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Francis L. W. Ratnieks - One of the best experts on this subject based on the ideXlab platform.
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a morphologically specialized soldier caste improves Colony Defense in a neotropical eusocial bee
Proceedings of the National Academy of Sciences of the United States of America, 2012Co-Authors: Christoph Grüter, Cristiano Menezes, Vera Lucia Imperatrizfonseca, Francis L. W. RatnieksAbstract:Division of labor among workers is common in insect societies and is thought to be important in their ecological success. In most species, division of labor is based on age (temporal castes), but workers in some ants and termites show morphological specialization for particular tasks (physical castes). Large-headed soldier ants and termites are well-known examples of this specialization. However, until now there has been no equivalent example of physical worker subcastes in social bees or wasps. Here we provide evidence for a physical soldier subcaste in a bee. In the neotropical stingless bee Tetragonisca angustula, nest Defense is performed by two groups of guards, one hovering near the nest entrance and the other standing on the wax entrance tube. We show that both types of guards are 30% heavier than foragers and of different shape; foragers have relatively larger heads, whereas guards have larger legs. Low variation within each subcaste results in negligible size overlap between guards and foragers, further indicating that they are distinct physical castes. In addition, workers that remove garbage from the nest are of intermediate size, suggesting that they might represent another unrecognized caste. Guards or soldiers are reared in low but sufficient numbers (1–2% of emerging workers), considering that <1% usually perform this task. When challenged by the obligate robber bee Lestrimelitta limao, an important natural enemy, larger workers were able to fight for longer before being defeated by the much larger robber. This discovery opens up opportunities for the comparative study of physical castes in social insects, including the question of why soldiers appear to be so much rarer in bees than in ants or termites.
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A morphologically specialized soldier caste improves Colony Defense in a neotropical eusocial bee
Proceedings of the National Academy of Sciences of the United States of America, 2012Co-Authors: Christoph Grüter, Cristiano Menezes, Vera Lúcia Imperatriz-fonseca, Francis L. W. RatnieksAbstract:Division of labor among workers is common in insect societies and is thought to be important in their ecological success. In most species, division of labor is based on age (temporal castes), but workers in some ants and termites show morphological specialization for particular tasks (physical castes). Large-headed soldier ants and termites are well-known examples of this specialization. However, until now there has been no equivalent example of physical worker subcastes in social bees or wasps. Here we provide evidence for a physical soldier subcaste in a bee. In the neotropical stingless bee Tetragonisca angustula, nest Defense is performed by two groups of guards, one hovering near the nest entrance and the other standing on the wax entrance tube. We show that both types of guards are 30% heavier than foragers and of different shape; foragers have relatively larger heads, whereas guards have larger legs. Low variation within each subcaste results in negligible size overlap between guards and foragers, further indicating that they are distinct physical castes. In addition, workers that remove garbage from the nest are of intermediate size, suggesting that they might represent another unrecognized caste. Guards or soldiers are reared in low but sufficient numbers (1–2% of emerging workers), considering that
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Preemptive Defensive Self‐Sacrifice by Ant Workers
The American Naturalist, 2008Co-Authors: Adam Tofilski, Margaret J Couvillon, Sophie E F Evison, Heikki Helanterä, Elva J H Robinson, Francis L. W. RatnieksAbstract:Worker insects altruistically sacrifice their own reproduction to rear nondescendant kin. This sacrifice reaches its most spectacular level in suicidal Colony Defense. Suicidal Defense, such as when the sting of a honeybee worker embeds in a predator and then breaks off, is normally a facultative response. Here we describe the first example of preemptive self-sacrifice in nest Defense. In the Brazilian ant Forelius pusillus, the nest entrance is closed at sunset. One to eight workers finish the job from the outside and, in doing so, sacrifice their lives.
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Preemptive defensive self-sacrifice by ant workers.
