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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.

INTRODUCTION: Adult sea lamprey (Petromyzon marinus) cease feeding and migrate to spawning streams where males build nests, undergo final sexual maturation, and subsequently produce and release large quantities of bile acid pheromones that attract mature females. These animals are predicted to rearrange their metabolic pathways drastically to support their reproductive strategies, presenting advantageous opportunities to examine how sex and the maturation processes affect metabolism. OBJECTIVES: The objective is to investigate the metabolic differences between sexes and maturation states in sea lamprey that support changes in physiological functions. METHODS: We compared plasma metabolomes of spawning and prespawning sea lamprey in both sexes using both non-targeted and targeted metabolomics approaches using UPLC/MS-MS with electrospray ionization in both positive and negative modes. The data were processed using Progenesis QI, Compound Discoverer and XCMS softwares for alignment, peak picking, and deconvolution of the peaks. Principle component analyses (PCA) and partial least squares discriminant analyses (PLS-DA) were performed using SIMCA and Metaboanalyst softwares to identify discriminating features, followed by fragmentation matching with extensive database search and pathway mapping. RESULTS: The pheromonal bile acid biosynthesis was upregulated significantly in males compared to females. Spermiating males further upregulated bile acid biosynthesis by altering amino acid metabolisms, upregulating cofactors and nucleotide metabolisms, but downregulating carbohydrate and energy metabolisms. CONCLUSION: Plasma metabolomes are sex- and maturation-dependent and reflect the special metabolic demands at each life stage and reproductive strategy.

Sea lamprey (Petromyzon marinus) is a unique vertebrate model to examine how liver metabolomes support different reproductive functions. Juvenile sea lamprey prey on other fish species by attaching to their body and feeding on their blood and body fluids. Once reaching adulthood, they cease feeding, migrate to spawning streams and begin their final sexual maturation. During these processes, the male livers produce large quantities of bile acid pheromone precursors to be modified and released via gills, whereas the female livers synthesize vast amounts of vitellogenin (yolk lipophosphoprotein) to be transported to the ovary.

Reintroduction programs are important tools for wildlife conservation. However, captive rearing environments may lead to maladaptive behavior and physiological alterations that reduce survival probability after release. For captive rearing programs that raise individuals captured from the wild during early ontogeny for later release, there is a lack of information about when during ontogeny the detrimental effects of captive rearing may become evident. In this study we compared cortisol levels, predation rates and swimming behavior between hatchery-produced and wild-caught larval lake sturgeon (Acipenser fulvescens), a threatened fish species, at three times over 9 days. Cortisol levels did not indicate that hatchery-produced individuals were more stressed, but cortisol reactivity to an acute stressor disappeared for both hatchery-produced and wild-caught larvae after 9 days in the hatchery. Swimming activity levels decreased over time for hatchery-produced larvae but increased over time for wild-caught larvae, suggesting that behavioral trajectories may be programmed prior to the larval stage. Neither increasing nor decreasing activity levels was advantageous for survival, as predation rates increased over time in captivity for larvae from both treatments. Results suggest that physiological and behavioral phenotypes may not accurately predict survival for individuals released from reintroduction programs and that the captive environment may inhibit transition to the wild even if cortisol levels do not indicate high stress. Findings emphasize that even a short amount of time in captivity during early ontogeny can affect phenotypes of individuals captured from wild populations, which may impact the success of reintroduction programs.

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.

Costs to producing sexual signals can create selective pressures on males to invest signaling effort in particular contexts. When the benefits of signaling vary consistently across time, males can optimize signal investment to specific temporal contexts using biological rhythms. Sea lamprey, Petromyzon marinus, have a semelparous life history, are primarily nocturnal, and rely on pheromone communication for reproduction; however, whether male investment in pheromone transport and release matches increases in spawning activity remains unknown. By measuring (1) 3keto-petromyzonol sulfate (3kPZS, a main pheromone component) and its biosynthetic precursor PZS in holding water and tissue samples at six points over the course of 24 hours and (2) 3kPZS release over the course of several days, we demonstrate that 3kPZS release exhibits a consistent diel pattern across several days with elevated pheromone release just prior to sunset and at night. Trends in hepatic concentrations and circulatory transport of PZS and 3kPZS were relatively consistent with patterns of 3kPZS release and suggest the possibility of direct upregulation in pheromone transport and release rather than observed release patterns being solely a byproduct of increased behavioral activity. Our results suggest males evolved a signaling strategy that synchronizes elevated pheromone release with nocturnal increases in sea lamprey behavior. This may be imperative to ensure that male signaling effort is not wasted in a species having a single, reproductive event.

