Impacts of Exposure to Ultraviolet Radiation and an Agricultural Pollutant on Morphology and Behavior of Tadpoles (Limnodynastes tasmaniensis).

Amphibians are the most threatened vertebrate class globally. Multiple factors have been implicated in their global decline, and it has been hypothesized that interactions between stressors may be a major cause. Increased ultraviolet (UV) radiation, as a result of ozone depletion, has been identified as one such stressor. Exposure to UV radiation has been shown to have detrimental effects on amphibians and can exacerbate the effects of other stressors, such as chemical pollutants. Chemical pollution has likewise been recognized as a major factor contributing to amphibian declines, particularly, endocrine-disrupting chemicals. In this regard, 17ß-trenbolone is a potent anabolic steroid used in the agricultural industry to increase muscle mass in cattle and has been repeatedly detected in the environment where amphibians live and breed. At high concentrations, 17ß-trenbolone has been shown to impact amphibian survival and gonadal development. In the present study, we investigated the effects of environmentally realistic UV radiation and 17ß-trenbolone exposure, both in isolation and in combination, on the morphology and behavior of tadpoles (Limnodynastes tasmaniensis). We found that neither stressor in isolation affected tadpoles, nor did we find any interactive effects. The results from our 17ß-trenbolone treatment are consistent with recent research suggesting that, at environmentally realistic concentrations, tadpoles may be less vulnerable to this pollutant compared to other vertebrate classes. The absence of UV radiation-induced effects found in the present study could be due to species-specific variation in susceptibility, as well as the dosage utilized. We suggest that future research should incorporate long-term studies with multiple stressors to accurately identify the threats to, and subsequent consequences for, amphibians under natural conditions. Environ Toxicol Chem 2024;43:1615-1626. © 2024 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Impacts of caffeine on fathead minnow behaviour and physiology.

Pollution from regularly used substances such as pharmaceuticals, cleaning agents, and even food and beverages is an increasing problem in the environment. Caffeine, a commonly ingested stimulant, is one such contaminant that has been detected in aquatic environments worldwide. Yet, little is known about how ecologically relevant concentrations of caffeine influence the morphology, behaviour, and physiology of exposed organisms. To address this knowledge gap, we exposed fathead minnow (Pimephales promelas) to three caffeine treatments: a freshwater control (nominal: 0 ng/L), a low (nominal: 1,000 ng/L) and high environmentally relevant dose (nominal: 10,000 ng/L), for 35 days. We tested the learning abilities, anxiety, metabolic rates, and morphological features of exposed vs. control fish. Caffeine exposure did not affect the ability of fish to learn but did influence anxiety levels. Over the course of repeated anxiety testing, unexposed control fish visited a black square more often while fish exposed to low levels of caffeine did not, potentially indicating that these fish remained in a more anxious state. While caffeine did not impact metabolism, fish growth, or body size, it was associated with lower liver investment-although this response was only observed in our low caffeine treatment. Overall, our results suggest that even relatively low concentrations of caffeine may impact the liver size and anxiety of exposed fish, but further research is needed to assess how extended exposure to caffeine impacts fitness. Given the increase in anthropogenic contaminants in aquatic environments, it is important that we continue to investigate their effects on the organisms exposed to them.

Sexual Selection Increases Male Behavioral Consistency in Drosophila melanogaster.

AbstractSexual selection has been suggested to influence the expression of male behavioral consistency. However, despite predictions, direct experimental support for this hypothesis has been lacking. Here, we investigated whether sexual selection altered male behavioral consistency in Drosophila melanogaster-a species with both pre- and postcopulatory sexual selection. We took 1,144 measures of locomotor activity (a fitness-related trait in D. melanogaster) from 286 flies derived from replicated populations that have experimentally evolved under either high or low levels of sexual selection for >320 generations. We found that high sexual selection males were more consistent (decreased within-individual variance) in their locomotor activity than male conspecifics from low sexual selection populations. There were no differences in behavioral consistency between females from the high and low sexual selection populations. Furthermore, while females were more behaviorally consistent than males in the low sexual selection populations, there were no sex differences in behavioral consistency in high sexual selection populations. Our results demonstrate that behavioral plasticity is reduced in males from populations exposed to high levels of sexual selection. Disentangling whether these effects represent an evolved response to changes in the intensity of selection or are manifested through nongenetic parental effects represents a challenge for future research.

Leveraging AI to improve evidence synthesis in conservation.

