A unified evolutionary framework for understanding parasite infection and host migratory behaviour.

Animal migration impacts organismal health and parasite transmission: migrants are simultaneously exposed to parasites and able to reduce infection for both individuals and populations. However, these dynamics are difficult to study; empirical studies reveal disparate results while existing theory makes assumptions that simplify natural complexity. Here, we systematically review empirical studies of migration and infection across taxa, highlighting key gaps in our understanding. Next, we develop a unified evolutionary framework incorporating different selective pressures of parasite-migration interactions while accounting for ecological complexity that goes beyond previous theory. Our framework generates diverse migration-infection patterns paralleling those seen in empirical systems, including partial and differential migration. Finally, we generate predictions about which mechanisms dominate which empirical systems to guide future studies. Our framework provides an overarching understanding of selective pressures shaping migration patterns in the context of animal health and disease, which is critical for predicting how environmental change may threaten migration.

A warmer environment can reduce sociability in an ectotherm.

The costs and benefits of being social vary with environmental conditions, so individuals must weigh the balance between these trade-offs in response to changes in the environment. Temperature is a salient environmental factor that may play a key role in altering the costs and benefits of sociality through its effects on food availability, predator abundance, and other ecological parameters. In ectotherms, changes in temperature also have direct effects on physiological traits linked to social behaviour, such as metabolic rate and locomotor performance. In light of climate change, it is therefore important to understand the potential effects of temperature on sociality. Here, we took the advantage of a 'natural experiment' of threespine sticklebacks from contrasting thermal environments in Iceland: geothermally warmed water bodies (warm habitats) and adjacent ambient-temperature water bodies (cold habitats) that were either linked (sympatric) or physically distinct (allopatric). We first measured the sociability of wild-caught adult fish from warm and cold habitats after acclimation to a low and a high temperature. At both acclimation temperatures, fish from the allopatric warm habitat were less social than those from the allopatric cold habitat, whereas fish from sympatric warm and cold habitats showed no differences in sociability. To determine whether differences in sociability between thermal habitats in the allopatric population were heritable, we used a common garden breeding design where individuals from the warm and the cold habitat were reared at a low or high temperature for two generations. We found that sociability was indeed heritable but also influenced by rearing temperature, suggesting that thermal conditions during early life can play an important role in influencing social behaviour in adulthood. By providing the first evidence for a causal effect of rearing temperature on social behaviour, our study provides novel insights into how a warming world may influence sociality in animal populations.

Few studies of wild animal performance account for parasite infections: A systematic review.

Wild animals have parasites. This inconvenient truth has far-reaching implications for biologists measuring animal performance traits: infection with parasites can alter host behaviour and physiology in profound and sometimes counterintuitive ways. Yet, to what extent do studies on wild animals take individual infection status into account? We performed a systematic review across eight scientific journals primarily publishing studies in animal behaviour and physiology over a 5-year period to assess the proportion of studies which acknowledge, treat or control for parasite infection in their study design and/or analyses. We explored whether parasite inclusion differed between studies that are experimental versus observational, conducted in the field vs the laboratory and measured behavioural vs physiological traits. We also investigated the importance of other factors such as the journal, the trait category (e.g. locomotion, reproduction) measured, the vertebrate taxonomic group investigated and the host climatic zone of origin. Our results show that parasite inclusion was generally lacking across recent studies on wild vertebrates. In over 680 filtered papers, we found that only 21.9% acknowledged the potential effects of infections on animal performance in the text, and only 5.1% of studies treated animals for infection (i.e. parasite control) or considered infection status in the statistical analyses (i.e. parasite analysis). Parasite inclusion, control and analysis were higher in laboratory compared to field studies and higher for physiological studies compared to behavioural studies but did not differ among journals, performance trait categories and taxonomic groups. Among climatic zones, parasite inclusion, control and analysis were higher in tropical, subtropical and temperate zones than in boreal and polar zones. Overall, our literature review suggests that parasites are sorely under-acknowledged by researchers in recent years despite growing evidence that infections can modify animal performance. Given the ubiquity of parasites in the environment, we encourage scientists to consider individual infection status when assessing performance of wild animals. We also suggest ways for researchers to implement such practices in both experimental and observational studies.

Escaping from multiple visual threats: modulation of escape responses in Pacific staghorn sculpin (Leptocottus armatus).

