the extent of conservation of the biological traits and ecological factors that promote or inhibit tumorigenesis across the metazoan tree. Particularly, changes in food availability have been linked to increased cancer incidence in humans, as an outcome of evolutionary mismatch. Here, we apply evolutionary oncology principles to test whether food availability, regardless of the multicellular lineage considered, has an impact on tumorigenesis. We used two phylogenetically unrelated model systems, the cnidarian Hydra oligactis and the fish Danio rerio, to investigate the impact of resource availability on tumor occurrence and progression. Individuals from healthy and tumor-prone lines were placed on four diets that differed in feeding frequency and quantity. For both models, frequent overfeeding favored tumor emergence, while lean diets appeared more protective. In terms of tumor progression, high food availability promoted it, whereas low resources controlled it, but without having a curative effect. We discuss our results in light of current ideas about the possible conservation of basic processes governing cancer in metazoans (including ancestral life history trade-offs at the cell level) and in the framework of evolutionary medicine.

A novel perspective suggesting high sustained energy expenditure may be net protective against cancer.

Energy expenditure (EE) is generally viewed as tumorigenic, due to production of reactive oxygen species (ROS) that can damage cells and DNA. On this basis, individuals within a species that sustain high EE should be more likely to develop cancer. Here, we argue the opposite, that high EE may be net protective effect against cancer, despite high ROS production. This is possible because individuals that sustain high EE have a greater energetic capacity (=greater energy acquisition, expenditure and ability to up-regulate output), and can therefore allocate energy to multiple cancer-fighting mechanisms with minimal energetic trade-offs. Our review finds that individuals sustaining high EE have greater antioxidant production, lower oxidative stress, greater immune function and lower cancer incidence. Our hypothesis and literature review suggest that EE may indeed be net protective against cancer, and that individual variation in energetic capacity may be a key mechanism to understand the highly individual nature of cancer risk in contemporary human populations and laboratory animals. Lay summary The process of expending energy generates reactive oxygen species that can lead to oxidative stress, cell and DNA damage, and the accumulation of this damage is thought to be a major contributor to many ageing related diseases that include cancer. Here, we challenge this view, proposing how and why high energy expenditure (EE) may actually be net protective against cancer, and provide literature support for our hypothesis. We find individuals with high sustained EE have greater energetic capacity and thus can invest more in repair to counter oxidative stress, and more in immune function, both of which reduce cancer risk. Our hypothesis provides a novel mechanism to understand the highly individual nature of cancer, why taller individuals are more at risk, why physically active individuals have lower cancer risk, and why regular exercise can reduce cancer risk.

Rainfall driven and wild-bird mediated avian influenza virus outbreaks in Australian poultry.

Globally, outbreaks of Avian Influenza Virus (AIV) in poultry continue to burden economies and endanger human, livestock and wildlife health. Wild waterbirds are often identified as possible sources for poultry infection. Therefore, it is important to understand the ecological and environmental factors that directly influence infection dynamics in wild birds, as these factors may thereby indirectly affect outbreaks in poultry. In Australia, where large parts of the country experience erratic rainfall patterns, intense rainfalls lead to wild waterfowl breeding events at temporary wetlands and increased proportions of immunologically naïve juvenile birds. It is hypothesized that after breeding, when the temporary wetlands dry, increasing densities of immunologically naïve waterbirds returning to permanent water bodies might strongly contribute to AIV prevalence in wild waterfowl in Australia. Since rainfall has been implicated as an important environmental driver in AIV dynamics in wild waterbirds in southeast Australia and wild waterbirds are identified globally to have a role in virus spillover into poultry, we hypothesise that rainfall events have an indirect effect on AIV outbreaks in poultry in southeast Australia. In this study we investigated this hypothesis by examining the correlation between the timing of AIV outbreaks in poultry in and near the Murray-Darling basin in relation to temporal patterns in regional rainfall since 1970. Our findings support our hypothesis and suggest that the risk of AIV outbreaks in poultry increases after a period of high rainfall, with peak AIV risk two years after the onset of the high-rainfall period. This is presumably triggered by increased rates of waterbird breeding and consequent higher proportions of immunologically naïve juvenile waterbirds entering the population directly after major rainfall events, which subsequently aggregate near permanent water bodies when the landscape dries out.

Understanding the unexplained: The magnitude and correlates of individual differences in residual variance.