The American naturalist, 2008Co-Authors: Adam Tofilski, Margaret J Couvillon, Sophie E F Evison, Heikki Helanterä, Elva J H Robinson, Francis L. W. RatnieksAbstract:Worker insects altruistically sacrifice their own reproduction to rear nondescendant kin. This sacrifice reaches its most spectacular level in suicidal Colony Defense. Suicidal Defense, such as when the sting of a honeybee worker embeds in a predator and then breaks off, is normally a facultative response. Here we describe the first example of preemptive self-sacrifice in nest Defense. In the Brazilian ant Forelius pusillus, the nest entrance is closed at sunset. One to eight workers finish the job from the outside and, in doing so, sacrifice their lives.
Takema Fukatsu - One of the best experts on this subject based on the ideXlab platform.
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Temporal division of labor in an aphid social system.
Scientific reports, 2021Co-Authors: Harunobu Shibao, Mayako Kutsukake, Takema FukatsuAbstract:Temporal division of labor, or age polyethism, in which altruistic caste individuals change their tasks with aging, is widely found in bees and ants (Hymenoptera) and also in other social insects. Here we report the discovery of elaborate age polyethism in a social aphid (Hemiptera). Tuberaphis styraci is a gall-forming aphid in which monomorphic first instar nymphs differentiate into normal nymphs and soldiers upon second instar molt. Soldiers neither grow nor reproduce but perform gall cleaning and Colony Defense. Using an artificial diet rearing system, we collected age-defined groups of soldiers and monitored their social behaviors. We observed that young soldiers tend to clean whereas old soldiers preferentially attack, thereby verifying age-dependent task switching from housekeeping to Defense. Strategic sampling, age estimation and behavioral observation of soldiers from natural galls revealed that (1) young cleaning soldiers tend to inhabit upper gall regions with adult insects, (2) old attacking soldiers tend to be distributed in lower gall regions, particularly around the gall openings, and (3) the gall structure is linked to intra-nest movement, aging and task switching of soldiers in an adaptive manner. These results highlight an evolutionary parallelism comparable to the sophisticated temporal division of labor observed in honeybee colonies.
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Plant Manipulation by Gall-Forming Social Aphids for Waste Management
Frontiers in Plant Science, 2019Co-Authors: Mayako Kutsukake, Keigo Uematsu, Takema FukatsuAbstract:Many social aphids form spectacular galls on their host plants, in which hundreds to thousands of aphids thrive for several months or even for over a year. Here, in addition to Colony Defense against natural enemies, waste disposal is an important task for the gall dwellers to sustain their social life. In open galls, soldier nymphs actively clean Colony wastes such as honeydew droplets, cast-off skins and cadavers by pushing them with their head out of the gall opening. In the gall, the excreted honeydew is coated with aphid-derived powdery wax to form “honeydew balls”, which prevents the aphids from wetting and drowning with their own excretion. How the aphids deal with the accumulated honeydew in closed galls has been a mystery. Here, we report a novel gall cleaning mechanism: the gall inner surface absorbs and removes the liquid waste through the plant vascular system. Such a plant-mediated water-absorbing property is commonly found in aphids forming closed galls, which must have evolved at least three times independently. By contrast, the inner surface of open galls is wax-coated and water-repellent, and in some cases, the inner surface is covered with dense trichomes, which further enhance the water repellency. In conclusion, gall-forming aphids induce novel plant phenotypes to manage the waste problems by manipulating plant morphogenesis and physiology for their own sake. This review describes our recent studies on waste management strategies by gall-forming social aphids and discuss future directions of this research topic.
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Exaggeration and cooption of innate immunity for social Defense.
