2024/10/01 更新

写真a

オカダ ヤスカズ
岡田 泰和
OKADA Yasukazu
所属
大学院理学研究科 理学専攻 生命理学 教授
大学院担当
大学院理学研究科
学部担当
理学部 生命理学科
職名
教授
 

論文 45

  1. A specific type of insulin-like peptide regulates the conditional growth of a beetle weapon 査読有り 国際誌

    Yasukazu Okada, Masako Katsuki, Naoki Okamoto, Haruna Fujioka, Kensuke Okada

    PLoS Biology   17 巻 ( 11 ) 頁: e3000541   2019年

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:PUBLIC LIBRARY SCIENCE  

    Evolutionarily conserved insulin/insulin-like growth factor (IGF) signaling (IIS) has been identified as a major physiological mechanism underlying the nutrient-dependent regulation of sexually selected weapon growth in animals. However, the molecular mechanisms that couple nutritional state with weapon growth remain largely unknown. Here, we show that one specific subtype of insulin-like peptide (ILP) responds to nutrient status and thereby regulates weapon size in the broad-horned flour beetle Gnatocerus cornutus. By using transcriptome information, we identified five G. cornutus ILP (GcorILP1-5) and two G. cornutus insulin-like receptor (GcorInR1, -2) genes in the G. cornutus genome. RNA interference (RNAi)-mediated gene silencing revealed that a certain subtype of ILP, GcorILP2, specifically regulated weapon size. Importantly, GcorILP2 was highly and specifically expressed in the fat body in a condition-dependent manner. We further found that GcorInR1 and Gcor-InR2 are functionally redundant but that the latter is partially specialized for regulating weapon growth. These results strongly suggest that GcorILP2 is an important component of the developmental mechanism that couples nutritional state to weapon growth in G. cornutus. We propose that the duplication and subsequent diversification of IIS genes played a pivotal role in the evolution of the complex growth regulation of secondary sexual traits.

    DOI: 10.1371/journal.pbio.3000541

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  2. Social dominance alters nutrition-related gene expression immediately: transcriptomic evidence from a monomorphic queenless ant 査読有り 国際誌

    Yasukazu Okada, Yutaka Watanabe, Mandy M.Y. Tin, Kazuki Tsuji, Alexander S. Mikheyev

    Molecular Ecology   26 巻 ( 11 ) 頁: 2922 - 2938   2017年6月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:WILEY  

    Queen–worker differentiation in eusocial organisms may have originated from decoupling of maternal care and reproductive behaviours. Recent advances in sequencing techniques have begun to elucidate the molecular basis of queen–worker differentiation. However, current knowledge of the molecular basis of caste differentiation is limited, especially to species with morphological castes. It seems likely that at the dawn of eusociality morphologically undifferentiated, monomorphic females underwent physiological differentiation that yielded egg-laying and caretaking castes. The molecular basis of such physiological differentiation may provide evolutionary insight into the emergent state of eusociality. In this study, we identify genes associated with monomorphic caste differentiation, specifically focusing on the onset of queen–worker differentiation, using a monomorphic queenless ant, Diacamma sp., that secondarily lost morphological castes. Using individuals experimentally manipulated to become sterile or reproductive, we identified 1546 caste-biased transcripts in brain and 10 in gaster. Because caste differentiation occurs in Diacamma soon after eclosion via behavioural dominance, identified transcripts are interpreted as molecular agents responding immediately to dominance rank formation. Among identified genes, expression levels of genes involved in nutrition processing and storage, such as insulin signalling genes and hexamerins, were strongly altered soon after dominance rank formation. We conclude that the rapid modification of nutrition-related genes in response to social rank may be the fundamental mechanism underlying caste differentiation in Diacamma. Together with functional evidence from the literature, we show that a specific set of genes frequently plays a role in reproductive differentiation across systems with and without morphological castes.

    DOI: 10.1111/mec.13989

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  3. Ant circadian activity associated with brood care type 査読有り 国際誌

    Haruna Fujioka, Masato S. Abe, Taro Fuchikawa, Kazuki Tsuji, Masakazu Shimada, Yasukazu Okada

    Biology Letters   13 巻 ( 2 )   2017年2月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:ROYAL SOC  

    In group-living animals, social interactions influence various traits including circadian activity. Maternal care, in particular, can have a strong effect on the circadian activity of parents or nurses across taxa. In social insects, nestmates are known to have diverse activity rhythms; however, what kind of social environment is crucial in shaping an individual's rhythm is largely unknown. Here, we show that the focal brood types being taken care of (i.e. egg, larva and pupa) have significant effects on individual activity/rest rhythm, using the monomorphic ant Diacamma (putative species indicum). When isolated from a colony, nurses exhibited a clear circadian rhythm. However, when paired with eggs or larvae, they exhibited around-the-clock activity with no apparent rhythm. In contrast, a clear activity rhythm emerged when nurses were paired with a pupa, requiring little care. Such brood-type-specific changes in circadian activity are considered to arise from the difference in caretaking demands. Our finding may contribute to the understanding of the organization of a colony in the context of behavioural variability under different microenvironments.

    DOI: 10.1098/rsbl.2016.0743

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  4. Queen contact and among-worker interactions dually suppress worker brain dopamine as a potential regulator of reproduction in an ant 査読有り

    Hiroyuki Shimoji, Hitoshi Aonuma, Toru Miura, Kazuki Tsuji, Ken Sasaki, Yasukazu Okada

    Behavioral Ecology and Sociobiology   71 巻 ( 2 )   2017年2月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:SPRINGER  

    Abstract: How individual organisms whose behavior is potentially driven by selfish interests cooperate to form a society is a central question in evolutionary biology. Worker reproduction and its suppression in eusocial insects provide an illuminating model of such a conflict resolution. Although many theoretical and empirical studies focus on the nature and evolutionary consequences of this reproductive conflict, little is known about its physiological underpinnings. Here, we hypothesized that the dopaminergic system, which has a gonadotropic function in eusocial Hymenoptera, is controlled by social suppression via the queen presence signal and the worker-worker dominance interactions. In Diacamma sp. from Japan, the queen presence signal is transferred to workers by direct contact, and worker-worker dominance interaction occurs commonly in large colonies, even when a queen is present. Using the ant Diacamma sp., we showed that the aggressive interactions among workers suppressed brain dopamine levels of the workers. Moreover, our data suggest that the queen presence signal transmitted by direct contact suppresses the brain dopamine level and the transcription of dopamine synthetic enzyme (ddc) of workers. Our data provide clear empirical evidence that worker brain dopamine is suppressed by both social stimuli directed from dominant workers and the queen. Significance statement: In eusocial Hymenoptera, worker reproduction is suppressed by social interactions such as queen presence information and dominance interaction. Dopamine, one of the biogenic amines, is a well-known gonadotropic neurohormone in eusocial Hymenoptera. Honeybee studies revealed that the queen presence information regulated dopamine levels in worker brains. In an ant, the dominance interaction also controlled dopamine levels of workers. In a queenless ant Diacamma sp., queen presence information and dominance interaction are known to dually suppress worker reproduction. Given the above examples, dopaminergic signaling is predicted to be a general mechanism that can suppress worker reproduction in multiple ways. We here test whether both the queen- and worker-originated signals (i.e., queen presence information and dominance interaction) affect the worker dopamine level. We show that dopaminergic signaling is affected by dual social factors, suggesting the general role of dopaminergic signaling in mediating social interaction and reproductive suppression.

    DOI: 10.1007/s00265-016-2263-3

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  5. Histone deacetylases control module-specific phenotypic plasticity in beetle weapons 査読有り 国際誌

    Takane Ozawa, Tomoko Mizuhara, Masataka Arata, Masakazu Shimada, Teruyuki Niimi, Kensuke Okada, Yasukazu Okada, Kunihiro Ohta

    Proceedings of the National Academy of Sciences of the United States of America   113 巻 ( 52 ) 頁: 15042 - 15047   2016年12月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:NATL ACAD SCIENCES  

    Nutritional conditions during early development influence the plastic expression of adult phenotypes. Among several body modules of animals, the development of sexually selected exaggerated traits exhibits striking nutrition sensitivity, resulting in positive allometry and hypervariability distinct from other traits. Using de novo RNA sequencing and comprehensive RNA interference (RNAi) for epigenetic modifying factors, we found that histone deacetylases (HDACs) and polycomb group (PcG) proteins preferentially influence the size of mandibles (exaggerated male weapon) and demonstrate nutrition-dependent hypervariability in the broad-horned flour beetle, Gnatocerus cornutus. RNAi-mediated HDAC1 knockdown (KD) in G. cornutus larvae caused specific curtailment of mandibles in adults, whereas HDAC3 KD led to hypertrophy. Notably, these KDs conferred opposite effects on wing size, but little effect on the size of the core body and genital modules. PcG RNAi also reduced adult mandible size. These results suggest that the plastic development of exaggerated traits is controlled in a module-specific manner by HDACs.