Behavioral and physiological ecologists have long been interested in explaining the causes and consequences of trait variation, with a focus on individual differences in mean values. However, the majority of phenotypic variation typically occurs within individuals, rather than among individuals (as indicated by average repeatability being less than 0.5). Recent studies have further shown that individuals can also differ in the magnitude of variation that is unexplained by individual variation or environmental factors (i.e., residual variation). The significance of residual variation, or why individuals differ, is largely unexplained, but is important from evolutionary, methodological, and statistical perspectives. Here, we broadly reviewed literature on individual variation in behavior and physiology, and located 39 datasets with sufficient repeated measures to evaluate individual differences in residual variance. We then analyzed these datasets using methods that permit direct comparisons of parameters across studies. This revealed substantial and widespread individual differences in residual variance. The magnitude of individual variation appeared larger in behavioral traits than in physiological traits, and heterogeneity was greater in more controlled situations. We discuss potential ecological and evolutionary implications of individual differences in residual variance and suggest productive future research directions.

Ecological and Evolutionary Consequences of Anticancer Adaptations.

Cellular cheating leading to cancers exists in all branches of multicellular life, favoring the evolution of adaptations to avoid or suppress malignant progression, and/or to alleviate its fitness consequences. Ecologists have until recently largely neglected the importance of cancer cells for animal ecology, presumably because they did not consider either the potential ecological or evolutionary consequences of anticancer adaptations. Here, we review the diverse ways in which the evolution of anticancer adaptations has significantly constrained several aspects of the evolutionary ecology of multicellular organisms at the cell, individual, population, species, and ecosystem levels and suggest some avenues for future research.

Can Energetic Capacity Help Explain Why Physical Activity Reduces Cancer Risk?

Increased physical activity reduces cancer risk in humans, but why this whole-organism attribute reduces cancer remains unclear. Active individuals tend to have high capacity to generate energy on a sustained basis, which in turn can permit greater immune responses crucial for fighting emerging neoplasia. Thus, we suggest energetic capacity as a potential mechanism to explain the activity-cancer link, given that humans are intrinsically (not externally) energy limited. Human and rodent studies show that individuals with high energetic capacity mount greater immune responses and have lower cancer incidence; these trends persist after controlling for actual physical activity, supporting a direct role of energetic capacity. If true, exercise efforts might best target those that increase one's energetic capacity, which may be both individual and exercise specific.

Obesity paradox in cancer: Is bigger really better?

While obesity is widely recognized as a risk factor for cancer, survival among patients with cancer is often higher for obese than for lean individuals. Several hypotheses have been proposed to explain this "obesity paradox," but no consensus has yet emerged. Here, we propose a novel hypothesis to add to this emerging debate which suggests that lean healthy persons present conditions unfavorable to malignant transformation, due to powerful natural defenses, whereby only rare but aggressive neoplasms can emerge and develop. In contrast, obese persons present more favorable conditions for malignant transformation, because of several weight-associated factors and less efficient natural defenses, leading to a larger quantity of neoplasms comprising both nonaggressive and aggressive ones to regularly emerge and progress. If our hypothesis is correct, testing would require the consideration of the raw quantity, not the relative frequency, of aggressive cancers in obese patients compared with lean ones. We also discuss the possibility that in obese persons, nonaggressive malignancies may prevent the subsequent progression of aggressive cancers through negative competitive interactions between tumors.

Metabolic Scope as a Proximate Constraint on Individual Behavioral Variation: Effects on Personality, Plasticity, and Predictability.

Behavioral ecologists have hypothesized that among-individual differences in resting metabolic rate (RMR) may predict consistent individual differences in mean values for costly behaviors or for behaviors that affect energy intake rate. This hypothesis has empirical support and presently attracts considerable attention, but, notably, it does not provide predictions for individual differences in (a) behavioral plasticity or (b) unexplained variation (residual variation from mean individual behavior, here termed predictability). We outline how consideration of aerobic maximum metabolic rate (MMR) and particularly aerobic scope (= MMR - RMR) can be used to simultaneously make predictions about mean and among- and within-individual variation in behavior. We predict that while RMR should be proportional to an individual's mean level of sustained behavioral activity (one aspect of its personality), individuals with greater aerobic scope will also have greater scope to express behavioral plasticity and/or greater unpredictability in behavior (=greater residual variation). As a first step toward testing these predictions, we analyze existing activity data from selectively bred lines of mice that differ in both daily activity and aerobic scope. We find that replicate high-scope mice are more active on average and show greater among-individual variation in activity, greater among-individual variation in plasticity, and greater unpredictability. These data provide some tentative first support for our hypothesis, suggesting that further research on this topic would be valuable.