Proceedings of the National Academy of Sciences of the United States of America, 2019Co-Authors: Mayako Kutsukake, Naruo Nikoh, Minoru Moriyama, Shuji Shigenobu, Xian-ying Meng, Chiyo Noda, Satoru Kobayashi, Takema FukatsuAbstract:Social insects often exhibit striking altruistic behaviors, of which the most spectacular ones may be self-destructive defensive behaviors called autothysis, “self-explosion,” or “suicidal bombing.” In the social aphid Nipponaphis monzeni, when enemies damage their plant-made nest called the gall, soldier nymphs erupt to discharge a large amount of body fluid, mix the secretion with their legs, and skillfully plaster it over the plant injury. Dozens of soldiers come out, erupt, mix, and plaster, and the gall breach is promptly sealed with the coagulated body fluid. What molecular and cellular mechanisms underlie the self-sacrificing nest repair with body fluid for the insect society? Here we demonstrate that the body cavity of soldier nymphs is full of highly differentiated large hemocytes that contain huge amounts of lipid droplets and phenoloxidase (PO), whereas their hemolymph accumulates huge amounts of tyrosine and a unique repeat-containing protein (RCP). Upon breakage of the gall, soldiers gather around the breach and massively discharge the body fluid. The large hemocytes rupture and release lipid droplets, which promptly form a lipidic clot, and, concurrently, activated PO converts tyrosine to reactive quinones, which cross-link RCP and other macromolecules to physically reinforce the clot to seal the gall breach. Here, soldiers’ humoral and cellular immune mechanisms for wound sealing are extremely up-regulated and utilized for Colony Defense, which provides a striking case of direct evolutionary connection between individual immunity and social immunity and highlights the importance of exaggeration and cooption of preexisting traits to create evolutionary novelties.
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Altruistic Colony Defense by menopausal female insects.
Current biology : CB, 2010Co-Authors: Keigo Uematsu, Mayako Kutsukake, Takema Fukatsu, Masakazu Shimada, Harunobu ShibaoAbstract:Summary Recent studies have suggested that an extended postreproductive life span, such as life after menopause in human females, will evolve when the indirect (kin-selected) fitness benefits from altruistic behavior are greater than the direct fitness benefits from continuing reproduction [1–4]. Under some conditions in which postreproductive altruism is more beneficial and/or continuing reproduction is more costly, the postreproductive life span can be shaped by natural selection [5, 6]. However, indirect fitness benefits during postreproductive survival have been documented mainly in intelligent mammals such as humans and cetaceans, in which elder females possess enhanced social knowledge through learning [7–10]. Here we show that postreproductive females of the gall-forming aphid Quadrartus yoshinomiyai (Nipponaphidini) can gain indirect fitness benefits through their altruistic Colony Defense. These females cease reproduction around the time of gall opening and defend the Colony by sticking themselves to intruding predators with a waxy secretion that is accumulated in their body with aging. Our results suggest that the presence of an age-related trait for altruistic behavior promotes the evolution of postreproductive altruism in this social insect via kin selection under natural selection imposed by predators.
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Venomous protease of aphid soldier for Colony Defense
Proceedings of the National Academy of Sciences of the United States of America, 2004Co-Authors: Mayako Kutsukake, Harunobu Shibao, Naruo Nikoh, Mizue Morioka, Tomohiro Tamura, Tamotsu Hoshino, Satoru Ohgiya, Takema FukatsuAbstract:In social aphids, morphological, behavioral, and physiological differences between soldiers and normal insects are attributed to differences in gene expression between them, because they are clonal offspring parthenogenetically produced by the same mothers. By using cDNA subtraction, we identified a soldier-specific cysteine protease of the family cathepsin B in a social aphid, Tuberaphis styraci, with a second-instar soldier caste. The cathepsin B gene was specifically expressed in soldiers and first-instar nymphs destined to be soldiers. The cathepsin B protein was preferentially produced in soldiers and showed a protease activity typical of cathepsin B. The cathepsin B mRNA and protein were localized in the midgut of soldiers. For Colony Defense, soldiers attack enemies with their stylet, which causes paralysis and death of the victims. Notably, after soldiers attacked moth larvae, the cathepsin B protein was detected from the paralyzed larvae. Injection of purified recombinant cathepsin B protein certainly killed the recipient moth larvae. From these results, we concluded that the cathepsin B protein is a major component of the aphid venom produced by soldiers of T. styraci. Soldier-specific expression of the cathepsin B gene was found in other social aphids of the genus Tuberaphis. The soldier-specific cathepsin B gene showed an accelerated molecular evolution probably caused by the action of positive selection, which had been also known from venomous proteins of other animals.