    DOI: 10.1073/pnas.1615688114

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  6. Social dominance and reproductive differentiation mediated by dopaminergic signaling in a queenless ant 査読有り 国際誌

    Yasukazu Okada, Ken Sasaki, Satoshi Miyazaki, Hiroyuki Shimoji, Kazuki Tsuji, Toru Miura

    Journal of Experimental Biology   218 巻 ( 7 ) 頁: 1091 - 1098   2015年4月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:COMPANY OF BIOLOGISTS LTD  

    In social Hymenoptera withnomorphological caste, adominantfemale becomes an egg layer, whereas subordinates become sterile helpers. The physiological mechanism that links dominance rank and fecundity is an essential part of the emergence of sterile females, which reflects the primitive phase of eusociality. Recent studies suggest that brain biogenic amines are correlated with the ranks in dominance hierarchy. However, the actual causality between aminergic systems and phenotype (i.e. fecundity and aggressiveness) is largely unknown due to the pleiotropic functions of amines (e.g. age-dependent polyethism) and the scarcity of manipulation experiments. To clarify the causality among dominance ranks, amine levels and phenotypes, we examined the dynamics of the aminergic system during the ontogeny of dominance hierarchy in the queenless ant Diacamma sp., which undergoes rapid physiological differentiation based on dominance interactions. Brain dopamine levels differed between dominants and subordinates at day 7 after eclosion, although they did not differ at day 1, reflecting fecundity but not aggressiveness. Topical applications of dopamine to the subordinate workers induced oocyte growthbut didnot induceaggressiveness, suggestingthegonadotropic effect of dopamine. Additionally, dopamine receptor transcripts (dopr1 and dopr2) were elevated in the gaster fat body of dominant females, suggesting that the fat body is a potential target of neurohormonal dopamine. Based on this evidence, we suggest that brain dopamine levels are elevated in dominants as a result of hierarchy formation, and differences in dopamine levels cause the reproductive differentiation, probably via stimulation of the fat body.

    DOI: 10.1242/jeb.118414

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  7. Ovarian development and insulin-signaling pathways during reproductive differentiation in the queenless ponerine ant Diacamma sp. 査読有り

    Yasukazu Okada, Satoshi Miyazaki, Hitoshi Miyakawa, Asano Ishikawa, Kazuki Tsuji, Toru Miura

    JOURNAL OF INSECT PHYSIOLOGY   56 巻 ( 3 ) 頁: 288 - 295   2010年3月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:PERGAMON-ELSEVIER SCIENCE LTD  

    In many social hymenopteran species, workers possess functional ovaries that are physiologically inactive in the presence of queens. We investigated the ovarian regulatory mechanism of workers and reproductives in a queenless ponerine ant, Diacamma sp., using histological and molecular techniques. In this ant, clear reproductive differentiation occurs via a highly sophisticated dominance behavioral interaction called "gemmae mutilation". This clear and rapid bifurcation of reproductive physiology allows us to elucidate the detailed ovarian differentiation process. Histological characteristics of functional ovaries (fusomes and ring canals) were found in both workers and reproductives, suggesting that early oogenesis is not blocked in workers. Since insulin/insulin-like growth factor signaling (IIS) is known to control insect reproduction, orthologs of 2 positive Its regulators, insulin receptor and serine-threonine kinase Akt (protein kinase B), were cloned in Diacamma (DiaInR, DiaAkt); their expression patterns during reproductive differentiation were examined by real-time quantitative polymerase chain reaction; DiaInR and DiaAkt were strongly expressed in the gasters of reproductives. Whole-mount in situ hybridization of ovaries indicated that DiaInR and DiaAkt were expressed in nurse cells, oocytes, and upper germarial regions of reproductives but not of workers. Our data suggest that the IIS pathway accounts for reproductive differentiation in late oogenesis. (C) 2009 Elsevier Ltd. All rights reserved.

    DOI: 10.1016/j.jinsphys.2009.10.013

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  8. No sign of reproductive cessation in the old workers of a queenless ponerine ant

    Kodai Kishino, Keiko Sakiyama, Haruna Fujioka, Yasukazu Okada

    Behavioral Ecology and Sociobiology   78 巻 ( 3 )   2024年2月

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    掲載種別:研究論文(学術雑誌)   出版者・発行元:Springer Science and Business Media LLC  

    Abstract

    In many social hymenopterans, workers of different ages engage in different tasks; younger workers remain inside the nest as intranidal workers, while older workers go outside the nest as extranidal workers (i.e., age polyethism). Previous studies have shown that ovarian activity is diminished in old, extranidal workers, but it remains unclear whether workers’ reproductive ability persists for life or whether they exhibit post-reproductive lifespans. In this study, we investigated the age-dependence of worker reproductive ability in a monomorphic ponerine ant Diacamma cf. indicum. In Diacamma ants, all females in a colony have reproductive ability, but effective reproduction is limited to one or a few dominant females, and the remaining females act as sterile helpers. Using long-term laboratory rearing, we investigated whether worker reproductive ability lasts throughout a worker’s lifetime. The ages of workers were accurately tracked, and the reproductive ability of young and old workers was examined by creating several gamergate-less sub-colonies. Results showed that at least one individual in each sub-colony developed ovaries, even in the sub-colonies that solely consisted of very old workers (> 252 days old). Interestingly, in the presence of younger workers, old workers rarely showed ovarian development. Besides age, we found a positive correlation between the amount of fat (i.e., nutritional condition) and ovarian development in old workers. Our data suggest that reproductive activity of old workers is low but maintained throughout their life in Diacamma.

    Significance statement

    Females of social animals, such as cetaceans, are known to stop reproducing before the end of their lifespan. It is suggested that the reproductive ability of ant queens does not decline and is maintained throughout their lives; however, it is unclear whether this is also true in ant workers. We maintained ant colonies for more than 500 days and then tested whether the reproductive ability of ant workers is maintained throughout their lifespan. Even in small groups composed of only very old workers (> 252 days old), at least one individual in each group always reproduced actively. Interestingly, the presence of young workers seemed to suppress the reproduction of old workers. In addition, fat content was positively associated with the individual’s reproductive potential.

    DOI: 10.1007/s00265-024-03445-8

    その他リンク: https://link.springer.com/article/10.1007/s00265-024-03445-8/fulltext.html

  9. Transcriptomic and functional screening of weapon formation genes implies significance of cell adhesion molecules and female-biased genes in broad-horned flour beetle

    Miyu Sugiyama, Takane Ozawa, Kunihiro Ohta, Kensuke Okada, Teruyuki Niimi, Katsushi Yamaguchi, Shuji Shigenobu, Yasukazu Okada

    PLOS Genetics   19 巻 ( 12 ) 頁: e1011069 - e1011069   2023年12月

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    掲載種別:研究論文(学術雑誌)   出版者・発行元:Public Library of Science (PLoS)  

    For understanding the evolutionary mechanism of sexually selected exaggerated traits, it is essential to uncover its molecular basis. By using broad-horned flour beetle that has male-specific exaggerated structures (mandibular horn, head horn and gena enlargement), we investigated the transcriptomic and functional characters of sex-biased genes. Comparative transcriptome of male vs. female prepupal heads elucidated 673 sex-biased genes. Counter-intuitively, majority of them were female-biased (584 genes), and GO enrichment analysis showed cell-adhesion molecules were frequently female-biased. This pattern motivated us to hypothesize that female-biased transcripts (i.e. the transcripts diminished in males) may play a role in outgrowth formation. Potentially, female-biased genes may act as suppressors of weapon structure. In order to test the functionality of female-biased genes, we performed RNAi-mediated functional screening for top 20 female-biased genes and 3 genes in the most enriched GO term (cell-cell adhesion, fat1/2/3, fat4 and dachsous). Knockdown of one transcription factor, zinc finger protein 608 (zfp608) resulted in the formation of male-like gena in females, supporting the outgrowth suppression function of this gene. Similarly, knockdown of fat4 induced rudimental, abnormal mandibular horn in female. fat1/2/3<sup>RNAi</sup>, fat4<sup>RNAi</sup> and dachsous<sup>RNAi</sup> males exhibited thick and/or short mandibular horns and legs. These cell adhesion molecules are known to regulate tissue growth direction and known to be involved in the weapon formation in Scarabaeoidea beetles. Functional evidence in phylogenetically distant broad-horned flour beetle suggest that cell adhesion genes are repeatedly deployed in the acquisition of outgrowth. In conclusion, this study clarified the overlooked functions of female-biased genes in weapon development.

    DOI: 10.1371/journal.pgen.1011069

  10. Natural selection increases female fitness by reversing the exaggeration of a male sexually selected trait

    Kensuke Okada, Masako Katsuki, Manmohan D. Sharma, Katsuya Kiyose, Tomokazu Seko, Yasukazu Okada, Alastair J. Wilson, David J. Hosken

    Nature Communications   12 巻 ( 1 )   2021年12月

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    掲載種別:研究論文(学術雑誌)  

    Theory shows how sexual selection can exaggerate male traits beyond naturally selected optima and also how natural selection can ultimately halt trait elaboration. Empirical evidence supports this theory, but to our knowledge, there have been no experimental evolution studies directly testing this logic, and little examination of possible associated effects on female fitness. Here we use experimental evolution of replicate populations of broad-horned flour beetles to test for effects of sex-specific predation on an exaggerated sexually selected male trait (the mandibles), while also testing for effects on female lifetime reproductive success. We find that populations subjected to male-specific predation evolve smaller sexually selected mandibles and this indirectly increases female fitness, seemingly through intersexual genetic correlations we document. Predation solely on females has no effects. Our findings support fundamental theory, but also reveal unforseen outcomes—the indirect effect on females—when natural selection targets sex-limited sexually selected characters.

