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Adult size in numerous insects is strongly dependent on temperature. In several cases, a temperature-size rule is observed in which developmental temperature and adult size tradeoff. Although several previous studies have demonstrated the temperature-size rule, only a few have explored the relationship between developmental temperature and weapon traits or sexual size dimorphism. This study was conducted to investigate the size of the broad-horned flour beetle Gnatocerus cornutus when it was developed under different temperatures. G. cornutus males possess weapon traits for male-male combat and exhibit sexual size dimorphism in other morphological traits. Results showed that male weapon size and body size complied with the temperature-size rule. Furthermore, the extent of sex dimorphism in genae width, a weapon-supportive trait, were larger at lower temperatures. Our findings suggest that the temperature-size rule also influences the size of sexual traits.

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Many species often show male-male combat for mating opportunities and resources within the species. Sexual selection through this radical combat leads to the evolution of males with exaggerated traits used as weapons, such as horns or mandibles, that often result in victory during combat. However, heterospecific interaction due to errors in species identification has often been observed, which results in decreased mating opportunities within the same species and fewer fertilized eggs. Males with exaggerated weapons may show dominance in resource acquisition over males without weapons and may decrease the reproductive success of the latter due to competition between the two. However, few studies have examined heterospecific interaction focusing on males with or without weapons. In this study, we investigated the effects of the male weapon on reproductive traits in heterospecific interaction in two species: the broad-horned flour beetle (Gnatocerus cornutus), in which males have exaggerated weapon traits; and the red flour beetle (Tribolium castaneum), in which males have no weapon traits. Both species are closely related and use the same food resources. G. cornutus males interfered with the resource acquisition and reproductive opportunities of T. castaneum by attacking T. castaneum. The reproductive success of T. castaneum decreased when they cohabited with G. cornutus males. These findings show that male weapon traits, which are important for sexual selection within the same species, can also greatly influence reproduction in other species.

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Movement is an important behavior observed in a wide range of taxa. Previous studies have examined genes controlling movement using wing polymorphic insects and genes controlling wing size. However, few studies have investigated genes controlling movement activity rather than morphological traits. In the present study, we conducted RNA sequencing using populations with higher (WL) and lower (WS) mobility established by artificial selection in the red flour beetle Tribolium castaneum and compared gene expression levels between selected populations with two replicate lines. As a result, we found significant differences between the selected populations in 677 genes expressed in one replicate line and 1198 genes expressed in another replicate line, of which 311 genes were common to the two replicate lines. Furthermore, quantitative PCR focusing on 6 of these genes revealed that neuropeptide F receptor gene (NpF) was significantly more highly expressed in the WL population than in the WS population, which was common to the two replicate lines. We discuss differences in genes controlling movement between walking activity and wing polymorphism.

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Death-feigning behaviour is a phenomenon in which a prey is rendered motionless due to stimulation or threat from a predator. This anti-predator defence mechanism has been observed across numerous animal taxa and is considered adaptive in nature. However, longer durations of death feigning can result in decreased opportunities for feeding and reproduction, and therefore is often associated with fitness costs as compared to environments without predators. Differences have also been observed in the frequencies and durations of death feigning within populations, and these differences are thought to be influenced by the balance between survival and other fitness costs. Furthermore, this balance is predicted to vary in response to changes in environmental conditions. In this study, we examined the death feigning in 38 populations of the red flour beetle (Tribolium castaneum). Our results demonstrate that frequencies and durations of the death feigning in T. castaneum show geographical variations and a latitude cline, indicating that this behaviour is influenced by location as well as latitude. This study is the first to demonstrate the existence of a latitudinal cline in death feigning and suggests that death-feigning behaviour might have evolved in response to environmental factors that vary with latitude.

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Locomotor performance is an indicator of dynamic exercise; thus, it is a central trait in many animal behaviours. Although higher locomotor endurance may increase male reproductive success (e.g., in mate searching and male-male contests), investment in other male reproductive traits (e.g., male attractiveness and sperm competition) may be decreased through energy consumption due to higher activity levels. Here, I investigated male attractiveness, mating success, and paternity success using males of the red flour beetle Tribolium castaneum selected for higher (H) and lower (L) locomotor endurance. Although there was no difference in male attractiveness between the selection regimes, H males had significantly higher mating success than L males. Conversely, L males had significantly higher paternity success than H males. Therefore, there was a trade-off between mating success and paternity success among the selection regimes, suggesting that locomotor endurance affects male reproduction in T. castaneum, and individual variation of locomotor endurance may be maintained within a population.