Systematic evidence syntheses (systematic reviews and maps) summarize knowledge and are used to support decisions and policies in a variety of applied fields, from medicine and public health to biodiversity conservation. However, conducting these exercises in conservation is often expensive and slow, which can impede their use and hamper progress in addressing the current biodiversity crisis. With the explosive growth of large language models (LLMs) and other forms of artificial intelligence (AI), we discuss here the promise and perils associated with their use. We conclude that, when judiciously used, AI has the potential to speed up and hopefully improve the process of evidence synthesis, which can be particularly useful for underfunded applied fields, such as conservation science.

Sexual selection and speciation in the Anthropocene.

Anthropogenic change threatens global biodiversity by causing severe ecological disturbance and extinction. Here, we consider the effects of anthropogenic change on one process that generates biodiversity. Sexual selection (a potent evolutionary force and driver of speciation) is highly sensitive to the environment and, thus, vulnerable to anthropogenic ecological change. Anthropogenic alterations to sexual display and mate preference can make it harder to distinguish between conspecific and heterospecific mates or can weaken divergence via sexual selection, leading to higher rates of hybridization and biodiversity loss. Occasionally, anthropogenically altered sexual selection can abet diversification, but this appears less likely than biodiversity loss. In our rapidly changing world, a full understanding of sexual selection and speciation requires a global change perspective.

Size dependent antipredator responses in a fish-shrimp mutualism.

For prey, taking refuge from predators has obvious fitness benefits but may also be costly by impinging on time and effort available for feeding or attracting mates. The antipredator responses of refuge-seeking animals are therefore predicted to vary strategically depending on how threatening they perceive the risk. To test this, we studied the impacts of a simulated predatory threat on the antipredator responses of wild sandy prawn-gobies (Ctenogobiops feroculus) that co-inhabit burrows with Alpheus shrimp (family Alpheidae) in a mutualistic relationship. We exposed goby-shrimp pairs, repeatedly on three separate occasions, to an approaching threat and measured the antipredator behaviours of both partners. We found that re-emerging from the burrow took longer in large compared to small fish. Moreover, quicker re-emergence by small-but not medium or large-sized gobies-was associated with an earlier flight from the approaching threat (i.e. when the threat was still further away). Finally, the goby and shrimp sharing a burrow were matched in body size and their risk-taking behaviour was highly dependent on one another. The findings contribute to our understanding of how an individual's phenotype and perception of danger relates to its risk-taking strategy, and how mutualistic partners can have similar risk sensitivities.

No effect of testosterone or sexual ornamentation on telomere dynamics: A case study and meta-analyses.

Life-history theory predicts that reproductive investments are traded-off against self-maintenance. Telomeres, the protective caps on the ends of chromosomes, offer a promising avenue for assessing life-history trade-offs, as they shorten in response to stressors and are predictive of the remaining lifespan. In males, testosterone frequently mediates life-history trade-offs, in part, through its effects on sexual ornamentation, which is an important aspect of reproductive investment. However, studies of within-individual associations between telomere dynamics and sexual ornamentation are limited in number and have produced mixed results. Furthermore, most such studies have been observational, making it difficult to discern the nature of any causal relationship. To address this, we used short-acting testosterone implants in free-living male superb fairy-wrens (Malurus cyaneus) to stimulate the production of a sexual ornament: early moult into a costly blue breeding plumage. We found no evidence that elevated testosterone, and the consequent earlier moult into breeding plumage, accelerated telomere shortening. We therefore followed up with a systematic review and two meta-analyses (28 studies, 54 effect sizes) exploring the associations between telomeres and (1) testosterone and (2) sexual ornamentation. In line with our experimental findings, neither meta-analysis showed an overall correlation of testosterone or sexual ornamentation with telomere length or telomere dynamics. However, meta-regression showed that experimental, compared to observational, studies reported greater evidence of trade-offs. Our meta-analyses highlight the need for further experimental studies to better understand potential responses of telomere length or telomere dynamics to testosterone or sexual ornamentation.

Convergent genomic signatures associated with vertebrate viviparity.