    DOI: 10.1038/s41467-021-23804-7

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  11. Social Evolution With Decoupling of Multiple Roles of Biogenic Amines Into Different Phenotypes in Hymenoptera

    Ken Sasaki, Yasukazu Okada, Hiroyuki Shimoji, Hitoshi Aonuma, Toru Miura, Kazuki Tsuji

    Frontiers in Ecology and Evolution   9 巻   2021年5月

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    掲載種別:研究論文(学術雑誌)   出版者・発行元:Frontiers Media SA  

    Convergent evolution of eusociality with the division of reproduction and its plastic transition in Hymenoptera has long attracted the attention of researchers. To explain the evolutionary scenario of the reproductive division of labor, several hypotheses had been proposed. Among these, we focus on the most basic concepts, i.e., the ovarian ground plan hypothesis (OGPH) and the split-function hypothesis (SFH). The OGPH assumes the physiological decoupling of ovarian cycles and behavior into reproductive and non-reproductive individuals, whereas the SFH assumes that the ancestral reproductive function of juvenile hormone (JH) became split into a dual function. Here, we review recent progress in the understanding of the neurohormonal regulation of reproduction and social behavior in eusocial hymenopterans, with an emphasis on biogenic amines. Biogenic amines are key substances involved in the switching of reproductive physiology and modulation of social behaviors. Dopamine has a pivotal role in the formation of reproductive skew irrespective of the social system, whereas octopamine and serotonin contribute largely to non-reproductive social behaviors. These decoupling roles of biogenic amines are seen in the life cycle of a single female in a solitary species, supporting OGPH. JH promotes reproduction with dopamine function in primitively eusocial species, whereas it regulates non-reproductive social behaviors with octopamine function in advanced eusocial species. The signal transduction networks between JH and the biogenic amines have been rewired in advanced eusocial species, which could regulate reproduction in response to various social stimuli independently of JH action.

    DOI: 10.3389/fevo.2021.659160

  12. Octopaminergic system orchestrates combat and mating behaviors: A potential regulator of alternative male mating tactics in an armed beetle

    Katsuya Kiyose, Masako Katsuki, Yû Suzaki, Kensuke Okada, Yasukazu Okada

    Journal of Insect Physiology   131 巻   2021年5月

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    掲載種別:研究論文(学術雑誌)  

    Male-male combats over females and territories are widespread across animal taxa. The winner of a combat gains resources, while the loser suffers significant costs (e.g. time, energy and injury) without gaining resources. Many animals have evolved behavioral flexibility, depending on their nutritional condition and experience, to avoid combat in order to reduce such costs. In these cases, male aggression often correlates with mating behavior changes, that is, the deployment of alternative reproductive tactics. Therefore, uncovering the physiological mechanism that orchestrates combat and mating behaviors is essential to understand the evolution of alternative mating tactics. However, so far, our knowledge is limited to specific behaviors (i.e., fighting or mating) of specific model species. In this study, we used an armed beetle (Gnatocerus cornutus) and hypothesized that one of the key neuromodulators of invertebrate aggression, octopamine (OA), would control male combat and other mating behaviors. Using receptor agonists (chlordimeform and benzimidazole), we showed that the octopaminergic (OAergic) system down-regulated the combat and courtship behaviors, while it up-regulated locomotor activity and sperm size. This suggests that the OAergic system orchestrates a suite of fighting and mating behaviors, thereby implying that correlated behavioral responses to OAergic signaling may have driven the evolution of alternative mating tactics in this beetle.

    DOI: 10.1016/j.jinsphys.2021.104211

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  13. Bipartite network analysis of ant-task associations reveals task groups and absence of colonial daily activity

    Haruna Fujioka, Yasukazu Okada, Masato S. Abe

    Royal Society Open Science   8 巻 ( 1 )   2021年1月

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    掲載種別:研究論文(学術雑誌)  

    Social insects are one of the best examples of complex self-organized systems exhibiting task allocation. How task allocation is achieved is the most fascinating question in behavioural ecology and complex systems science. However, it is difficult to comprehensively characterize task allocation patterns due to behavioural complexity, such as the individual variation, context dependency and chronological variation. Thus, it is imperative to quantify individual behaviours and integrate them into colony levels. Here, we applied bipartite network analyses to characterize individual-behaviour relationships. We recorded the behaviours of all individuals with verified age in ant colonies and analysed the individual-behaviour relationship at the individual, module and network levels. Bipartite network analysis successfully detected the module structures, illustrating that certain individuals performed a subset of behaviours (i.e. task groups). We confirmed age polyethism by comparing age between modules. Additionally, to test the daily rhythm of the executed tasks, the data were partitioned between daytime and nighttime, and a bipartite network was re-constructed. This analysis supported that there was no daily rhythm in the tasks performed. These findings suggested that bipartite network analyses could untangle complex task allocation patterns and provide insights into understanding the division of labour.

    DOI: 10.1098/rsos.201637

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  14. Sexually selected traits and life history traits of larger and smaller males of the horned flour beetle Gnatocerus cornutus

    Katsuya Kiyose, Yasukazu Okada, Masako Katsuki, Y. Suzaki, Kensuke Okada

    Ecological Entomology   46 巻 ( 4 ) 頁: 807 - 815   2021年

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    掲載種別:研究論文(学術雑誌)  

    1. Expression of sexual weapons is strongly affected by environmental factors in armed insects, resulting in a remarkable morphological difference between larger and smaller males. 2. Morphological differences in weapon between larger and smaller males can promote differences in non-sexual traits. This is because weapon sizes are often associated with developments of non-sexual traits such as somatic traits and life history traits. The resulting different subsets of multiple traits may contribute to the reproductive success of larger and smaller males, respectively. 3. There were relatively few studies that couple differences in life history and reproductive traits between larger and smaller males. Here we investigated differences in morphology, behaviours, and life history in Gnatocerus cornutus. 4. Larger males have relatively larger mandibles and the advantage in male fighting to access females. Also, the developmental period was significantly shorter in the larger males than in the smaller males. 5. Smaller males with rudimentary weapons have higher locomotion. This suggests higher performance in the dispersal to new territories. Larger and smaller males showed different suites of multiple traits, and the combinations of multiple traits are probably related to expression of weapons.

    DOI: 10.1111/een.13016

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  15. Individual Ants Do Not Show Activity-Rest Rhythms in Nest Conditions

    Haruna Fujioka, Masato S. Abe, Yasukazu Okada

    Journal of Biological Rhythms     2021年

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    掲載種別:研究論文(学術雑誌)  

    Circadian rhythms, which respond to the day-night cycle on the earth, arise from the endogenous timekeeping system within organisms, called the “biological clock.” For accurate circadian rhythms, daily fluctuations in light and temperature are considered one of the important time cues. In social insects, both abiotic and biotic factors (i.e., social interactions) play a significant role in activity-rest rhythm regulation. However, it is challenging to monitor individual activity-rest rhythms in a colony because of the large group size and small body size. Therefore, it is unclear whether individuals in a colony exhibit activity-rest rhythms and how social interactions regulate their activity-rest rhythms in the colony. This study developed an image-based tracking system using 2D barcodes for Diacamma cf. indicum from Japan (a monomorphic ant) and measured the locomotor activities of all colony members under laboratory colony conditions. We also investigated the effect of broods on activity-rest rhythms by removing all broods under colony conditions. Activity-rest rhythms appeared only in isolated ants, not under colony conditions. In addition, workers showed arrhythmic activities after brood removal. These results suggested that a mixture of social interactions, and not light and temperature, induces the loss of activity-rest rhythms. These results contribute to the knowledge of a diverse pattern of circadian activity rhythms in social insects.

    DOI: 10.1177/07487304211002934

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  16. Older males are more competitive in male fights and more aggressive toward females in the broad-horned flour beetle Gnatocerus cornutus 査読有り

    Kensuke Okada, Masako Katsuki, Katsuya Kiyose, Yasukazu Okada

    Behavioral Ecology and Sociobiology   74 巻 ( 3 )   2020年3月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:SPRINGER  

    Abstract: In theory, a male should change the allocation of fighting and mating efforts in relation to his age. Thus, the consequences of sexual selection may be complicated by changes in the male resource allocation due to aging. However, previous studies have focused on changes in female mate choice and male-male competition with aging separately, and the impact of aging on the relationship between mate choice and male competition is unknown. Here, we examined how male competitiveness and attractiveness and their relationship changes over male lifespan in Gnatocerus cornutus. In this species, males perform courtship displays and fight rival males for mates. Older males are more competitive in male fighting and aggressive toward females than younger males. The aggression is also directed toward females. Almost all older males who attacked a female failed to copulate, while younger males never attacked the females. As a result, copulation success decreased with age. When an older male did not mistake a female for a male, he exhibited more frequent courtship. However, mating with older males imposed direct costs on females in terms of both fecundity and lifespan, with no offsetting indirect benefits for her offspring. The courtship behavior of older males does not supply females with cues for mate-choice benefits but are used to coerce females into mating. Our results suggest that male–male competition constrains female preference for older males. Thus, female choice and male–male competition may not be reinforcing in older G. cornutus males. Significance statement: When males get older, they often pay more attention to females in a variety of ways, such as courting and fighting for access. This is because older males have not long to live. In Gnatocerus cornutus as well, older males attend to fighting and courting. The older males seem to be competitive in male fights and attractive to females. However, they are not only aggressive toward rival males but also sometimes use violence on females. As a result, these older males are rejected by the assaulted females and cannot mate. Additionally, the violence of older males can reduce female fecundity and lifespan. Thus, mating with older males is costly to females in G. cornutus, and a female preference for older males is not expected to evolve.