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Reciprocal crossing of different strains is a suitable method to investigate the dominance and inheritance of a focal trait. Herein, we performed reciprocal crossing among strains of Tribolium castaneum exhibiting a genetically high (H strain) and low (L strain) moving activity and investigated the related heritable factors in the F1 and F2 generations. We also evaluated death-feigning behavior, which negatively responded to artificial selection for moving activity in T. castaneum. The results obtained for the F1 generation suggest that low moving activity and short duration of death feigning were dominant. In the F2 generation, movement and death feigning exhibited continuous segregation. The distribution of each trait value in the F2 generation differed from that in the parental generation, and no individuals transgressing the distribution of trait values in the parental generation emerged in the F2 generation. These results suggest that the genetic correlation between movement and death-feigning behavior is controlled in a polygenic manner. Moreover, the examination of the proportions of both behaviors (high vs. low moving activity and long vs. short death-feigning duration) in the F1 generation revealed that the two behaviors may be controlled by the maternal genotype, suggesting that the gene(s) that control movement and death feigning are located on the sex chromosome in T. castaneum.

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Death-feigning behavior is an anti-predatory technique used in several animal taxa and often correlates with inhibited movements (i.e., death-feigning syndrome). We performed a reciprocal crossing among strains exhibiting a genetically longer (L-strain) and shorter (S-strain) duration of death feigning. Then, we investigated related heritable factors in F1 and F2 populations. We also evaluated movement activities, which negatively responded to artificial selection for death feigning in T. castaneum. Our results indicated that death feigning occurred more frequently and for shorter periods in the F1 population. However, in the F2 population, death feigning and movement exhibited continuous segregation. Although the distribution of each trait value in the F2 generation differed from that of the parental generation, no individuals transgressing the distribution of trait values in the parental generation emerged from the F2 generation. Besides, chi-square analysis of the observed death feigning and movement of F1 and F2 progenies rejected the hypothesis of mono-major gene inheritance. These results suggested that the death-feigning syndrome was polygenically controlled, indicating the usefulness of reciprocal crossing experiments in assessing the quantitative inheritance of behavioral traits.

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Whole-organism performance, including locomotor activity, is an important fitness trait in many animals. Locomotor activity is often classified into sprint speed and locomotor endurance and differences in sprint speed and locomotor endurance affect on other traits such as life-history traits. Previous studies found that locomotor endurance, sprint speed and brain dopamine (DA) levels are correlated with artificial selection for death feigning (an anti-predator behaviour that we refer to as 'death-feigning syndrome') in some insect species. Thus, if the syndrome has a genetic basis, death feigning, sprint speed and brain DA levels may be affected by artificial selection for locomotor endurance. We artificially selected for locomotor endurance over 10 generations in the red flour beetle Tribolium castaneum, and established higher (H) and lower activity (L) strains, then compared their death-feigning behaviour, sprint speed and brain DA levels. H-strain beetles exhibited significantly shorter duration of death-feigning, and significantly higher sprint speeds, suggesting variation in death-feigning syndrome. Surprisingly, although brain DA expression affects various animal behaviours, we found no significant differences in the brain DA expressions of H- and L-strain beetles. Thus, our results imply genetic correlations between locomotor endurance, sprint speed and death feigning, but not with brain DA expression, suggesting that differences in the biogenic amine results of our and previous studies may reflect differences in behavioural expression mechanisms.

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Prey evolve antipredator strategies against multiple enemies in nature. We examined how a prey species adopts different predation avoidance tactics against pursuit or sit-and-wait predators. As prey, we used three strains of Tribolium beetles artificially selected for short (short strain) or long (long strain) duration of death feigning, and a stock culture (base population). Death feigning is known to be effective for evading a jumping spider in the case of the long strains, while the present study showed that the long-strain beetles used freezing against a sit-and-wait type predator, Amphibolus venator, in this study. The short- strain beetles were more easily oriented toward predators. The time to predation was also shorter in the short strains compared to the long strains. The results showed that, as prey, the short strains displayed the same behavior, escaping, against both types of predators. Traditionally, death feigning has been thought to be the last resort in a series of antipredator avoidance behaviors. However, our results showed that freezing and death feigning were not parts of a series of behaviors, but independent strategies against different predators, at least for long-strain beetles. We also examined the relationship between a predator's starvation level and its predatory behavior. In addition, the orientation behavior toward and predation rate on the prey were observed to determine how often the predatory insect attacked the beetles.

