Zoological Science

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ORIGINAL ARTICLES
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Comparative Study of Gamma Radiation Tolerance between Desiccation-Sensitive and Desiccation-Tolerant Tardigrades
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Tardigrades are small metazoans renowned for their exceptional tolerance against various harsh environments in a dehydrated state. Some species exhibited an extraordinary tolerance against high-dose irradiation even in a hydrated state. Given that natural sources of high radiation are rare, the selective pressure to obtain such a high radiotolerance during evolution remains elusive. It has been postulated that high radiation tolerances could be derived from adaptation to dehydration, because both dehydration and radiation cause similar damage on biomolecules at least partly, e.g., DNA cleavage and oxidation of various biomolecules, and dehydration is a common environmental stress that terrestrial organisms should adapt to. Although tardigrades are known for high radiotolerance, the radiotolerance records have been reported only for desiccation-tolerant tardigrade species and nothing was known about the radiotolerance in desiccation-sensitive tardigrade species. Hence, the relationship between desiccation-tolerance and radiotolerance remained unexplored. To this end, we examined the radiotolerance of the desiccation-sensitive tardigrade Grevenius myrops (formerly known as Isohypsibius myrops) in comparison to the well-characterized desiccation-tolerant tardigrade, Ramazzottius varieornatus. The median lethal dose (LD50) of G. myrops was approximately 2240 Gy. This was much lower than those reported for desiccation tolerant eutardigrades. The effects of irradiation on the lifespan and the ovipositions were more severe in G. myrops compared to those in R. varieornatus. The present study provides precise records on the radiotolerance of a desiccation-sensitive tardigrade and the current data supported the correlation between desiccation tolerance and radiotolerance at least in eutardigrades.
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Convergent Gene Duplication in Arctic and Antarctic Teleost Fishes
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Teleost fishes have independently colonized polar regions multiple times, facing many physiological and biochemical challenges due to frigid temperatures. Although increased gene copy numbers can contribute to adaptive evolution in extreme environments, it remains unclear which categories of genes exhibit increased copy numbers associated with polar colonization. Using 104 species of ray-finned fishes, we systematically identified genes with a significant correlation between copy number and polar colonization after phylogenetic correction. Several genes encoding extracellular glycoproteins, including zona pellucida (ZP) proteins, which increase their copy number in Antarctic notothenioid fishes, exhibited elevated copy numbers across multiple polar fish lineages. Additionally, some genes reported to be highly expressed under cold stress, such as cold-inducible RNA-binding protein (CIRBP), had significantly increased copy numbers in polar fishes. Further analysis will provide a fundamental basis for understanding the role of gene duplication in polar adaptations.
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REVIEWS
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Nutritional Adaptation and Microbes: Insights From Drosophila
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Life-history traits such as growth, reproduction, and lifespan in animals are shaped by both genetic and environmental factors, with nutrition being one of the most important environmental factors. However, it remains unclear how and to what extent changes in the nutritional environment affect animals and what molecular mechanisms they employ to adapt to these varying conditions. In recent years, the fruit fly Drosophila melanogaster and related species have been developed as model systems for studying the effects of nutrition and microbes on animals at the molecular level. This review summarizes recent findings on nutritional adaptation in Drosophila species, focusing on nutrition-dependent neuronal developmental mechanisms, carbohydrate-responsive systems that generate differences in adaptabilities among species, and animal-associated microbes that support host growth.
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Evolution of Temperature Receptors and Their Roles in Sensory Diversification and Adaptation
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Among various environmental factors, temperature is one of the critical factors for organisms since it can affect most, if not all, biological processes. Therefore, animals precisely sense ambient and body temperatures and physiologically and behaviorally respond to temperature changes. Taking such nature into consideration, alteration of thermal perception should have played a pivotal role in adaptation to diverse thermal niches. Temperature as well as other physical and chemical stimuli are perceived by the primary afferent neurons where transient receptor potential (TRP) channels are expressed, and these channels serve as multimodal receptors in the somatosensory system. To understand the roles of TRP channels in the evolution of sensory perception, comparative analyses have been performed using various animal species, and their functional diversity has been well documented over the past 2 decades. Furthermore, in recent years, species differences in the thermal responses of TRP channels have been found among closely related species inhabiting different thermal niches, which have uncovered the contributions of TRP channels to environmental adaptation in various vertebrate species. The purpose of this review is to summarize the studies that addressed the functional evolution of TRP channels associated with sensory diversification and environmental adaptation.
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Environmentally Dependent Alteration of Reproductive Strategies and Juvenile Hormone Signaling in Daphnia (Crustacea: Cladocera)
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Daphnia switches between asexual and sexual reproductive strategies, depending on environmental conditions. For sexual reproduction, unfavorable environmental signals induce production of males and formation of meiotic eggs. Induction of both these phenotypes is strongly dependent upon the arthropod endocrine factor juvenile hormone (JH). This review presents the current state of research on regulatory mechanisms of reproductive strategy alteration in Daphnia, focusing on studies related to JH signaling conducted during the past several decades. Additionally, it discusses what is needed in future research to fully understand these mechanisms and evolution of complicated life cycle and environmental adaptation systems in Daphnia.