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.

The lampricides 3-trifluoromethyl-4-nitrophemol (TFM) and niclosamide have been used for over 60 years to control the invasive sea lamprey (Petromyzon marinus) population in the Laurentian Great Lakes. In this review, we summarize these findings in the context of the mode of action of both lampricides, with a focus on: (1) the physiology of uptake, bodily distribution and mode of action, detoxification, and excretion of lampricides in lamprey and non-target fishes, (2) the development of an Adverse Outcome Pathway for TFM and niclosamide, and (3) the identification of novel avenues for future research that can be further explored to ensure continuous suppression of the sea lamprey population in the Great Lakes. We explored how research on the mode of action of lampricides has provided novel insights into the gill microenvironment and how this impacts lampricide toxicity; described new information on mitochondria and tissue physiology; and discussed how the activity of enzymes that are involved in detoxification pathways impacts the response of fishes to xenobiotics. Considering the information that has been generated over the years on sea lamprey and bony fish physiology from studying the mode of action of lampricides, here we propose an Adverse Outcome Pathway for TFM and niclosamide and identify novel avenues for research on the short and long-term effects of lampricide applications, either alone or in combination. Lastly, we discuss how the differences in physiology between sea lampreys and non-target fishes can be further exploited to ensure continuous suppression of the sea lamprey population in the Great Lakes.

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.

Predator encounters during early life can elicit behavioral and physiological responses that have fitness consequences during subsequent prey life stages. In threatened lake sturgeon (Acipenser fulvescens) and other lithophilic-spawning fishes, newly hatched larvae (free embryos) are exposed to abundant predators including aquatic insect larvae that co-occupy stream substrates. We investigated stress effects on lake sturgeon larvae after encounters with common aquatic insect predators by quantifying mortality, body size, cortisol levels, and swimming behavior. Free embryos were exposed to either Perlidae (stonefly obligate predators) or Isonychiidae (mayfly filterers and facultative predators) or to no predators (controls). Free embryos that encountered perlids experienced high mortality, elevated cortisol levels, and exhibited cortisol reactivity when subsequently exposed to an acute stressor. Free embryos that encountered isonychiids exhibited elevated mortality, and elevated cortisol and cortisol reactivity relative to controls. Findings indicate that lake sturgeon free embryos are stressed by exposure to members of benthic stream communities during early life stages (predation of nearby conspecifics), and that metrics of stress exhibited threat sensitivity. Data are consistent with predictions that individuals modulate antipredator behavior in response to the intensity of perceived predation threat in the environment. We determined that behavioral outcomes associated with encounters with aquatic insects altered future behavioral trajectories, potentially as an adaptive response that can affect predation rates in subsequent life stages. Results contribute to a broader understanding of how interspecies interactions among co-occurring predator and prey communities may impact individual fitness and fish population recruitment.

Migratory fishes are renowned for their ability to home to natal streams for spawning. Learned olfactory cues play a critical role in natal homing of Pacific salmon and other fishes, but the underlying chemical signature of streams remains poorly understood after decades of study. The molecules that convey a stream-specific odour must differ among sites but remain constant over time. Among leading odorant candidates are amino acids; however, little research has assessed the spatial and temporal variability of amino acid profiles in streams. We report a comprehensive chemical study of dissolved amino acids as potential olfactory cues for homing by migratory fish. Specifically, we profiled amino acids in water from 23 streams in the upper Laurentian Great Lakes basin over 2 years. We investigated variation in amino acid profiles (1) among regions and rivers within a year, (2) between years and (3) among sites and across the seasons of migration and early life history within a stream. Liquid-chromatography tandem mass spectrometry revealed nanomolar concentrations for most of the 20 L-amino acids measured, above the levels detectable by studied migratory fishes. Moreover, amino acid profiles were temporally stable between 2 years and across an annual season from adult spawning migration through offspring early-life development within a stream. However, spatial differences in amino acid profiles were evident primarily over large geographic distances (among regions) but not among tributaries within regions or among sites within a stream. Collectively, our results indicate dissolved amino acids may be consistent components of rivers' odorant profiles but suggest additional molecules are likely important for natal homing of migratory fishes to specific spawning sites. We suggest that future studies consider the combined importance of amino acids and molecules from other chemical classes. Understanding the chemical basis of olfactory-guided natal homing is especially important as human activities could alter the odorant profiles of streams and thereby disrupt fish migrations and negatively impact population recruitment.

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.