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Predator avoidance is an important behavior that affects the degree of adaptation of organisms. We compared the DNA variation of one of the predator-avoidance behaviors, the recently extensively studied "death-feigning behavior", between the long strain bred for feigning death for a long time and the short strain bred for feigning death for a short time. To clarify how the difference in DNA sequences between the long and short strains corresponds to the physiological characteristics of the death-feigning duration at the transcriptome level, we performed comprehensive and comparative analyses of gene variants in Tribolium castaneum strains using DNA-resequencing. The duration of death feigning involves many gene pathways, including caffeine metabolism, tyrosine metabolism, tryptophan metabolism, metabolism of xenobiotics by cytochrome P450, longevity regulating pathways, and circadian rhythm. Artificial selection based on the duration of death feigning results in the preservation of variants of genes in these pathways in the long strain. This study suggests that many metabolic pathways and related genes may be involved in the decision-making process of anti-predator animal behavior by forming a network in addition to the tyrosine metabolic system, including dopamine, revealed in previous studies.

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Since the variables inherent to various diseases cannot be controlled directly in humans, behavioral dysfunctions have been examined in model organisms, leading to better understanding their underlying mechanisms. However, because the spatial and temporal scales of animal locomotion vary widely among species, conventional statistical analyses cannot be used to discover knowledge from the locomotion data. We propose a procedure to automatically discover locomotion features shared among animal species by means of domain-adversarial deep neural networks. Our neural network is equipped with a function which explains the meaning of segments of locomotion where the cross-species features are hidden by incorporating an attention mechanism into the neural network, regarded as a black box. It enables us to formulate a human-interpretable rule about the cross-species locomotion feature and validate it using statistical tests. We demonstrate the versatility of this procedure by identifying locomotion features shared across different species with dopamine deficiency, namely humans, mice, and worms, despite their evolutionary differences.

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Bet-hedging via polyandry (spreading the extinction risk of the female's lineage over multiple males) may explain the evolution of female multiple mating, which is found in a wide range of animal and plant taxa. This hypothesis posits that females can increase their fitness via polyandrous mating when "unsuitable" males (i.e., males causing reproductive failure for various reasons) are frequent in the population and females cannot discriminate such unsuitable mates. Although recent theoretical studies have shown that polyandry can operate as a bet-hedging strategy, empirical tests are scarce. In the present study, we tested the bet-hedging polyandry hypothesis by using the red flour beetle Tribolium castaneum. We compared female reproductive success between monandry and polyandry treatments when females mated with males randomly collected from an experimental population, including 20% irradiated (infertile) males. In addition, we evaluated geometric mean fitness across multiple generations as the index of adaptability of bet-hedging traits. Polyandrous females showed a significantly higher egg hatching rate and higher geometric mean fitness than monandrous females. These results strongly support the bet-hedging polyandry hypothesis.

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Many species show rhythmicity in activity, from the timing of flowering in plants to that of foraging behavior in animals. The free-running periods and amplitude (sometimes called strength or power) of circadian rhythms are often used as indicators of biological clocks. Many reports have shown that these traits are highly geographically variable, and interestingly, they often show latitudinal or longitudinal clines. In many cases, the higher the latitude is, the longer the free-running circadian period (i.e., period of rhythm) in insects and plants. However, reports of positive correlations between latitude or longitude and circadian rhythm traits, including free-running periods, the power of the rhythm and locomotor activity, are limited to certain taxonomic groups. Therefore, we collected a cosmopolitan stored-product pest species, the red flour beetle Tribolium castaneum, in various parts of Japan and examined its rhythm traits, including the power and period of the rhythm, which were calculated from locomotor activity. The analysis revealed that the power was significantly lower for beetles collected in northern areas than southern areas in Japan. However, it is worth noting that the period of circadian rhythm did not show any clines; specifically, it did not vary among the sampling sites, despite the very large sample size (n = 1585). We discuss why these cline trends were observed in T. castaneum.

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Tonic immobility and escape are adaptive anti-predator tactics used by many animals. Escape requires movement, whereas tonic immobility does not. If anti-predator tactics relate to weapon size, males with larger weapons may adopt tonic immobility, whereas males with smaller weapons may adopt escape. However, no study has investigated the relationship between weapon size and anti-predator tactics. In this study, we investigated the relationship between male weapon size and tonic immobility in the beetle Gnathocerus cornutus. The results showed that tonic immobility was more frequent in males with larger weapons. Although most studies of tonic immobility in beetles have focused on the duration, rather than the frequency, tonic immobility duration was not affected by weapon size in G. cornutus. Therefore, this study is the first, to our knowledge, to suggest that the male weapon trait affects anti-predator tactics.