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It Pays to Sit Tight: Stable Night-Time Incubation Increases Hatching Success in Urban and Forest Great Tits, Parus major
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Animals organize their time so that their behaviors do not conflict with each other and align well with environmental conditions. In species with parental care, adults must also accommodate offspring needs into their temporal allocation of resources and activities. Avian parents face harsh constraints on their time budget during incubation, when they must sustain themselves but also transfer heat to eggs. During day-time, their shuttling between incubating and foraging is well studied. At night, birds usually rest on the nest and provide stable incubation. However, the stability of night rest depends on parental physiology and environmental conditions, and its patterns and consequences are poorly understood. We propose that stable parental night rest enhances the chances of embryos to hatch and might shorten incubation time, but that, in an urbanizing world, night rest may be compromised. We recorded nocturnal incubation restlessness, defined as variation in nest temperature, by placing thermal loggers into nest boxes of urban (25 clutches) and forest (70 clutches) great tits, where only females incubate. We found that with increasing nocturnal restlessness, hatching success dropped by ca. 60% per unit of increase in incubation restlessness in both habitats, despite higher hatching success in the forest. One putative driver of unstable incubation was artificial light at night, which for urban nest boxes was associated with increased nocturnal restlessness. Restlessness did not affect time to hatching. We conclude that sitting tight at night provides fitness pay-offs for incubating birds, but is influenced by environmental conditions, including those shaped by human activities.
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ORIGINAL ARTICLES
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Yawning and Its Temperature-Dependent Modulation in Leopard Geckos
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Yawning is a stereotyped behavior widely observed in vertebrates, serving as an adaptation to the environment. Previous research has highlighted the correlations between yawning and physiological arousal or temperature regulation. However, the majority of those studies have primarily focused on endothermic animals. Thus far, the function of yawning in ectothermic animals remains unclear. In this study, we observed the behavior of leopard geckos, Eublepharis macularius, ectothermic reptiles, over a period of 3 days under constant ambient temperatures of 25°C, 30°C, or 35°C. By investigating the relationship between temperature, spontaneous yawning, and activity levels, we found that yawning frequency is affected by ambient temperature, and also observed a significant increase in post-yawning activity particularly under the 30°C and 35°C conditions. Furthermore, a near 24-hour periodicity in yawning was detected under all temperature conditions. These results align with previous studies conducted on endothermic animals, suggesting the conservation of primitive functions of yawning across vertebrate species.
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Physiology of Overwintering in a Microhabitat Fully Exposed to Adverse Weather Conditions: Lime Seed Bugs on Tree Trunks and Branches
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The present study investigates the physiological aspects of overwintering in an exposed microhabitat in the lime seed bug, Oxycarenus lavaterae. We found that the overwintering lime seed bugs do not survive freezing of their body fluids, but instead rely on supercooling (freeze avoidance). The seasonal modulation of the supercooling capacity was very limited, with the midwinter mean supercooling point reaching –15.5°C, but the individual variability was very high (– 6°C to – 22°C). Most of the other physiological parameters of overwintering lime seed bugs (utilization of energy substrates, changes in hydration, and metabolite composition [although metabolite levels were low]) were consistent with the general knowledge gathered for other freeze-avoiding insects. A significant exception was found in the amount of osmotically active water (“freezable” water), which constituted up to 95% of the lime seed bug body water. Such a proportion is unusually high, as it typically ranges from 59% to 86% in other insects and invertebrates. At present, we have no plausible explanation for this anomaly or its possible relationship to the lime seed bug's overwintering microhabitat.
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REVIEWS
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Temperature Acclimation and Cold Tolerance in Caenorhabditis Elegans are Regulated by Multiorgan Coordination
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To ensure survival and reproduction, organisms must continually adapt to environmental fluctuations, such as temperature, humidity, oxygen level, and salinity. Particularly, temperature profoundly influences biochemical reactions crucial for survival. Here, we present the mechanisms employed by the nematode Caenorhabditis elegans to anticipate and respond to cold temperatures. Our findings reveal that temperature is detected by specific neurons linked to various physiological processes in the gut, spermatheca, and muscles. Notably, the gut, a primary fat storage organ in C. elegans, regulates fat mobilization and accumulation in a temperature-dependent manner, thereby contributing to temperature adaptation. Furthermore, normal spermatogenetic mechanisms influence cold tolerance by modulating the responsiveness of thermosensory neurons to temperature changes. Considering our results together with recent reports, we suggest that a polyU-specific endoribonuclease expressed in muscle cells plays a role in cold tolerance through a non-cell-autonomous mechanism, possibly involving transportation intertissues. Thus, understanding cold tolerance and temperature acclimation in C. elegans can provide valuable insights on systemic physiological regulation in response to temperature fluctuations. Moreover, they could help elucidate the actions of thermosensory neurons and their downstream neuronal circuits or neuropeptides on the peripheral organs.
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Seasonal Adaptation of Mammalian Development: Effect of Early-Life Photoperiod on Reproduction, Somatic Growth, and Neurobehavioral Systems
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For the survival and efficient breeding of wild-living animals, it is crucial to predict seasonal changes and prepare appropriate physiological functions and neurobehavioral mechanisms. In mammals, photoperiod serves as a reliable cue for seasonal changes in the environment, primarily transmitted by melatonin. This review focuses on the seasonal adaptation of mammalian development, specifically the effect of early-life photoperiod on reproductive, somatic, and neurobehavioral development in small- and large-sized mammals. Prediction of seasons through early-life photoperiod is particularly important for small mammals, which have relatively short longevity, to adjust their maximum growth and breeding ability in appropriate seasons during the birth year or the following round. Brain plasticity, as well as cognitive and emotional behaviors, are also highly modulated by early-life photoperiods for successful mating and spatial memory for foraging. This review first summarizes the basic knowledge and recent progress in the programming and epigenetic regulatory mechanisms of reproductive and neurobehavioral development in small mammals, including C57BL/6J mice, which cannot produce detectable amounts of melatonin. The review then focuses on the influence of perinatal environmental conditions or birth season on adult phenotypes in large livestock and humans. Studies have advanced on the concept of the developmental origins of health and disease (DOHaD). Evidence from large mammals suggests that the prediction of seasons is crucial for high-fitness functions over several years. Finally, this review discusses the association of the season of birth with life course physiology and diseases in humans, and the possible mechanisms.
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