BACKGROUND: Viviparity-live birth-is a complex and innovative mode of reproduction that has evolved repeatedly across the vertebrate Tree of Life. Viviparous species exhibit remarkable levels of reproductive diversity, both in the amount of care provided by the parent during gestation, and the ways in which that care is delivered. The genetic basis of viviparity has garnered increasing interest over recent years; however, such studies are often undertaken on small evolutionary timelines, and thus are not able to address changes occurring on a broader scale. Using whole genome data, we investigated the molecular basis of this innovation across the diversity of vertebrates to answer a long held question in evolutionary biology: is the evolution of convergent traits driven by convergent genomic changes? RESULTS: We reveal convergent changes in protein family sizes, protein-coding regions, introns, and untranslated regions (UTRs) in a number of distantly related viviparous lineages. Specifically, we identify 15 protein families showing evidence of contraction or expansion associated with viviparity. We additionally identify elevated substitution rates in both coding and noncoding sequences in several viviparous lineages. However, we did not find any convergent changes-be it at the nucleotide or protein level-common to all viviparous lineages. CONCLUSIONS: Our results highlight the value of macroevolutionary comparative genomics in determining the genomic basis of complex evolutionary transitions. While we identify a number of convergent genomic changes that may be associated with the evolution of viviparity in vertebrates, there does not appear to be a convergent molecular signature shared by all viviparous vertebrates. Ultimately, our findings indicate that a complex trait such as viviparity likely evolves with changes occurring in multiple different pathways.

Pharmaceutical pollution alters the cost of bacterial infection and its relationship to pathogen load.

The relationship between pathogen proliferation and the cost of infection experienced by a host drives the ecology and evolution of host-pathogen dynamics. While environmental factors can shape this relationship, there is currently limited knowledge on the consequences of emerging contaminants, such as pharmaceutical pollutants, on the relationship between a pathogen's growth within the host and the damage it causes, termed its virulence. Here, we investigated how exposure to fluoxetine (Prozac), a commonly detected psychoactive pollutant, could alter this key relationship using the water flea Daphnia magna and its bacterial pathogen Pasteuria ramosa as a model system. Across a variety of fluoxetine concentrations, we found that fluoxetine shaped the damage a pathogen caused, such as the reduction in fecundity or intrinsic growth experienced by infected individuals, but with minimal change in average pathogen spore loads. Instead, fluoxetine modified the relationship between the degree of pathogen proliferation and its virulence, with both the strength of this trade-off and the component of host fitness most affected varying by fluoxetine concentration and host genotype. Our study underscores the potential for pharmaceutical pollution to modify the virulence of an invading pathogen, as well as the fundamental trade-off between host and pathogen fitness, even at the trace amounts increasingly found in natural waterways.

Mitochondrial genetic variation as a potential mediator of intraspecific behavioural diversity.

Mitochondrial genes play an essential role in energy metabolism. Variation in the mitochondrial DNA (mtDNA) sequence often exists within species, and this variation can have consequences for energy production and organismal life history. Yet, despite potential links between energy metabolism and the expression of animal behaviour, mtDNA variation has been largely neglected to date in studies investigating intraspecific behavioural diversity. We outline how mtDNA variation and interactions between mitochondrial and nuclear genotypes may contribute to the expression of individual-to-individual behavioural differences within populations, and why such effects may lead to sex differences in behaviour. We contend that integration of the mitochondrial genome into behavioural ecology research may be key to fully understanding the evolutionary genetics of animal behaviour.

Sex-specific effects of psychoactive pollution on behavioral individuality and plasticity in fish.

The global rise of pharmaceutical contaminants in the aquatic environment poses a serious threat to ecological and evolutionary processes. Studies have traditionally focused on the collateral (average) effects of psychoactive pollutants on ecologically relevant behaviors of wildlife, often neglecting effects among and within individuals, and whether they differ between males and females. We tested whether psychoactive pollutants have sex-specific effects on behavioral individuality and plasticity in guppies (Poecilia reticulata), a freshwater species that inhabits contaminated waterways in the wild. Fish were exposed to fluoxetine (Prozac) for 2 years across multiple generations before their activity and stress-related behavior were repeatedly assayed. Using a Bayesian statistical approach that partitions the effects among and within individuals, we found that males-but not females-in fluoxetine-exposed populations differed less from each other in their behavior (lower behavioral individuality) than unexposed males. In sharp contrast, effects on behavioral plasticity were observed in females-but not in males-whereby exposure to even low levels of fluoxetine resulted in a substantial decrease (activity) and increase (freezing behavior) in the behavioral plasticity of females. Our evidence reveals that psychoactive pollution has sex-specific effects on the individual behavior of fish, suggesting that males and females might not be equally vulnerable to global pollutants.

Toward Real-Time Animal Tracking with Integrated Stimulus Control for Automated Conditioning in Aquatic Eco-Neurotoxicology.