Fish perform rapid escape responses to avoid sudden predatory attacks. During escape responses, fish bend their bodies into a C-shape and quickly turn away from the predator and accelerate. The escape trajectory is determined by the initial turn (stage 1) and a contralateral bend (stage 2). Previous studies have used a single threat or model predator as a stimulus. In nature, however, multiple predators may attack from different directions simultaneously or in close succession. It is unknown whether fish are able to change the course of their escape response when startled by multiple stimuli at various time intervals. Pacific staghorn sculpin (Leptocottus armatus) were startled with a left and right visual stimulus in close succession. By varying the timing of the second stimulus, we were able to determine when and how a second stimulus could affect the escape response direction. Four treatments were used: a single visual stimulus (control); or two stimuli coming from opposite sides separated by a 0 ms (simultaneous treatment), 33 ms or 83 ms time interval. The 33 ms and 83 ms time intervals were chosen to occur either side of a predicted 60 ms visual escape latency (i.e. during stage 1). The 0 ms and 33 ms treatments influenced both the escape trajectory and the stage 1 turning angle, compared with a single stimulation, whereas the 83 ms treatment had no effect on the escape trajectory. We conclude that Pacific staghorn sculpin can modulate their escape trajectory only between stimulation and the onset of the response, but the escape trajectory cannot be modulated after the body motion has started.

Use of a shuttle box model to assess the behavioral and analgesic effects of opioid injections in goldfish (Carassius auratus).

OBJECTIVE: To evaluate if opioid-induced behavioral effects, such as sedation, can be detected using a shuttle box experimental apparatus and whether thermal preference following noxious stimulation using mustard oil is reversed by morphine administration in fish. METHODS: 5 goldfish (Carassius auratus) underwent 2 randomized blinded experimental trials, with a crossover study design. First, opioid effects were tested in a shuttle box without painful stimulus. Fish were injected 5 days apart with butorphanol at 0.4 or 10 mg/kg, morphine at 5 or 10 mg/kg, or saline IM. After 30 minutes, each fish was placed in a shuttle box for 2 hours with a temperature gradient of 26 to 28 °C. Temperature preference, time spent immobile, and swimming velocity were assessed. The second trial consisted of cutaneous noxious stimulation using mustard oil immersion for 5 minutes followed by an assessment of thermal preference for 4 minutes in the shuttle box after either morphine at 10 mg/kg or saline IM injections. Linear mixed models were used to compare treatment groups. RESULTS: Before noxious stimulation, a low dose of morphine caused sedation compared with control group and high-dose morphine and butorphanol treatments. Immersion in mustard oil caused fish to spend more time in the cold area in the control group. Morphine administration reversed this pattern. CONCLUSIONS: The sedative and analgesic effects of opioids were detected through this model. CLINICAL RELEVANCE: The shuttle box model could be used to assess the analgesic effects of other opioids in goldfish while reducing biases associated with the sedative and stimulatory effects of these drugs.

Mitochondrial Enzyme Activities and Body Condition of Naturally Infected Sunfish (Lepomis gibbosus).

AbstractParasites can affect host behavior, cognition, locomotion, body condition, and many other physiological traits. Changes to host aerobic metabolism may be responsible for these parasite-induced performance alterations. Whole-organism metabolic rate is underpinned by cellular energy metabolism driven most prominently by mitochondria. However, few studies have explored how mitochondrial enzymatic activity relates to body condition and parasite infection, despite it being a putative site for metabolic disruptions related to health status. We studied correlations among natural parasite infection, host body condition, and activity of key mitochondrial enzymes in target organs from wild-caught pumpkinseed sunfish (Lepomis gibbosus) to better understand the cellular responses of fish hosts to endoparasite infection. Enzymatic activities in the gills, spleen, and brain of infected fish were not significantly related to parasite infection or host body condition. However, the activity of cytochrome c oxidase, an enzyme involved in oxidative phosphorylation, in fish hearts was higher in individuals with a lower body condition. Activities of citrate synthase, electron transport system (complexes I and III), and carnitine palmitoyltransferase were also significantly different among organ types. These results provide preliminary information regarding the likely mitochondrial pathways affecting host body condition, the maintenance energetic requirements of different organs, and the organs' specific dependency on particular mitochondrial pathways. These results help pave the way for future studies on the effects of parasite infection on mitochondrial metabolism.