    DOI: 10.1007/s00265-020-2815-4

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  17. Polyandry and paternity affect disease resistance in eusocial wasps

    Tatsuya Saga, Masaki Okuno, Kevin J. Loope, Koji Tsuchida, Kako Ohbayashi, Masakazu Shimada, Yasukazu Okada

    Behavioral Ecology   31 巻 ( 5 ) 頁: 1172 - 1179   2020年

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:OXFORD UNIV PRESS INC  

    Polyandry (multiple mating by females) is a central challenge for understanding the evolution of eusociality. Several hypotheses have been proposed to explain its observed benefits in eusocial Hymenoptera, one of which, the parasite-pathogen hypothesis (PPH), posits that high genotypic variance among workers for disease resistance prevents catastrophic colony collapse. We tested the PPH in the polyandrous wasp Vespula shidai. We infected isolated workers with the entomopathogenic fungus Beauveria bassiana and quantified their survival in the laboratory. Additionally, we conducted a paternity analysis of the workers using nine microsatellite loci to investigate the relationship between survival and the matriline and patriline membership of the workers. As predicted by the PPH, nestmate workers of different patrilines showed differential resistance to B. bassiana. We also demonstrated variation in virulence among strains of B. bassiana. Our results are the first to directly support the PPH in eusocial wasps and suggest that similar evolutionary pressures drove the convergent origin and maintenance of polyandry in ants, bees, and wasps.

    DOI: 10.1093/beheco/araa062

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  18. Liquid exchange via stomodeal trophallaxis in the ponerine ant Diacamma sp. from Japan 査読有り

    Haruna Fujioka, Yasukazu Okada

    Journal of Ethology   37 巻 ( 3 ) 頁: 371 - 375   2019年9月

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    担当区分:最終著者   掲載種別:研究論文(学術雑誌)   出版者・発行元:Springer Science and Business Media LLC  

    Trophallaxis plays a major role in the sharing of food in colonies of many social insects, and two modes of this are known: stomodeal (oral) and proctodeal (abdominal) trophallaxis. In social Hymenoptera, only a small proportion of colony members perform the task of food collection, and oral trophallaxis is predominant in their social sharing of food. Typically, foragers distribute liquid food stored in their crop to nestmates via oral trophallaxis. Similar to bees, some ants (Formicidae) forage for liquid food from plant secretions (nectars) and insect exudates (honeydew). While regurgitation is common in ants, it has been documented in only two species of the Ponerinae. Here, we report the ability of Diacamma sp. from Japan to perform trophallaxis. After thirsty ants had been paired with ants provided with colored water, the abdomens of both groups of ants were dissected. The digestive organ was colored red in half of the receivers. In addition, we observed mouth-to-mouth interactions in the laboratory, not “social bucket” behavior (i.e., exchange of liquid held between mandibles). Our results suggest that Diacamma sp. can exchange liquid by true oral trophallaxis and shed new light on social organization via liquid exchange.

    DOI: 10.1007/s10164-019-00602-9

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    その他リンク: http://link.springer.com/article/10.1007/s10164-019-00602-9/fulltext.html

  19. Observation of plugging behaviour reveals entrance-guarding schedule of morphologically specialized caste in Colobopsis nipponicus 査読有り

    Haruna Fujioka, Masato S. Abe, Yasukazu Okada

    Ethology   125 巻 ( 8 ) 頁: 526 - 534   2019年8月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:WILEY  

    The success of social insects is often attributed to the specialized morphologies and behaviours of workers. One of the most elaborate specializations in ant species is the workers’ plugging behaviour, in which their uniquely shaped heads are used for nest defence. These species generally nest in tree cavities. Without morphologically specialized workers (major workers) plugging the nest entrance, nests are easily attacked and replaced by conspecific and heterospecific cavity-dwelling ants and other predators. Therefore, major workers are expected to defend the nest at all times. However, empirical evidence on the social time investment for nest defence is still lacking. Here, we investigated how major workers of Colobopsis nipponicus achieve nest defence (plugging behaviour) in terms of their work schedule. Our results showed that the nests had more major workers than entrances. The observation of artificial plastic nests over 6 days in the laboratory revealed that the nest entrance was guarded almost continuously by multiple major workers. The entrance-guarding schedule was not equally divided among major workers, and there were no clear shift patterns in the timing of changeovers. We highlight the importance of investigating the time investment of workers to fully understand the defence strategies of this morphologically specialized caste.

    DOI: 10.1111/eth.12877

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  20. Loser-effect duration evolves independently of fighting ability 査読有り 国際誌

    Kensuke Okada, Yasukazu Okada, Sasha R.X. Dall, David J. Hosken

    Proceedings of the Royal Society B: Biological Sciences   286 巻 ( 1903 ) 頁: 20190582 - 20190582   2019年5月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:ROYAL SOC  

    Winning or losing contests can impact subsequent competitive behaviour and the duration of these effects can be prolonged. While it is clear effects depend on social and developmental environments, the extent to which they are heritable, and hence evolvable, is less clear and remains untested. Furthermore, theory predicts that winner and loser effects should evolve independently of actual fighting ability, but again tests of this prediction are limited. Here we used artificial selection on replicated beetle populations to show that the duration of loser effects can evolve, with a realized heritability of about 17%. We also find that naive fighting ability does not co-evolve with reductions in the duration of the loser effect. We discuss the implications of these findings and how they corroborate theoretical predictions.

    DOI: 10.1098/rspb.2019.0582

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  21. Ant activity-rest rhythms vary with age and interaction frequencies of workers 査読有り

    Haruna Fujioka, Masato S. Abe, Yasukazu Okada

    Behavioral Ecology and Sociobiology   73 巻 ( 3 )   2019年3月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:SPRINGER  

    Abstract: Social insect colonies are highly organized systems, where communication among nestmates (i.e., social interactions) has a pivotal function for colonial organization. In order to further the understanding of social organization, the chronobiological system of social insect species, particularly their circadian rhythm, has recently attracted much attention. However, gaps still remain in our understanding of how individual active/rest rhythms are governed in various social contexts. In this study, we investigate the effects of worker-worker interactions on circadian activity rhythms, using the monomorphic ant, Diacamma sp. Continuous tracking of solitary ants elucidated circadian activity rhythms, both in young and old workers (< 30 days and > 70 days after eclosion, respectively). The color tag–based automatic tracking of multiple workers revealed that young-old interactions reduced circadian rhythmic activities in both young and old workers, whereas young workers retained active/rest rhythms under young-young worker interactions. Together with the analyses of worker-worker interaction frequencies, we conclude that interactions between workers in different age groups (i.e., workers with different tasks) function as different cues to alter worker active/rest patterns. We discuss the potential roles of worker-worker interactions on the chronobiological organization of the ant society. Significance statement: In social animals, how individual behavioral rhythms are governed by social interactions is a fundamental question towards the mechanistic understanding of complex biological systems. Using an image-based tracking system, we composed artificial ant worker groups consisting of different functions (i.e., young nurses and old foragers) and investigated whether the age composition and the resulting interactions had an effect on the active/rest rhythms of individual workers, and of the whole group. In solitary conditions, both young and old workers showed circadian activity; however, when grouped with workers from different age groups, both young and old workers turned to show weak circadian rhythmicity or around-the-clock activity. Our results suggest that even simple social cues (i.e., frequency of contact with young and old workers) could alter worker activity patterns. To our knowledge, this is the first evidence showing that specific worker-worker interaction induces weakly rhythmic and/or arrhythmic states.

    DOI: 10.1007/s00265-019-2641-8

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  22. Rapid development and characterization of EST-SSR markers for the honey locust seed beetle, Megabruchidius dorsalis (Coleoptera: Bruchidae), using de novo transcriptome analysis based on next-generation sequencing 査読有り

    Kako Ohbayashi, Naoko Ishikawa, Yoshikuni Hodoki, Yasukazu Okada, Shin ichi Nakano, Motomi Ito, Masakazu Shimada

    Applied Entomology and Zoology   54 巻 ( 1 ) 頁: 141 - 145   2019年2月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:SPRINGER JAPAN KK  

    We developed 10 novel simple sequence repeat markers from expressed sequence tags for the honey locust seed beetle, Megabruchidius dorsalis Fåhraeus 1839 (Coleoptera: Bruchidae, using de novo transcriptome analysis based on next-generation sequencing. In a M. dorsalis Harataima (Kanagawa-pref.) population, the number of alleles per locus ranged from 2 to 6, with an average of 4.0. Observed and expected heterozygosities ranged from 0.13 to 0.72 and 0.17 to 0.72, respectively. We initially developed 11 novel markers, but one was eliminated because it showed significant linkage disequilibrium with another locus after Bonferroni correction. To check the applicability of the remaining 10 markers, we used them to analyze two additional geographic populations (Yashima, Akita-pref., and Kameoka, Kyoto-pref.). Mean numbers of alleles per locus in the Yashima and Kameoka populations were 2.6 and 2.9, respectively, with corresponding mean observed heterozygosities of 0.36 and 0.52. These results based on the two additional populations confirm that our developed markers worked efficiently. The simple sequence repeat markers developed from expressed sequence tags in the present study should, therefore, be useful for explicating the population genetic structure of M. dorsalis and for future paternal analyses.