Mayako Kutsukake - One of the best experts on this subject based on the ideXlab platform.
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Temporal division of labor in an aphid social system.
Scientific reports, 2021Co-Authors: Harunobu Shibao, Mayako Kutsukake, Takema FukatsuAbstract:Temporal division of labor, or age polyethism, in which altruistic caste individuals change their tasks with aging, is widely found in bees and ants (Hymenoptera) and also in other social insects. Here we report the discovery of elaborate age polyethism in a social aphid (Hemiptera). Tuberaphis styraci is a gall-forming aphid in which monomorphic first instar nymphs differentiate into normal nymphs and soldiers upon second instar molt. Soldiers neither grow nor reproduce but perform gall cleaning and Colony Defense. Using an artificial diet rearing system, we collected age-defined groups of soldiers and monitored their social behaviors. We observed that young soldiers tend to clean whereas old soldiers preferentially attack, thereby verifying age-dependent task switching from housekeeping to Defense. Strategic sampling, age estimation and behavioral observation of soldiers from natural galls revealed that (1) young cleaning soldiers tend to inhabit upper gall regions with adult insects, (2) old attacking soldiers tend to be distributed in lower gall regions, particularly around the gall openings, and (3) the gall structure is linked to intra-nest movement, aging and task switching of soldiers in an adaptive manner. These results highlight an evolutionary parallelism comparable to the sophisticated temporal division of labor observed in honeybee colonies.
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Plant Manipulation by Gall-Forming Social Aphids for Waste Management
Frontiers in Plant Science, 2019Co-Authors: Mayako Kutsukake, Keigo Uematsu, Takema FukatsuAbstract:Many social aphids form spectacular galls on their host plants, in which hundreds to thousands of aphids thrive for several months or even for over a year. Here, in addition to Colony Defense against natural enemies, waste disposal is an important task for the gall dwellers to sustain their social life. In open galls, soldier nymphs actively clean Colony wastes such as honeydew droplets, cast-off skins and cadavers by pushing them with their head out of the gall opening. In the gall, the excreted honeydew is coated with aphid-derived powdery wax to form “honeydew balls”, which prevents the aphids from wetting and drowning with their own excretion. How the aphids deal with the accumulated honeydew in closed galls has been a mystery. Here, we report a novel gall cleaning mechanism: the gall inner surface absorbs and removes the liquid waste through the plant vascular system. Such a plant-mediated water-absorbing property is commonly found in aphids forming closed galls, which must have evolved at least three times independently. By contrast, the inner surface of open galls is wax-coated and water-repellent, and in some cases, the inner surface is covered with dense trichomes, which further enhance the water repellency. In conclusion, gall-forming aphids induce novel plant phenotypes to manage the waste problems by manipulating plant morphogenesis and physiology for their own sake. This review describes our recent studies on waste management strategies by gall-forming social aphids and discuss future directions of this research topic.
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Exaggeration and cooption of innate immunity for social Defense.