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A comparative analysis of animal behavior (e.g., male vs. female groups) has been widely used to elucidate behavior specific to one group since pre-Darwinian times. However, big data generated by new sensing technologies, e.g., GPS, makes it difficult for them to contrast group differences manually. This study introduces DeepHL, a deep learning-assisted platform for the comparative analysis of animal movement data, i.e., trajectories. This software uses a deep neural network based on an attention mechanism to automatically detect segments in trajectories that are characteristic of one group. It then highlights these segments in visualized trajectories, enabling biologists to focus on these segments, and helps them reveal the underlying meaning of the highlighted segments to facilitate formulating new hypotheses. We tested the platform on a variety of trajectories of worms, insects, mice, bears, and seabirds across a scale from millimeters to hundreds of kilometers, revealing new movement features of these animals.

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Death feigning is considered to be an adaptive antipredator behaviour. Previous studies on Tribolium castaneum have shown that prey which death feign have a fitness advantage over those that do not when using a jumping spider as the predator. Whether these effects are repeatable across species or whether they can be seen in nature is, however, unknown. Therefore, the present study involved two experiments: (a) divergent artificial selection for the duration of death feigning using a related species T. freemani as prey and a predatory bug as predator, demonstrating that previous results are repeatable across both prey and predator species, and (b) comparison of the death-feigning duration of T. castaneum populations collected from field sites with and without predatory bugs. In the first experiment, T. freemani adults from established selection regimes with longer durations of death feigning had higher survival rates and longer latency to being preyed on when they were placed with predatory bugs than the adults from regimes selected for shorter durations of death feigning. As a result, the adaptive significance of death-feigning behaviour was demonstrated in another prey-predator system. In the second experiment, wild T. castaneum beetles from populations with predators feigned death longer than wild beetles from predator-free populations. Combining the results from these two experiments with those from previous studies provided strong evidence that predators drive the evolution of longer death feigning.

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The molecular basis of death feigning, an antipredator behavior that has received much attention recently, was analyzed. We compared the gene expression profiles of strains with different behaviors, i.e., different durations of death feigning, in the beetle Tribolium castaneum. Beetles artificially selected for short (S) and long (L) durations of death feigning for many generations were compared thoroughly by RNA sequencing. We identified 518 differentially expressed genes (DEGs) between the strains. The strains also showed divergence in unexpected gene expression regions. As expected from previous physiological studies, genes associated with the metabolic pathways of tyrosine, a precursor of dopamine, were differentially expressed between the S and L strains; these enzyme-encoding genes were expressed at higher levels in the L strain than in the S strain. We also found that several genes associated with insulin signaling were expressed at higher levels in the S strain than in the L strain. Quantitative real-time PCR analysis showed that the relative expression levels of Tchpd (encoding 4-hydroxyphenylpyruvate dioxygenase, Hpd) and Tcnat (encoding N-acetyltransferase, Nat) were significantly higher in the L strain than in the S strain, suggesting the influence of these enzymes on the supply of dopamine and duration of death feigning.

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Tonic immobility (TI) is an effective anti-predator strategy. However, long immobility status on the ground increases the risk of being eaten by predators, and thus insects must rouse themselves when appropriate stimulation is provided. Here, the strength of vibration causing arousal from the state of TI was examined in strains artificially selected for longer duration of TI (L-strains: long sleeper) in a beetle. We provided different strengths of vibration stimuli to the long sleepers in Tribolium castaneum. Although immobilized beetles were never awakened by the stimuli from 0.01 to 0.12 mm in amplitude, almost of the beetles were aroused from immobilized status by the stimulus at 0.21 mm. There was a difference in sensitivity of individuals when the stimuli of 0.14 mm and 0.18 mm were provided. F2 individuals were also bred by crossing experiments of the strains selected for shorter and longer duration of TI. The arousal sensitivity to vibration was well separated in the F2 individuals. A positive relationship was observed between the duration of TI and the vibration amplitude, suggesting that immobilized beetles are difficult to arouse from a deep sleep, while light sleepers are easily aroused by even small vibrations. The results indicate a genetic basis for sensitivity to arousal from TI.

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In many animals, movement often affects fitness components such as foraging or migration. On the other hand, individuals with higher mobility also often have fitness costs. This trade-off between movement and other traits may explain the maintenance of variation in moving ability in a population. However, few studies have focused on movement by walking, although many previous studies of insects have investigated the evolution of variations in mobility with wing polymorphism. In this study, we focused on the walking ability of the red flour beetle (Tribolium castaneum) and investigated whether females with higher than lower walking ability have fitness costs. The present results showed that females with genetically higher walking ability produced smaller eggs and had lower starvation resistance than females with lower walking ability. These results suggest that higher walking ability is costly for females, and this fitness cost may explain maintenance of variations of walking ability in a population.

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