    DOI: 10.1007/s13355-019-00605-5

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  23. Environmental factors affecting pupation decision in the horned flour beetle gnatocerus cornutus 査読有り

    Takane Ozawa, Kunihiro Ohta, Masakazu Shimada, Kensuke Okada, Yasukazu Okada

    Zoological Science   32 巻 ( 2 ) 頁: 183 - 187   2015年4月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:ZOOLOGICAL SOC JAPAN  

    Social environments often affect the development of organisms. In Tenebrionidae beetles, larval development can be arrested at the final instar stage in the presence of conspecific larvae. This developmental plasticity is considered to be an anti-cannibalistic strategy but the critical environmental determinants and actual effects remain to be elucidated. In this study, we examined the effects of the heterospecific environment, conspecific sexual environment (i.e., presence of conspecific male or female), and abiotic physical stimulation on the pupation decision of the sexually dimorphic horned-flour beetle Gnatocerus cornutus. Additionally, actual anti-cannibalistic or antipredatory effects of developmental arrest were evaluated by analyzing stage-dependent vulnerabilities. When G. cornutus larvae were maintained with a G. cornutus larva, a G. cornutus adult, or T. castaneum adult, the developmental period up to the prepupal stage was significantly elongated, suggesting that the cue is not species-specific. Sexual environment did not affect the timing of pupation in G. cornutus; however, we found that abiotic tactile stimulations by glass beads could repress pupation. We also discovered that prepupal and pupal stages were more vulnerable to cannibalism and predation than the larval stage. These data suggest that G. cornutus larvae use non-species specific tactile stimulation as a decision cue for pupation and it has broader defensive effects against heterospecific predation as well as conspecific cannibalism.

    DOI: 10.2108/zs140203

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  24. Relationships among male sexually selected traits in the bean bug, Riptortus pedestris (Heteroptera: Alydidae) 査読有り

    Yû Suzaki, Masako Katsuki, Takahisa Miyatake, Yasukazu Okada

    Entomological Science   18 巻 ( 2 ) 頁: 278 - 282   2015年4月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:WILEY  

    Current concepts of sexual selection suggest that male reproductive success is determined by multiple sexual traits. As expression and production of multiple sexual traits are frequently associated with each other, positive or negative correlations among multiple sexual traits ensue. These relationships among traits associated with male reproductive success may be crucial in the evolution of male reproductive strategies. Here, we investigate phenotypic relationships among sexually selected traits in the armed bean bug Riptortus pedestris. In this insect, males with a larger body and weapon are more likely to win male-male competitions, and males with a larger weapon or higher courtship rate are more attractive to females. There was a significant positive correlation between body size and weapon size, whereas the courtship rate had significant negative correlations with body size and weapon size. Our results suggested that there was a phenotypic trade-off between courtship rate and male morphology. In this insect, smaller males may make more effort in courtship behavior as an alternative mating tactic.

    DOI: 10.1111/ens.12114

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  25. Heat shock proteins mediate trade-offs between early-life reproduction and late survival in Drosophila melanogaster 査読有り

    Yasukazu Okada, Kohei Teramura, Kazuo H. Takahashi

    PHYSIOLOGICAL ENTOMOLOGY   39 巻 ( 4 ) 頁: 304 - 312   2014年12月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:WILEY  

    Ageing and the resulting increased likelihood mortality are the inescapable fate of organisms because selection pressures on genes that exert their function late in life is weak, promoting the evolution of genes that enhance early-life reproductive performance at the same time as sacrificing late survival. Heat shock proteins (HSP) are known to buffer various environmental stresses and are also involved in protein homeostasis and longevity. The characteristics of genes for HSPs (hsp) imply that they affect various life-history traits, which in turn affect longevity; however, little is known about the effects of hsp genes on life-history traits and their interaction with longevity. In the present study, the effects of hsp genes on multiple fitness traits, such as locomotor activity, total fecundity, early fecundity and survival time, are investigated in Drosophila melanogasterMeigen using RNA interference (RNAi). In egg-laying females, RNAi knockdown of six hsp genes (hsp22, hsp23, hsp67Ba, hsp67Bb, hsp67Bc and hsp27-like) does not shorten survival but rather increases it. Knockdown of five of those genes on an individual basis reduces early-life reproduction, suggesting that several hsp genes mediate the trade-off between early reproduction and late survival. The data indicate a positive effect of hsp genes on early reproduction and also negative effects on survival time, supporting the antagonistic pleiotropic effects predicted by the optimality theory of ageing.

    DOI: 10.1111/phen.12076

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  26. Social dominance modifies behavioral rhythm in a queenless ant 査読有り

    Taro Fuchikawa, Yasukazu Okada, Takahisa Miyatake, Kazuki Tsuji

    BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY   68 巻 ( 11 ) 頁: 1843 - 1850   2014年11月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:SPRINGER  

    Social insects provide an intriguing model system in chronobiology. Typically, an egg-laying queen exhibits arrhythmicity in activity while foraging worker has clear rhythmicity. In the queenless ant, Diacamma sp., from Japan, colony members lack morphological caste, and reproductive differentiation occurs as a consequence of dominance hierarchy formation. Their specialized dominance interaction "gemmae mutilation", provide us a fascinating model system to investigate the effect of social dominance on rhythmic ontogeny. Measurement of individual rhythms revealed that they have clear circadian rhythm at eclosion but it is diminished by social mutilation of gemmae. Moreover, unlike highly eusocial species, mated egg-layer (i.e., gamergate) possessed a circadian rhythm even after mating in Diacamma. Measurement of colony-level rhythms revealed that gemmae mutilations are performed in the limited time of the day, but foraging occurs around-the-clock. The above finding is a novel form of temporal organization in social insects, providing a new insight in morphologically casteless species. We discuss the causes and consequences of rhythmic variability in social organization.

    DOI: 10.1007/s00265-014-1793-9

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  27. Sexually Dimorphic Body Color Is Regulated by Sex-Specific Expression of Yellow Gene in Ponerine Ant, Diacamma Sp. 査読有り 国際誌

    Satoshi Miyazaki, Yasukazu Okada, Hitoshi Miyakawa, Gaku Tokuda, Richard Cornette, Shigeyuki Koshikawa, Kiyoto Maekawa, Toru Miura

    PLOS ONE   9 巻 ( 3 ) 頁: e92875   2014年3月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:PUBLIC LIBRARY SCIENCE  

    Most hymenopteran species exhibit conspicuous sexual dimorphism due to ecological differences between the sexes. As hymenopteran genomes, under the haplodiploid genetic system, exhibit quantitative differences between sexes while remaining qualitatively identical, sexual phenotypes are assumed to be expressed through sex-specific gene usage. In the present study, the molecular basis for expression of sexual dimorphism in a queenless ant, Diacamma sp., which exhibits a distinct color dimorphism, was examined. Worker females of the species appear bluish-black, while winged males exhibit a yellowish-brown body color. Initially, observations of the pigmentation processes during pupal development revealed that black pigmentation was present in female pupae but not in males, suggesting that sex-specific melanin synthesis was responsible for the observed color dimorphism. Therefore, five orthologs of the genes involved in the insect melanin synthesis (yellow, ebony, tan, pale and dopa decarboxylase) were subcloned and their spatiotemporal expression patterns were examined using real-time quantitative RT-PCR. Of the genes examined, yellow, which plays a role in black melanin synthesis in insects, was expressed at higher levels in females than in males throughout the entire body during the pupal stage. RNA interference of yellow was then carried out in order to determine the gene function, and produced females with a more yellowish, brighter body color similar to that of males. It was concluded that transcriptional regulation of yellow was responsible for the sexual color dimorphism observed in this species.

    DOI: 10.1371/journal.pone.0092875

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  28. Male Courtship Behavior and Weapon Trait as Indicators of Indirect Benefit in the Bean Bug, Riptortus pedestris 査読有り 国際誌

    Yu Suzaki, Masako Katsuki, Takahisa Miyatake, Yasukazu Okada

    PLOS ONE   8 巻 ( 12 ) 頁: e83278   2013年12月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:PUBLIC LIBRARY SCIENCE  

    Females prefer male traits that are associated with direct and/or indirect benefits to themselves. Male-male competition also drives evolution of male traits that represent competitive ability. Because female choice and male-male competition rarely act independently, exploring how these two mechanisms interact is necessary for integrative understanding of the evolution of sexually selected traits. Here, we focused on direct and indirect benefits to females from male attractiveness, courtship, and weapon characters in the armed bug Riptortus pedestris. The males use their hind legs to fight other males over territory and perform courtship displays for successful copulation. Females of R. pedestris receive no direct benefit from mating with attractive males. On the other hand, we found that male attractiveness, courtship rate, and weapon size were significantly heritable and that male attractiveness had positive genetic covariances with both courtship rate and weapon traits. Thus, females obtain indirect benefits from mating with attractive males by producing sons with high courtship success rates and high competitive ability. Moreover, it is evident that courtship rate and hind leg length act as evaluative cues of female choice. Therefore, female mate choice and male-male competition may facilitate each other in R. pedestris. This is consistent with current basic concepts of sexual selection.