Cancer Is Not (Only) a Senescence Problem.

Age is one of the strongest predictors of cancer and risk of death from cancer. Cancer is therefore generally viewed as a senescence-related malady. However, cancer also exists at subclinical levels in humans and other animals, but its earlier effects on the body are poorly known by comparison. We argue here that cancer is a significant but ignored burden on the body and is likely to be a strong selective force from early during the lifetime of an organism. It is time to adopt this novel view of malignant pathologies to improve our understanding of the ways in which oncogenic phenomena influence the ecology and evolution of animals long before their negative impacts become evident and fatal.

Changes in diet associated with cancer: An evolutionary perspective.

Changes in diet are frequently correlated with the occurrence and progression of malignant tumors (i.e., cancer) in both humans and other animals, but an integrated conceptual framework to interpret these changes still needs to be developed. Our aim is to provide a new perspective on dietary changes in tumor-bearing individuals by adapting concepts from parasitology. Dietary changes may occur alongside tumor progression for several reasons: (i) as a pathological side effect with no adaptive value, (ii) as the result of self-medication by the host to eradicate the tumor and/or to slow down its progression, (iii) as a result of host manipulation by the tumor that benefits its progression, and finally (iv) as a host tolerance strategy, to alleviate and repair damages caused by tumor progression. Surprisingly, this tolerance strategy can be beneficial for the host even if diet changes are beneficial to tumor progression, provided that cancer-induced death occurs sufficiently late (i.e., when natural selection is weak). We argue that more data and a unifying evolutionary framework, especially during the early stages of tumorigenesis, are needed to understand the links between changes in diet and tumor progression. We argue that a focus on dietary changes accompanying tumor progression can offer novel preventive and therapeutic strategies against cancer.

Cancer: A disease at the crossroads of trade-offs.

Central to evolutionary theory is the idea that living organisms face phenotypic and/or genetic trade-offs when allocating resources to competing life-history demands, such as growth, survival, and reproduction. These trade-offs are increasingly considered to be crucial to further our understanding of cancer. First, evidences suggest that neoplastic cells, as any living entities subject to natural selection, are governed by trade-offs such as between survival and proliferation. Second, selection might also have shaped trade-offs at the organismal level, especially regarding protective mechanisms against cancer. Cancer can also emerge as a consequence of additional trade-offs in organisms (e.g., eco-immunological trade-offs). Here, we review the wide range of trade-offs that occur at different scales and their relevance for understanding cancer dynamics. We also discuss how acknowledging these phenomena, in light of human evolutionary history, may suggest new guidelines for preventive and therapeutic strategies.

Towards powerful experimental and statistical approaches to study intraindividual variability in labile traits.

There is a long-standing interest in behavioural ecology, exploring the causes and correlates of consistent individual differences in mean behavioural traits ('personality') and the response to the environment ('plasticity'). Recently, it has been observed that individuals also consistently differ in their residual intraindividual variability (rIIV). This variation will probably have broad biological and methodological implications to the study of trait variation in labile traits, such as behaviour and physiology, though we currently need studies to quantify variation in rIIV, using more standardized and powerful methodology. Focusing on activity rates in guppies (Poecilia reticulata), we provide a model example, from sampling design to data analysis, in how to quantify rIIV in labile traits. Building on the doubly hierarchical generalized linear model recently used to quantify individual differences in rIIV, we extend the model to evaluate the covariance between individual mean values and their rIIV. After accounting for time-related change in behaviour, our guppies substantially differed in rIIV, and it was the active individuals that tended to be more consistent (lower rIIV). We provide annotated data analysis code to implement these complex models, and discuss how to further generalize the model to evaluate covariances with other aspects of phenotypic variation.

Individual boldness traits influenced by temperature in male Siamese fighting fish.