Aquatic eco-neurotoxicology is an emerging field that requires new analytical systems to study the effects of pollutants on animal behaviors. This is especially true if we are to gain insights into one of the least studied aspects: the potential perturbations that neurotoxicants can have on cognitive behaviors. The paucity of experimental data is partly caused by a lack of low-cost technologies for the analysis of higher-level neurological functions (e.g., associative learning) in small aquatic organisms. Here, we present a proof-of-concept prototype that utilizes a new real-time animal tracking software for on-the-fly video analysis and closed-loop, external hardware communications to deliver stimuli based on specific behaviors in aquatic organisms, spanning three animal phyla: chordates (fish, frog), platyhelminthes (flatworm), and arthropods (crustacean). The system's open-source software features an intuitive graphical user interface and advanced adaptive threshold-based image segmentation for precise animal detection. We demonstrate the precision of animal tracking across multiple aquatic species with varying modes of locomotion. The presented technology interfaces easily with low-cost and open-source hardware such as the Arduino microcontroller family for closed-loop stimuli control. The new system has potential future applications in eco-neurotoxicology, where it could enable new opportunities for cognitive research in diverse small aquatic model organisms.

Invasive species behaviour in a toxic world.

Invasive species and chemical pollution both threaten biodiversity. Here, we discuss how pollution, through its impacts on wildlife behaviour, shapes invasion dynamics by altering species interactions. Addressing knowledge gaps will have implications for the management of invasive species and conservation of native ecosystems in an increasingly toxic world.

The role of cognition in nesting.

For many animals, nests are essential for reproductive success. Nesting individuals need to carry out a range of potentially challenging tasks, from selecting an appropriate site and choosing suitable materials to constructing the nest and defending it against competitors, parasites and predators. Given the high fitness stakes involved, and the diverse impacts both the abiotic and social environment can have on nesting success, we might expect cognition to facilitate nesting efforts. This should be especially true under variable environmental conditions, including those changing due to anthropogenic impacts. Here, we review, across a wide range of taxa, evidence linking cognition to nesting behaviours, including selection of nesting sites and materials, nest construction, and nest defence. We also discuss how different cognitive abilities may increase an individual's nesting success. Finally, we highlight how combining experimental and comparative research can uncover the links between cognitive abilities, nesting behaviours and the evolutionary pathways that may have led to the associations between them. In so doing, the review highlights current knowledge gaps and provides suggestions for future research. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Long-term effects of incubation temperature on growth and thermal physiology in a small ectotherm.

Thermal conditions in the developmental environment can substantially affect an individual's phenotype, particularly in egg-laying ectotherms. However, whether these effects persist into adulthood is rarely examined. To investigate this, we incubated delicate skink, Lampropholis delicata, eggs at either cool (22°C), mild (26°C) or hot (30°C) temperatures. After hatching, we measured growth, thermal performance curves of locomotor activity, and thermal sensitivity of resting metabolic rate of offspring as juveniles (4-6 weeks of age), sub-adults (approx. 200 days of age), and adults (approx. 2 years of age), and then measured developmental temperature impacts on male fertility. Incubation temperature had a lasting effect on growth and locomotor performance, with cool and hot incubation temperatures resulting in faster growth and larger maximum size, and hot incubation temperatures reducing locomotor performance at all timepoints. Effects on resting metabolic rate were only present in sub-adults, with a higher metabolic rate at high and average body mass and negative metabolic scaling exponent in cool-incubated lizards. Additionally, cool and hot incubation treatments resulted in shorter sperm midpieces and heads. Incubation temperature did not affect testis mass or sperm count. Overall, our results demonstrate that incubation temperature can have lasting effects on later life stages, highlighting the importance of maternal nest-site selection, but that some effects are age dependent. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Temperature change exerts sex-specific effects on behavioural variation.

Temperature is a key factor mediating organismal fitness and has important consequences for species' ecology. While the mean effects of temperature on behaviour have been well-documented in ectotherms, how temperature alters behavioural variation among and within individuals, and whether this differs between the sexes, remains unclear. Such effects likely have ecological and evolutionary consequences, given that selection acts at the individual level. We investigated the effect of temperature on individual-level behavioural variation and metabolism in adult male and female Drosophila melanogaster (n = 129), by taking repeated measures of locomotor activity and metabolic rate at both a standard temperature (25°C) and a high temperature (28°C). Males were moderately more responsive in their mean activity levels to temperature change when compared to females. However, this was not true for either standard or active metabolic rate, where no sex differences in thermal metabolic plasticity were found. Furthermore, higher temperatures increased both among- and within-individual variation in male, but not female, locomotor activity. Given that behavioural variation can be critical to population persistence, we suggest that future studies test whether sex differences in the amount of behavioural variation expressed in response to temperature change may result in sex-specific vulnerabilities to a warming climate.