    DOI: 10.1371/journal.pone.0083278

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  29. Soldier Morphogenesis in the Damp-Wood Termite Is Regulated by the Insulin Signaling Pathway 査読有り 国際誌

    Akiko Hattori, Yasuhiro Sugime, Chifune Sasa, Hitoshi Miyakawa, Yuki Ishikawa, Satoshi Miyazaki, Yasukazu Okada, Richard Cornette, Laura Corley Lavine, Douglas J. Emlen, Shigeyuki Koshikawa, Toru Miura

    JOURNAL OF EXPERIMENTAL ZOOLOGY PART B-MOLECULAR AND DEVELOPMENTAL EVOLUTION   320B 巻 ( 5 ) 頁: 295 - 306   2013年7月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:WILEY  

    Eusocial insects exhibit various morphological castes associated with the division of labor within a colony. Termite soldiers possess defensive traits including mandibles that are greatly exaggerated and enlarged, as compared to termite reproductives and workers. The enlarged mandibles of soldiers are known to result from dynamic morphogenesis during soldier differentiation that can be induced by juvenile hormone and its analogs. However, the detailed developmental mechanisms still remain unresolved. Because the insulin/insulin-like growth factor signaling (IIS) pathway has been shown to regulate the relative sizes of organs (i.e., allometry) in other insects, we examined the expression profiles of major IIS factors in the damp-wood termite Hodotermopsis sjostedti, during soldier differentiation. The relative expression patterns of orthologs for termite InR (HsjInR), PKB/Akt (HsjPKB/Akt), and FOXO (HsjFOXO) suggest that HsjInR and HsjPKB/Akt were up-regulated in the period of elongation of mandibles during soldier development. In situ hybridization showed that HsjInR was strongly expressed in the mandibular epithelial tissues, and RNA interference (RNAi) for HsjInR disrupted soldier-specific morphogenesis including mandibular elongation. These results suggest that signaling through the IIS pathway is required for soldier-specific morphogenesis. In addition, up-regulation of the IIS pathway in other body tissues occurred at earlier stages of development, indicating that there is tissue-specific IIS regulation. Because the IIS pathway is generally thought to act upstream of JH in insects, our results suggest the damp-wood termite may have evolved a novel feedback loop between JH and IIS that enables social interactions, rather than nutrition, to regulate caste determination. J. Exp. Zool. (Mol. Dev. Evol.) 320B:295-306, 2013. (c) 2013 Wiley Periodicals, Inc.

    DOI: 10.1002/jez.b.22501

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  30. Impacts of diet quality on life-history and reproductive traits in male and female armed beetle, Gnatocerus cornutus 査読有り

    Masako Katsuki, Yasukazu Okada, Kensuke Okada

    ECOLOGICAL ENTOMOLOGY   37 巻 ( 6 ) 頁: 463 - 470   2012年12月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:WILEY  

    1. The energy available for reproduction is usually limited by resource acquisition (i.e. condition). Because condition is known to be strongly affected by environmental factors, reproductive investments also vary across heterogeneous environments. 2. Although the condition dependence of reproductive investment is common to both sexes, reproductive traits may exhibit sexually different responses to environmental fluctuation due to sex-specific life-history strategies. However, few direct experimental studies have investigated the condition dependence of reproductive investments in both sexes. 3. We investigated the condition dependence of life-history and reproductive traits of males and females in the beetle Gnatocerus cornutus Fabricus by manipulating larval and adult diet quality. We found that male and female life-history traits exhibited similar responses to environmental fluctuations. 4. By contrast, the sexes exhibit different patterns of condition dependence in reproductive traits (i.e. the adult nutritional environment has a strong impact on the female lifetime reproductive success, whereas larval nutritional environment strongly affects the secondary sexual trait in males). 5. This difference in the plasticity of reproductive traits may lead to different selection pressures for each sex, even if both sexes develop and/or live in the same environment.

    DOI: 10.1111/j.1365-2311.2012.01390.x

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  31. DEFICIENCY SCREENING FOR GENOMIC REGIONS WITH EFFECTS ON ENVIRONMENTAL SENSITIVITY OF THE SENSORY BRISTLES OF DROSOPHILA MELANOGASTER 査読有り 国際誌

    Kazuo H. Takahashi, Yasukazu Okada, Kouhei Teramura

    EVOLUTION   66 巻 ( 9 ) 頁: 2878 - 2890   2012年9月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:WILEY  

    Environmental canalization is defined as a reduction in the effect of external environmental perturbations on a phenotype, while phenotypic plasticity is defined as the production of different phenotypes in alternative environments. These terms describe different aspects of the same phenomenon, that is, the sensitivity of the phenotype to the environment. Genetic regulation of the environmental sensitivity has been a central topic in the field of evolutionary biology. In this study, we performed deficiency screening to detect genomic regions with effects on the environmental sensitivity of Drosophila melanogaster sensory bristles. We used a collection of isogenic deficiency strains established by the DrosDel Project for screening. We screened 423 genomic deficiencies that encompassed approximately 63.6% of the entire D. melanogaster genome. We identified 29 genomic deficiencies showing significant effects on environmental sensitivity, suggesting that multiple genomic regions may influence phenotypic variation. We also found significant correlations among the effects of deficiencies on environmental sensitivity for different bristle traits, suggesting that the same genetic mechanism can regulate environmental sensitivity of multiple traits. Current high-resolution mapping will facilitate the examination of individual candidate genes using mutations or RNAi approaches in future studies.

    DOI: 10.1111/j.1558-5646.2012.01636.x

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  32. Juvenile hormone mediates developmental integration between exaggerated traits and supportive traits in the horned flour beetle Gnatocerus cornutus 査読有り 国際誌

    Yasukazu Okada, Hiroki Gotoh, Toru Miura, Takahisa Miyatake, Kensuke Okada

    EVOLUTION & DEVELOPMENT   14 巻 ( 4 ) 頁: 363 - 371   2012年7月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:WILEY  

    Sexually selected exaggerated traits are often coupled with modifications in other nontarget traits. In insects with weapons, enlargements of nontarget characters that functionally support the weapon often occur (i.e. supportive traits). The support of sexual traits requires developmental coordination among functionally related multiple traitsan explicit example of morphological integration. The genetic theory predicts that developmental integration among different body modules, for which development is regulated via different sets of genes, is likely to be coordinated by pleiotropic factors. However, the developmental backgrounds of morphological integrations are largely unknown. We tested the hypothesis that the juvenile hormone (JH), as a pleiotropic factor, mediates the integration between exaggerated and supportive traits in an armed beetle Gnatocerus cornutus. During combat, males of this beetle use exaggerated mandibles to lift up their opponents with the supportive traits, that is, the head and prothoracic body parts. Application of methoprene, a JH analog (JHA), during the larval to prepupal period, induced the formation of large mandibles relative to the body sizes in males. Morphometric examination of nontarget traits elucidated an increase in the relative sizes of supportive traits, including the head and prothoracic body parts. In addition, reductions in the hind wing area and elytra length, which correspond to flight and reproductive abilities, were detected. Our findings are consistent with the genetic theory and support the idea that JH is a key pleiotropic factor that coordinates the developmental integration of exaggerated traits and supportive characters, as well as resource allocation trade-offs.

    DOI: 10.1111/j.1525-142X.2012.00554.x

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  33. Effect of weapon-supportive traits on fighting success in armed insects 査読有り

    Yasukazu Okada, Yu Suzaki, Takahisa Miyatake, Kensuke Okada

    ANIMAL BEHAVIOUR   83 巻 ( 4 ) 頁: 1001 - 1006   2012年4月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:ACADEMIC PRESS LTD- ELSEVIER SCIENCE LTD  

    Male fighting frequently results in the evolution of traits used as weapons. These are often coupled with correlated modifications in other somatic traits (hereafter referred to as supportive traits), which are thought to support the weapon functionally. No previous studies have investigated whether supportive traits themselves affect fighting success. We evaluated this possibility in two armed insects, the beetle Gnatocerus cornutus and the bug Riptortus pedestris. Using a principal components analysis, we identified a subset of supportive traits that were associated with weapons in both species. The patterns of supportive structures differed between the two species, probably reflecting differences in the use of weapons during fights. In both species, fighting success was higher in males with enhanced supportive traits. It appears that weapon-supportive structures develop as the result of selection that favours coordination among multiple traits associated with fighting behaviour. Thus, our results provide rare evidence of the benefit of a supportive trait that is a clear example of phenotypic integration. (C) 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

    DOI: 10.1016/j.anbehav.2012.01.021

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  34. Screening of Upregulated Genes Induced by High Density in the Vetch Aphid Megoura crassicauda 査読有り