Temperature has profound effects on physiology of ectothermic animals. However, the effects on temperature variation on behavioral traits are poorly studied in contrast to physiological endpoints. This may be important as even small differences in temperatures have large effects on physiological rates including overall metabolism, and behavior is known to be linked to metabolism at least in part. The primary aim of this study was to determine the effects of ambient temperature on boldness responses of a species of fish commonly used in behavioral experiments, the Siamese fighting fish (Betta splendens). At 26°C, subjects were first examined for baseline behaviors over three days, using three different (but complementary) 'open field' type assays tested in a fixed order. Those same fish were next exposed to either the same temperature (26°C) or a higher temperature (30°C) for 10days, and then the same behavioral assays were repeated. Those individuals exposed to increased temperatures reduced their latency to leave the release area (area I), spent more time in area III (farthest from release area), and were more active overall; together we infer these behaviors to reflect an increase in general 'boldness' with increased temperature. Our results add to a limited number of studies of temperature effects on behavioral tendencies in ectotherms that are evident even after some considerable acclimation. From a methodological perspective, our results indicate careful temperature control is needed when studying behavior in this and other species of fish.

High atmospheric temperatures and 'ambient incubation' drive embryonic development and lead to earlier hatching in a passerine bird.

Tropical and subtropical species typically experience relatively high atmospheric temperatures during reproduction, and are subject to climate-related challenges that are largely unexplored, relative to more extensive work conducted in temperate regions. We studied the effects of high atmospheric and nest temperatures during reproduction in the zebra finch. We characterized the temperature within nests in a subtropical population of this species in relation to atmospheric temperature. Temperatures within nests frequently exceeded the level at which embryo's develop optimally, even in the absence of parental incubation. We experimentally manipulated internal nest temperature to demonstrate that an average difference of 6°C in the nest temperature during the laying period reduced hatching time by an average of 3% of the total incubation time, owing to 'ambient incubation'. Given the avian constraint of laying a single egg per day, the first eggs of a clutch are subject to prolonged effects of nest temperature relative to later laid eggs, potentially increasing hatching asynchrony. While birds may ameliorate the negative effects of ambient incubation on embryonic development by varying the location and design of their nests, high atmospheric temperatures are likely to constitute an important selective force on avian reproductive behaviour and physiology in subtropical and tropical regions, particularly in the light of predicted climate change that in many areas is leading to a higher frequency of hot days during the periods when birds breed.

Avian influenza infection dynamics under variable climatic conditions, viral prevalence is rainfall driven in waterfowl from temperate, south-east Australia.

Understanding Avian Influenza Virus (AIV) infection dynamics in wildlife is crucial because of possible virus spill over to livestock and humans. Studies from the northern hemisphere have suggested several ecological and environmental drivers of AIV prevalence in wild birds. To determine if the same drivers apply in the southern hemisphere, where more irregular environmental conditions prevail, we investigated AIV prevalence in ducks in relation to biotic and abiotic factors in south-eastern Australia. We sampled duck faeces for AIV and tested for an effect of bird numbers, rainfall anomaly, temperature anomaly and long-term ENSO (El-Niño Southern Oscillation) patterns on AIV prevalence. We demonstrate a positive long term effect of ENSO-related rainfall on AIV prevalence. We also found a more immediate response to rainfall where AIV prevalence was positively related to rainfall in the preceding 3-7 months. Additionally, for one duck species we found a positive relationship between their numbers and AIV prevalence, while prevalence was negatively or not affected by duck numbers in the remaining four species studied. In Australia largely non-seasonal rainfall patterns determine breeding opportunities and thereby influence bird numbers. Based on our findings we suggest that rainfall influences age structures within populations, producing an influx of immunologically naïve juveniles within the population, which may subsequently affect AIV infection dynamics. Our study suggests that drivers of AIV dynamics in the northern hemisphere do not have the same influence at our south-east Australian field site in the southern hemisphere due to more erratic climatological conditions.

Cancer and life-history traits: lessons from host-parasite interactions.

Despite important differences between infectious diseases and cancers, tumour development (neoplasia) can nonetheless be closely compared to infectious disease because of the similarity of their effects on the body. On this basis, we predict that many of the life-history (LH) responses observed in the context of host-parasite interactions should also be relevant in the context of cancer. Parasites are thought to affect LH traits of their hosts because of strong selective pressures like direct and indirect mortality effects favouring, for example, early maturation and reproduction. Cancer can similarly also affect LH traits by imposing direct costs and/or indirectly by triggering plastic adjustments and evolutionary responses. Here, we discuss how and why a LH focus is a potentially productive but under-exploited research direction for cancer research, by focusing our attention on similarities between infectious disease and cancer with respect to their effects on LH traits and their evolution. We raise the possibility that LH adjustments can occur in response to cancer via maternal/paternal effects and that these changes can be heritable to (adaptively) modify the LH traits of their offspring. We conclude that LH adjustments can potentially influence the transgenerational persistence of inherited oncogenic mutations in populations.