The ethics of intervening in animal behaviour for conservation.

Conservation behaviour is a growing field that applies insights from the study of animal behaviour to address challenges in wildlife conservation and management. Conservation behaviour interventions often aim to manage specific behaviours of a species to solve conservation challenges. The field is often viewed as offering approaches that are less intrusive or harmful to animals than, for example, managing the impact of a problematic species by reducing its population size (frequently through lethal control). However, intervening in animal behaviour, even for conservation purposes, may still raise important ethical considerations. We discuss these issues and develop a framework and a decision support tool, to aid managers and researchers in evaluating the ethical considerations of conservation behaviour interventions against other options.

Bigger and bolder: Widespread agricultural pollutant 17ß-trenbolone increases growth and alters behaviour in tadpoles (Litoria ewingii).

Endocrine-disrupting chemicals-compounds that directly interfere with the endocrine system of exposed animals-are insidious environmental pollutants that can disrupt hormone function, even at very low concentrations. The dramatic impacts that some endocrine-disrupting chemicals can have on the reproductive development of wildlife are well documented. However, the potential of endocrine-disrupting chemicals to disrupt animal behaviour has received far less attention, despite the important links between behavioural processes and population-level fitness. Accordingly, we investigated the impacts of 14 and 21-day exposure to two environmentally realistic levels of 17ß-trenbolone (4.6 and 11.2 ng/L), a potent endocrine-disrupting steroid and agricultural pollutant, on growth and behaviour in tadpoles of an anuran amphibian, the southern brown tree frog (Litoria ewingii). We found that 17ß-trenbolone altered morphology, baseline activity and responses to a predatory threat, but did not affect anxiety-like behaviours in a scototaxis assay. Specifically, we found that tadpoles exposed to our high-17ß-trenbolone treatment were significantly longer and heavier at 14 and 21 days. We also found that tadpoles exposed to 17ß-trenbolone showed higher levels of baseline activity, and significantly reduced their activity following a simulated predator strike. These results provide insights into the wider repercussions of agricultural pollutants on key developmental and behavioural traits in aquatic species, and demonstrate the importance of behavioural studies in the ecotoxicological field.

Widespread psychoactive pollutant augments daytime restfulness and disrupts diurnal activity rhythms in fish.

Pharmaceutical pollution is a major driver of global change, with the capacity to alter key behavioural and physiological traits in exposed animals. Antidepressants are among the most commonly detected pharmaceuticals in the environment. Despite well-documented pharmacological effects of antidepressants on sleep in humans and other vertebrates, very little is known about their ecologically relevant impacts as pollutants on non-target wildlife. Accordingly, we investigated the effects of acute 3-day exposure of eastern mosquitofish (Gambusia holbrooki) to field-realistic levels (nominal concentrations: 30 and 300 ng/L) of the widespread psychoactive pollutant, fluoxetine, on diurnal activity patterns and restfulness, as indicators of disruptions to sleep. We show that exposure to fluoxetine disrupted diel activity patterns, which was driven by augmentation of daytime inactivity. Specifically, unexposed control fish were markedly diurnal, swimming farther during the day and exhibiting longer periods and more bouts of inactivity at night. However, in fluoxetine-exposed fish, this natural diel rhythm was eroded, with no differences in activity or restfulness observed between the day and night. As a misalignment in the circadian rhythm has been shown to adversely affect fecundity and lifespan in animals, our findings reveal a potentially serious threat to the survival and reproductive success of pollutant-exposed wildlife.

The roles of sexual selection and sexual conflict in shaping patterns of genome and transcriptome variation.

Sexual dimorphism is one of the most prevalent, and often the most extreme, examples of phenotypic variation within species, and arises primarily from genomic variation that is shared between females and males. Many sexual dimorphisms arise through sex differences in gene expression, and sex-biased expression is one way that a single, shared genome can generate multiple, distinct phenotypes. Although many sexual dimorphisms are expected to result from sexual selection, and many studies have invoked the possible role of sexual selection to explain sex-specific traits, the role of sexual selection in the evolution of sexually dimorphic gene expression remains difficult to differentiate from other forms of sex-specific selection. In this Review, we propose a holistic framework for the study of sex-specific selection and transcriptome evolution. We advocate for a comparative approach, across tissues, developmental stages and species, which incorporates an understanding of the molecular mechanisms, including genomic variation and structure, governing gene expression. Such an approach is expected to yield substantial insights into the evolution of genetic variation and have important applications in a variety of fields, including ecology, evolution and behaviour.