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Quantifying transgenerational effects of stress is important to predict outcomes of anthropogenic disturbances for wildlife species. Maternal stress can programme physiological and behavioural phenotypes in offspring, which may be maladaptive if maternal and offspring environments are mismatched. We investigated effects of a match and mismatch between egg cortisol and offspring stress levels in lake sturgeon, Acipenser fulvescens, using artificially elevated egg cortisol levels (simulating maternal stress) and a chronic unpredictable stress regime for offspring after hatch. Offspring cortisol levels were quantified at baseline and after an acute stressor. Multiple measures of offspring swimming activity were assessed in behaviour trials. Individuals that experienced elevated egg cortisol and high offspring stress exhibited a diminished cortisol response to an acute stressor, but responses varied among offspring from different families. Results suggest that the interaction between maternal and offspring experience may cue an offspring phenotype that is adaptive in high-stress conditions. Principal components analysis characterizing interindividual variation in offspring behavioural variables showed that treatment significantly affected multivariate offspring response along the PC1 axis (associated with inactivity), and both treatment and family significantly affected response along the PC2 axis (associated with shorter distance moved). The largest differences for PC1 occurred between the ‘mismatch’ treatments (high egg cortisol and low offspring stress exhibiting lower activity; low egg cortisol and high offspring stress exhibiting higher activity), indicating that the combination of egg cortisol and offspring stress is more important in determining offspring behaviour than is egg cortisol or offspring stress alone. Findings suggest that family effects, such as genetic components or maternal experience, may mediate how the interaction of maternal and offspring stress influences offspring physiological and behavioural outcomes, and indicate the need for further research into environmental factors experienced by females that influence how offspring respond to egg cortisol and early life stress.

Sexual signals evolve via selective pressures arising from male–male competition and female choice, including those originating from unintended receivers that detect the signal. For example, males can acquire information from other males signaling to females and alter their own signal. Relative to visual and acoustic signals, less is known about how such communication networks influence chemical signaling among animals. In sea lamprey (Petromyzon marinus), the chemical communication system is essential for reproduction, offering a useful system to study a pheromone communication network that includes signalers and both intended and unintended receivers. Male sea lamprey aggregate on spawning grounds, where individuals build nests and signal to females using sex pheromones. We examined how exposure to a major component of the male pheromone, 3keto-petromyzonol sulfate (3kPZS), influenced male pheromone signaling, and whether females had a preference for males that altered their signal. Exposure to 3kPZS, at a concentration of 5×10−10 mol l−1, simulated the presence of other male(s) and led to increased 3kPZS release rates within 10 min, followed by a return to baseline levels within 30 min. Exposure also led to increases in hepatic synthesis and circulatory transport of pheromone components. In behavioral assays, females preferred the odor of males that had been exposed to 3kPZS; therefore, males likely benefit from upregulating 3kPZS release after detecting competition for mates. Here, we define how a specific pheromone component influences chemical signaling during intrasexual competition, and show a rare example of how changes in chemical signaling strategies resulting from male competition may influence mate choice.

The relationships between pheromone stimuli and neuropeptides are not well established in vertebrates due to the limited number of unequivocally identified pheromone molecules. The sea lamprey (Petromyzon marinus) is an advantageous vertebrate model to study the effects of pheromone exposure on neuropeptides since many pheromone molecules and neuropeptides have been identified in this species. Sexually mature male sea lamprey release pheromones 7α, 12α, 24-trihydroxy-5α-cholan-3-one 24-sulfate (3 keto-petromyzonol sulfate, 3kPZS) and 7α, 12α-dihydroxy-5α-cholan-3-one-24-oic acid (3-keto allocholic acid, 3kACA) that differentially regulate gonadotropin-releasing hormone (lGnRH) and steroid levels in sexually immature sea lamprey. However, the effects of these pheromones on gonadotropin-inhibitory hormones (GnIHs), hypothalamic neuropeptides that regulate lGnRH release, are still elusive. In this report, we sought to examine the effects of waterborne pheromones on lamprey GnIH-related neuropeptide levels in sexually immature sea lamprey. Ultra-performance liquid chromatography tandem mass spectrometry (UPLC-MS/MS) analyses revealed sex differences in GnIH-related neuropeptide levels in the brain and plasma of immature sea lamprey. Exposure to 3kPZS and 3kACA exerted differential effects on GnIH-related neuropeptide levels in both sexes, but the effects were more prominent in female brains. We conclude that sea lamprey pheromones regulate GnIH-related neuropeptide levels in a sexually dimorphic manner.

Population control of invasive sea lamprey relies heavily on lampricide treatment of infested streams. The lampricide 3-trifluoromethyl-4-nitrophenol (TFM) is thought to impair mitochondrial ATP production through uncoupling oxidative phosphorylation. However, the effect of TFM on the entire electron transport chain (complexes I to V) in the mitochondria is not clear. In addition, TFM is reduced in phase I metabolism by sea lamprey at higher levels than in other fish species. The effects of these TFM reductive metabolites on mitochondria have not been explored. In this study, we sought to examine the effects of TFM and its reductive metabolite amino-TFM (TFMa) on cardiac mitochondrial oxygen consumption and membrane potential to delineate potential mechanisms for toxicity. To determine if molecules with similar structure also exhibit similar effects on mitochondria, we used 4-nitro-3-methylphenol (NMP) and its reductive metabolites 4-amino-3-methylphenol (NMPa) and 4-nitroso-3-methylphenol (NMPn) for comparisons. We found that mitochondrial bioenergetics was heavily affected with increasing concentrations of TFM, NMP, and NMPa when complexes I and II of the electron transport chain were examined, indicating that the toxic action of these compounds was exerted not only by uncoupling complex V, but also affecting complexes I and II.

Use of the first fish pheromone biopesticide, 3-keto petromyzonol sulfate (3kPZS) in sea lamprey (Petromyzon marinus) control requires an understanding of both how the amount 3kPZS applied to a trap relates to catch, and how that relationship varies among stream types. By conducting 3kPZS dose-response experiments over two years and across six varied trapping contexts, we conclude (1) that 3kPZS application is best standardized by how much is emitted from the trap instead of the fully mixed concentration achieved downstream, and (2) that 3kPZS is more effective in wide streams (>30 m). In wide streams, emission of 3kPZS at 50 mg hr.−1 from the trap increased capture rate by 10–15% as sea lamprey were 25–50% more likely to enter the trap after encounter. However, in narrow streams (< 15 m), 50 mg hr.−1 3kPZS generally reduced probabilities of upstream movement, trap encounter, and entrance. While 3kPZS significantly influenced upstream movement, encounter, and capture probabilities, these behaviors were also highly influenced by water temperature, stream width, sea lamprey length, and sex. This study highlights that a pheromone component in a stream environment does not ubiquitously increase trap catch in all contexts, but that where, how, and when the pheromone is applied has major impacts on whether it benefits or hinders trapping efforts.