Proceedings of the National Academy of Sciences of the United States of America, 2019Co-Authors: Mayako Kutsukake, Naruo Nikoh, Minoru Moriyama, Shuji Shigenobu, Xian-ying Meng, Chiyo Noda, Satoru Kobayashi, Takema FukatsuAbstract:Social insects often exhibit striking altruistic behaviors, of which the most spectacular ones may be self-destructive defensive behaviors called autothysis, “self-explosion,” or “suicidal bombing.” In the social aphid Nipponaphis monzeni, when enemies damage their plant-made nest called the gall, soldier nymphs erupt to discharge a large amount of body fluid, mix the secretion with their legs, and skillfully plaster it over the plant injury. Dozens of soldiers come out, erupt, mix, and plaster, and the gall breach is promptly sealed with the coagulated body fluid. What molecular and cellular mechanisms underlie the self-sacrificing nest repair with body fluid for the insect society? Here we demonstrate that the body cavity of soldier nymphs is full of highly differentiated large hemocytes that contain huge amounts of lipid droplets and phenoloxidase (PO), whereas their hemolymph accumulates huge amounts of tyrosine and a unique repeat-containing protein (RCP). Upon breakage of the gall, soldiers gather around the breach and massively discharge the body fluid. The large hemocytes rupture and release lipid droplets, which promptly form a lipidic clot, and, concurrently, activated PO converts tyrosine to reactive quinones, which cross-link RCP and other macromolecules to physically reinforce the clot to seal the gall breach. Here, soldiers’ humoral and cellular immune mechanisms for wound sealing are extremely up-regulated and utilized for Colony Defense, which provides a striking case of direct evolutionary connection between individual immunity and social immunity and highlights the importance of exaggeration and cooption of preexisting traits to create evolutionary novelties.
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Altruistic Colony Defense by menopausal female insects.
Current biology : CB, 2010Co-Authors: Keigo Uematsu, Mayako Kutsukake, Takema Fukatsu, Masakazu Shimada, Harunobu ShibaoAbstract:Summary Recent studies have suggested that an extended postreproductive life span, such as life after menopause in human females, will evolve when the indirect (kin-selected) fitness benefits from altruistic behavior are greater than the direct fitness benefits from continuing reproduction [1–4]. Under some conditions in which postreproductive altruism is more beneficial and/or continuing reproduction is more costly, the postreproductive life span can be shaped by natural selection [5, 6]. However, indirect fitness benefits during postreproductive survival have been documented mainly in intelligent mammals such as humans and cetaceans, in which elder females possess enhanced social knowledge through learning [7–10]. Here we show that postreproductive females of the gall-forming aphid Quadrartus yoshinomiyai (Nipponaphidini) can gain indirect fitness benefits through their altruistic Colony Defense. These females cease reproduction around the time of gall opening and defend the Colony by sticking themselves to intruding predators with a waxy secretion that is accumulated in their body with aging. Our results suggest that the presence of an age-related trait for altruistic behavior promotes the evolution of postreproductive altruism in this social insect via kin selection under natural selection imposed by predators.
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Venomous protease of aphid soldier for Colony Defense
Proceedings of the National Academy of Sciences of the United States of America, 2004Co-Authors: Mayako Kutsukake, Harunobu Shibao, Naruo Nikoh, Mizue Morioka, Tomohiro Tamura, Tamotsu Hoshino, Satoru Ohgiya, Takema FukatsuAbstract:In social aphids, morphological, behavioral, and physiological differences between soldiers and normal insects are attributed to differences in gene expression between them, because they are clonal offspring parthenogenetically produced by the same mothers. By using cDNA subtraction, we identified a soldier-specific cysteine protease of the family cathepsin B in a social aphid, Tuberaphis styraci, with a second-instar soldier caste. The cathepsin B gene was specifically expressed in soldiers and first-instar nymphs destined to be soldiers. The cathepsin B protein was preferentially produced in soldiers and showed a protease activity typical of cathepsin B. The cathepsin B mRNA and protein were localized in the midgut of soldiers. For Colony Defense, soldiers attack enemies with their stylet, which causes paralysis and death of the victims. Notably, after soldiers attacked moth larvae, the cathepsin B protein was detected from the paralyzed larvae. Injection of purified recombinant cathepsin B protein certainly killed the recipient moth larvae. From these results, we concluded that the cathepsin B protein is a major component of the aphid venom produced by soldiers of T. styraci. Soldier-specific expression of the cathepsin B gene was found in other social aphids of the genus Tuberaphis. The soldier-specific cathepsin B gene showed an accelerated molecular evolution probably caused by the action of positive selection, which had been also known from venomous proteins of other animals.
Michael D. Breed - One of the best experts on this subject based on the ideXlab platform.