    Asano Ishikawa, Yuki Ishikawa, Yasukazu Okada, Satoshi Miyazaki, Hitoshi Miyakawa, Shigeyuki Koshikawa, Jennifer A. Brisson, Toru Miura

    JOURNAL OF EXPERIMENTAL ZOOLOGY PART A-ECOLOGICAL AND INTEGRATIVE PHYSIOLOGY   317A 巻 ( 3 ) 頁: 194 - 203   2012年3月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:WILEY  

    Aphids exhibit several polyphenisms in which discontinuous, alternative phenotypes are produced depending on environmental conditions. One representative example is the wing polyphenism, where winged and wingless females are produced through parthenogenesis. Previous work has shown that, in some aphid species, the density condition sensed by the mother aphid determines the developmental fate of embryos in her ovary, with high densities leading to winged progeny and low densities to wingless progeny. However, little is known about the molecular and physiological mechanisms underlying the wing polyphenism. To identify genes involved in the wing-morph determination in the vetch aphid, Megoura crassicauda, we compared maternal and embryonic transcripts between high- and low-density conditions using differential display, followed by quantitative real-time PCR (qRT-PCR). Under the high-density condition, two genes (Uba1 and Naca) were found to be upregulated in maternal tissues without ovaries, while one gene (ClpP) was upregulated in ovaries containing embryos. Uba1 and Naca encode factors that function in protein modification or transcriptional/translational regulation, respectively. In addition to differential display, candidate gene approaches focusing on morphogenetic and endocrine genes, i.e., wg, dpp, ap, hh, InR, IRS, Foxo, EcR, and USP, were also carried out. We found that wg was upregulated in maternal tissues under the high-density condition. The identified genes from both approaches are candidates for further study of their involvement in the transduction of density signals in mother aphids and/or the initial process of wing differentiation in embryos. J. Exp. Zool. 317:194203, 2012. (c) 2012 Wiley Periodicals, Inc.

    DOI: 10.1002/jez.1713

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  35. DEFICIENCY MAPPING OF THE GENOMIC REGIONS ASSOCIATED WITH EFFECTS ON DEVELOPMENTAL STABILITY IN DROSOPHILA MELANOGASTER 査読有り 国際誌

    Kazuo H. Takahashi, Yasukazu Okada, Kouhei Teramura, Masahiro Tsujino

    EVOLUTION   65 巻 ( 12 ) 頁: 3565 - 3577   2011年12月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:WILEY  

    Developmental stability is the tendency of morphological traits to resist the effects of developmental noise, and is commonly evaluated by examining fluctuating asymmetry (FA)random deviations from perfect bilateral symmetry. Molecular mechanisms that control FA have been a long-standing topic of debate in the field of evolutionary biology and quantitative genetics. In this study, we mapped genomic regions associated with effects on the mean and FA of morphological traits, and characterized the trait specificity of those regions. A collection of isogenic deficiency strains established by the DrosDel project was used for deficiency mapping of genome regions associated with effects on FA. We screened 435 genome deficiencies or approximately 64.9% of the entire genome of Drosophila melanogaster to map the region that demonstrated a significant effect on FA of morphological traits. We found that 406 deficiencies significantly affected the mean of morphological traits, and 92 deficiencies increased FA. These results suggest that several genomic regions have the potential to affect developmental stability. They also suggest the possibility of the existence of trait-specific and trait-nonspecific mechanisms for stabilizing developmental processes. The new findings in this study could provide insight into the understanding of the genetic architecture underlying developmental stability.

    DOI: 10.1111/j.1558-5646.2011.01400.x

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  36. Male Aggressive Behavior and Exaggerated Hindlegs of the Bean Bug Riptortus pedestris 査読有り

    Kensuke Okada, Yu Suzaki, Yasukazu Okada, Takahisa Miyatake

    ZOOLOGICAL SCIENCE   28 巻 ( 9 ) 頁: 659 - 663   2011年9月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:ZOOLOGICAL SOC JAPAN  

    Males of the bean bug species Riptortus pedestris possess larger hindlegs than females. Observations of male-male interactions showed that the enlarged hindlegs are used as weapons in male fights, and that males with larger hindlegs win fights more frequently. Morphological analysis based on the positive allometry test showed that the femora of larger males are relatively bigger than those of smaller males, but femora of larger females are not relatively larger than those of smaller females. These results suggest that sexual selection in R. pedestris favors larger hindlegs for male fighting. In addition, the thorax and abdomen lengths were larger in the male than in the female. The males often lift their abdomen with their back to the opponent for displays against an opponent. As a result, abdominal size may be under stronger selection in the male than in the female, as for the exaggerated hindlegs.

    DOI: 10.2108/zsj.28.659

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  37. Genome-Wide Deficiency Mapping of the Regions Responsible for Temporal Canalization of the Developmental Processes of Drosophila melanogaster 査読有り

    Kazuo H. Takahashi, Yasukazu Okada, Kouhei Teramura

    JOURNAL OF HEREDITY   102 巻 ( 4 ) 頁: 448 - 457   2011年7月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:OXFORD UNIV PRESS INC  

    Developmental processes of organisms are programed to proceed in a finely regulated manner and finish within a certain period of time depending on the ambient environmental conditions. Therefore, variation in the developmental period under controlled genetic and environmental conditions indicates innate instability of the developmental process. In this study, we aimed to determine whether a molecular machinery exists that regulates the canalization of the developmental period and, if so, to test whether the same mechanism also stabilizes a morphological trait. To search for regions that influence the instability of the developmental period, we conducted genome-wide deficiency mapping with 441 isogenic deficiency strains covering 65.5% of the Drosophila melanogaster genome. We found that 11 independent deficiencies significantly increased the instability of the developmental period and 5 of these also significantly increased the fluctuating asymmetry of wing shape although there was no significant correlation between the instabilities of developmental period and wing shape in general. These results suggest that canalization processes of the developmental period and morphological traits are at least partially independent. Our findings emphasize the potential importance of temporal variation in development as an indicator of developmental stability and canalization and provide a novel perspective for understanding the regulation of phenotypic variability.

    DOI: 10.1093/jhered/esr026

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  38. Genome-wide deficiency screen for the genomic regions responsible for heat resistance in Drosophila melanogaster 査読有り 国際誌

    Kazuo H. Takahashi, Yasukazu Okada, Kouhei Teramura

    BMC GENETICS   12 巻   頁: 57 - 57   2011年6月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:BIOMED CENTRAL LTD  

    Background: Temperature adaptation is one of the most important determinants of distribution and population size of organisms in nature. Recently, quantitative trait loci (QTL) mapping and gene expression profiling approaches have been used for detecting candidate genes for heat resistance. However, the resolution of QTL mapping is not high enough to examine the individual effects of various genes in each QTL. Heat stress-responsive genes, characterized by gene expression profiling studies, are not necessarily responsible for heat resistance. Some of these genes may be regulated in association with the heat stress response of other genes.Results: To evaluate which heat-responsive genes are potential candidates for heat resistance with higher resolution than previous QTL mapping studies, we performed genome-wide deficiency screen for QTL for heat resistance. We screened 439 isogenic deficiency strains from the DrosDel project, covering 65.6% of the Drosophila melanogaster genome in order to map QTL for thermal resistance. As a result, we found 19 QTL for heat resistance, including 3 novel QTL outside the QTL found in previous studies.Conclusion: The QTL found in this study encompassed 19 heat-responsive genes found in the previous gene expression profiling studies, suggesting that they were strong candidates for heat resistance. This result provides new insights into the genetic architecture of heat resistance. It also emphasizes the advantages of genome-wide deficiency screen using isogenic deficiency libraries.

    DOI: 10.1186/1471-2156-12-57

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  39. Juvenile Hormone Regulates Extreme Mandible Growth in Male Stag Beetles 査読有り 国際誌

    Hiroki Gotoh, Richard Cornette, Shigeyuki Koshikawa, Yasukazu Okada, Laura Corley Lavine, Douglas J. Emlen, Toru Miura

    PLOS ONE   6 巻 ( 6 ) 頁: e21139   2011年6月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:PUBLIC LIBRARY SCIENCE  

    The morphological diversity of insects is one of the most striking phenomena in biology. Evolutionary modifications to the relative sizes of body parts, including the evolution of traits with exaggerated proportions, are responsible for a vast range of body forms. Remarkable examples of an insect trait with exaggerated proportions are the mandibular weapons of stag beetles. Male stag beetles possess extremely enlarged mandibles which they use in combat with rival males over females. As with other sexually selected traits, stag beetle mandibles vary widely in size among males, and this variable growth results from differential larval nutrition. However, the mechanisms responsible for coupling nutrition with growth of stag beetle mandibles (or indeed any insect structure) remain largely unknown. Here, we demonstrate that during the development of male stag beetles (Cyclommatus metallifer), juvenile hormone (JH) titers are correlated with the extreme growth of an exaggerated weapon of sexual selection. We then investigate the putative role of JH in the development of the nutritionally-dependent, phenotypically plastic mandibles, by increasing hemolymph titers of JH with application of the JH analog fenoxycarb during larval and prepupal developmental periods. Increased JH signaling during the early prepupal period increased the proportional size of body parts, and this was especially pronounced in male mandibles, enhancing the exaggerated size of this trait. The direction of this response is consistent with the measured JH titers during this same period. Combined, our results support a role for JH in the nutrition-dependent regulation of extreme mandible growth in this species. In addition, they illuminate mechanisms underlying the evolution of trait proportion, the most salient feature of the evolutionary diversification of the insects.