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Chapter 3 – Behavioral Genetics
Animal Behavior, 2012Co-Authors: Michael D. BreedAbstract:Publisher Summary Behavioral genetics forms a critical component of nearly all behavioral studies. Understanding genetics establishes a thread that runs from the ultimate evolutionary causes of behavior to the behavior's proximate underpinnings and knowing the genetic underpinnings of behavior is essential to understanding how behavior evolves. To understand the evolutionary roots of behavior (ultimate causes), behavioral geneticists often employ phylogeny. Genetics brings a broad range of tools to behavioral investigations. These tools are used to establish the phylogeny of animal groups, which can then be used to understand patterns of evolution for specific behaviors, such as nest construction by birds or Colony Defense by bees. Peeling away the layers of genetic and physiological regulation of a behavior using behavioral genetics—starting with differences among species and moving down to the regulation of gene expression—holds great promise for solving many of the mysteries of animal behavior. Single-gene effects on behavior are easily documented, but single-gene effects are relatively rare and may produce the erroneous notion that complex behavior is “controlled” by those genes. In fact, behavior is most often the result of a large number of genes acting together in a regulatory system. Quantitative genetics can be used to provide better explanations than single-gene models for most animal behavior traits. Studying heritability helps to unravel genetic and environmental influences on behavior. Molecular approaches to behavior genetics provide useful techniques in exploring the regulation of behavior.
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DEFENSIVE BEHAVIOR OF HONEY BEES: Organization, Genetics, and Comparisons with Other Bees
Annual review of entomology, 2004Co-Authors: Michael D. Breed, Ernesto Guzman-novoa, Greg J. HuntAbstract:One key advantage of eusociality is shared Defense of the nest, brood, and stored food; nest Defense plays an important role in the biology of eusocial bees. Recent studies on honey bees, Apis mellifera, have focused on the placement of defensive activity in the overall scheme of division of labor, showing that guard bees play a unique and important role in Colony Defense. Alarm pheromones function in integrating defensive responses; honey bee alarm pheromone is an excellent example of a multicomponent pheromonal blend. The genetic regulation of defensive behavior is now better understood from the mapping of quantitative trait loci (QTLs) associated with variation in defensiveness. Colony Defense in other eusocial bees is less well understood, but enough information is available to provide interesting comparisons between A. mellifera and other species of Apis, as well as with allodapine, halictine, bombine, and meliponine bees. These comparative studies illustrate the wide variety of evolutionary solutions to problems in Colony Defense in the Apoidea.
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defensive behavior of honey bees organization genetics and comparisons with other bees
Annual Review of Entomology, 2004Co-Authors: Michael D. Breed, Ernesto GuzmannovoaAbstract:▪ Abstract One key advantage of eusociality is shared Defense of the nest, brood, and stored food; nest Defense plays an important role in the biology of eusocial bees. Recent studies on honey bees, Apis mellifera, have focused on the placement of defensive activity in the overall scheme of division of labor, showing that guard bees play a unique and important role in Colony Defense. Alarm pheromones function in integrating defensive responses; honey bee alarm pheromone is an excellent example of a multicomponent pheromonal blend. The genetic regulation of defensive behavior is now better understood from the mapping of quantitative trait loci (QTLs) associated with variation in defensiveness. Colony Defense in other eusocial bees is less well understood, but enough information is available to provide interesting comparisons between A. mellifera and other species of Apis, as well as with allodapine, halictine, bombine, and meliponine bees. These comparative studies illustrate the wide variety of evolutiona...
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Post-stinging behavior of worker honey bees (Hymenoptera: Apidae)
Annals of the Entomological Society of America, 1998Co-Authors: S. J. Cunard, Michael D. BreedAbstract:Following sting autotomy, honey bee workers continue to participate in Colony Defense by following and harassing potential predators. Bees that pursue a human observer are highly likely to have previously stung a leather target at the Colony entrance, Wing wear and other characteristics of the pursuing bees suggest that they are soldier or guard bees rather than foragers or younger bees. We compared the responses of different behavioral castes by inducing a bee to sting and then assessing the response of that bee to other bees; after stinging, guard bees displayed heightened activity, but soldiers, foragers, or hive bees did not. Removal of the sting in cold-narcotized bees showed that the physiological stimulus for pursuit behavior was not solely the removal of the sting. The continued defensive role for bees that have lost their sting retains the residual value of individual workers to the Colony.