    DOI: 10.1371/journal.pone.0021139

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  40. Deficiency mapping of genome regions responsible for developmental stability 査読有り

    Kazuo Takahashi, Yasukazu Okada, Kouhei Teramura

    GENES & GENETIC SYSTEMS   85 巻 ( 6 ) 頁: 430 - 430   2010年12月

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    記述言語:英語   出版者・発行元:GENETICS SOC JAPAN  

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  41. Identification of a reproductive-specific, putative lipid transport protein gene in a queenless ponerine ant Diacamma sp. 査読有り 国際誌

    Yasukazu Okada, Satoshi Miyazaki, Shigeyuki Koshikawa, Richard Cornette, Kiyoto Maekawa, Kazuki Tsuji, Toru Miura

    NATURWISSENSCHAFTEN   97 巻 ( 11 ) 頁: 971 - 979   2010年11月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:SPRINGER  

    Of the various characteristics of social insects, communication for reproductive differentiation is one of the most important and basic social interactions among colony members. To elucidate the molecular basis underlying this process, genes responsible for reproductive differentiation in Diacamma were screened using fluorescent differential display. Differential display, together with real-time quantitative reverse transcriptase-polymerase chain reaction (qRT-PCR), revealed that a gene belonging to the family of cellular retinaldehyde-binding proteins was specifically expressed in the epidermis of the head, legs, and thorax in reproductives. The deduced protein sequence in the coding region, obtained by rapid amplification of cDNA ends (RACE)-PCR, was found to include cellular retinaldehyde-binding domain (CRAL-TRIO domain), suggesting that DiaCRALDCP functions in transportation of lipids, such as cuticular hydrocarbons. DiaCRALDCP transcript levels immediately decreased 1 day after the gemma mutilation, suggesting that DiaCRALDCP is involved in the physiological changes provoked by the behavioral regulation. Considering these results, the social functions of DiaCRALDCP in Diacamma are discussed.

    DOI: 10.1007/s00114-010-0713-8

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  42. Gene expression changes during caste-specific neuronal development in the damp-wood termite Hodotermopsis sjostedti 査読有り 国際誌

    Yuki Ishikawa, Yasukazu Okada, Asano Ishikawa, Hitoshi Miyakawa, Shigeyuki Koshikawa, Toru Miura

    BMC GENOMICS   11 巻   頁: 314 - 314   2010年5月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:BMC  

    Background: One of the key characters of social insects is the division of labor, in which different tasks are allocated to various castes. In termites, one of the representative groups of social insects, morphological differences as well as behavioral differences can be recognized among castes. However, very little is known about the neuronal and molecular bases of caste differentiation and caste-specific behavior. In almost all termite species, soldiers play defensive roles in their colonies, and their morphology and behavior are largely different from workers (or pseudergates). Therefore, we predicted that some genes linked to defensive behavior and/or those required for neuronal changes are differentially expressed between workers and soldiers, or during the soldier differentiation, respectively.Results: Using the brain and suboesophageal ganglion (SOG) of the damp-wood termite Hodotermopsis sjostedti, we first screened genes specifically expressed in soldiers or during soldier differentiation by the differential display method, followed by quantitative real-time polymerase chain reaction. No distinctive differences in expression patterns were detected between pseudergates and soldiers. In the course of soldier differentiation, however, five genes were found to be up-regulated in brain and/or SOG: 14-3-3epsilon, fibrillin2, beta-tubulin, ciboulot, and a hypothetical protein containing a SAP motif. Some of these genes are thought to be associated with cytoskeletal structure or motor-associated proteins in neuronal tissues.Conclusion: The identified five genes could be involved in soldier-specific neuronal modifications, resulting in defensive behaviors in termite soldiers. The temporal expression patterns of these genes were consistent with the neuronal changes during soldier differentiation, suggesting that molecular machineries, in which the identified factors would participate, play important roles in behavioral differentiation of termite soldiers.

    DOI: 10.1186/1471-2164-11-314

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  43. Gene up-regulation in response to predator kairomones in the water flea, Daphnia pulex 査読有り

    Hitoshi Miyakawa, Maki Imai, Naoki Sugimoto, Yuki Ishikawa, Asano Ishikawa, Hidehiko Ishigaki, Yasukazu Okada, Satoshi Miyazaki, Shigeyuki Koshikawa, Richard Cornette, Toru Miura

    BMC DEVELOPMENTAL BIOLOGY   10 巻   頁: 45   2010年4月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:BMC  

    Background: Numerous cases of predator-induced polyphenisms, in which alternate phenotypes are produced in response to extrinsic stimuli, have been reported in aquatic taxa to date. The genus Daphnia (Branchiopoda, Cladocera) provides a model experimental system for the study of the developmental mechanisms and evolutionary processes associated with predator-induced polyphenisms. In D. pulex, juveniles form neckteeth in response to predatory kairomones released by Chaoborus larvae (Insecta, Diptera).Results: Previous studies suggest that the timing of the sensitivity to kairomones in D. pulex can generally be divided into the embryonic and postembryonic developmental periods. We therefore examined which of the genes in the embryonic and first-instar juvenile stages exhibit different expression levels in the presence or absence of predator kairomones. Employing a candidate gene approach and identifying differentially-expressed genes revealed that the morphogenetic factors, Hox3, extradenticle and escargot, were up-regulated by kairomones in the postembryonic stage and may potentially be responsible for defense morph formation. In addition, the juvenile hormone pathway genes, JHAMT and Met, and the insulin signaling pathway genes, InR and IRS-1, were up-regulated in the first-instar stage. It is well known that these hormonal pathways are involved in physiological regulation following morphogenesis in many insect species. During the embryonic stage when morphotypes were determined, one of the novel genes identified by differential display was up-regulated, suggesting that this gene may be related to morphotype determination. Biological functions of the up-regulated genes are discussed in the context of defense morph formation.Conclusions: It is suggested that, following the reception of kairomone signals, the identified genes are involved in a series of defensive phenotypic alterations and the production of a defensive phenotype.

    DOI: 10.1186/1471-213X-10-45

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  44. Morph-dependent form of asymmetry in mandibles of the stag beetle Prosopocoilus inclinatus (Coleoptera : Lucanidae) 査読有り

    Yasukazu Okada, Hiroaki Fujisawa, Yousuke Kimura, Eisuke Hasegawa

    ECOLOGICAL ENTOMOLOGY   33 巻 ( 5 ) 頁: 684 - 689   2008年10月

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:WILEY  

    1. The form of asymmetry in bilateral organs usually follows the same pattern within single populations. However, some exceptions may occur when a population consists of different phenotypes that are from different ontogenic backgrounds and under different selective pressures. We investigated the asymmetric patterns of mandibles of larvae, females, and males in the stag beetle Prosopocoilus inclinatus.2. Larval mandibles exhibited directional asymmetry both in length and cross direction, whereas female mandibles showed directional asymmetry in cross direction. These asymmetric structures might be more effective in cutting wood fibres.3. For the relation of male mandible length to body size, a model with a switch point showed a better fit to the data than a convex curve model. This shows that the males are dimorphic with two distinct morphs.4. The form of asymmetry in male mandible length differed between the morphs. The smaller males exhibited left-biased directional asymmetry in common with larvae, whereas the larger males exhibited fluctuating asymmetry.5. This is a novel finding of a morph-dependent asymmetry. The morph-dependent asymmetry in males may be as a result of different selection on each morph or a developmental constraint from larval mandibles to adult ones.

    DOI: 10.1111/j.1365-2311.2008.01023.x

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  45. Morphological differences between sexes in the ponerine ant Diacamma sp (Formicidae : Ponerinae) 査読有り

    Yasukazu Okada, Kazuki Tsuji, Toru Miura

    SOCIOBIOLOGY   48 巻 ( 2 ) 頁: 527 - 541   2006年

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    記述言語:英語   掲載種別:研究論文(学術雑誌)   出版者・発行元:UNIV ESTADUAL FEIRA SANTANA  

    We report herein detailed morphological differences between sexes in the ponerine ant Diacamma sp. The female individuals of this species show monomorphism, making them particularly suitable among the social hymenopterans for comparing adult sexual traits and developmental processes. Our observations revealed some intriguing sex-specific characteristics. For example, antennal sensilla are gender-spccialized in these ants; males possess sensilla cocloconica, thought to respond to air conditions, while females possess a particular type of sensilla basiconica that is a putative contact chemoreceptor. The antennal cleaners in the foretibiae of the legs are also sex-specific, in addition to the trichome patterns on the spurs in the mid- and hind tibiae. Furthermore, only male tarsal claws have a denticle inside the claw, and the male posterior abdomen has a hook-like curved spine at the edge of the eighth tergite. This spine is thought to facilitate the tight connection of a mating pair. Based on these findings, we hypothesized that most of the sexually dimorphic traits are morphologically specialized for and thus function in the different gender life strategies, such as flight ability, lifespan, and male suicidal copulation.

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