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The behavioral genetics of Colony Defense in honeybees: Genetic variability for guarding behavior
Behavior Genetics, 1991Co-Authors: Michael D. Breed, Kevin B. RogersAbstract:Guard honeybees stand at the entrance of colonies and facilitate the exclusion of nonnestmates from the Colony. In this study, we examined the hypothesis that genetic variability among individuals in colonies might explain variability in guarding activity. To do this, we cross-fostered honey bees between colonies with high-defensive responses and colonies with low-defensive responses in alarm pheromone tests. Individuals from high-defensive colonies were more likely to guard in their own colonies (controls) than cross-fostered bees from low-defensive colonies. Cross-fostered high-defensive bees also were more likely to guard in low-Defense colonies. These results support the hypothesis that interindividual differences in guarding behavior are at least partially under genetic control. A positive correlation between number of guards and response to alarm pheromone demonstrates a link between behaviorally separated components of the overall defensive response.
Harunobu Shibao - One of the best experts on this subject based on the ideXlab platform.
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Temporal division of labor in an aphid social system.
Scientific reports, 2021Co-Authors: Harunobu Shibao, Mayako Kutsukake, Takema FukatsuAbstract:Temporal division of labor, or age polyethism, in which altruistic caste individuals change their tasks with aging, is widely found in bees and ants (Hymenoptera) and also in other social insects. Here we report the discovery of elaborate age polyethism in a social aphid (Hemiptera). Tuberaphis styraci is a gall-forming aphid in which monomorphic first instar nymphs differentiate into normal nymphs and soldiers upon second instar molt. Soldiers neither grow nor reproduce but perform gall cleaning and Colony Defense. Using an artificial diet rearing system, we collected age-defined groups of soldiers and monitored their social behaviors. We observed that young soldiers tend to clean whereas old soldiers preferentially attack, thereby verifying age-dependent task switching from housekeeping to Defense. Strategic sampling, age estimation and behavioral observation of soldiers from natural galls revealed that (1) young cleaning soldiers tend to inhabit upper gall regions with adult insects, (2) old attacking soldiers tend to be distributed in lower gall regions, particularly around the gall openings, and (3) the gall structure is linked to intra-nest movement, aging and task switching of soldiers in an adaptive manner. These results highlight an evolutionary parallelism comparable to the sophisticated temporal division of labor observed in honeybee colonies.
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Extended lifespan and overlapping of generations in a gall-forming social aphid, Quadrartus yoshinomiyai
Insectes Sociaux, 2018Co-Authors: Keigo Uematsu, Harunobu ShibaoAbstract:The evolutionary relationship between sociality and extended lifespan has been studied in many taxa. We investigated the seasonal population dynamics and individual lifespan in a gall-forming social aphid, Quadrartus yoshinomiyai, whose wingless adults defend the Colony after ceasing reproduction. The galls of this species are completely closed for over a year, which facilitates monitoring aphid mortality rates in natural galls. Gall foundresses, which were born before winter and formed galls in April, were alive until December, indicating that they can survive for a year. The second-generation wingless adults, born in May or June of the first year, were alive in mature galls collected in March or April of the second year. Morphometric analysis revealed an overlap of three generations in a mature gall; the appendages of the second-generation wingless adults were smaller than those of the third-generation wingless adults. Our results suggest that the extended lifespan, favored in a completely closed gall where extrinsic mortality is very low, promotes the overlap of generations and post-reproductive Colony Defense by the wingless adults. An extended post-reproductive lifespan might also be favored if the cost of death by the potentially rapid spread of infectious diseases in the completely closed space exceeds the cost of living without reproduction.
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Altruistic Colony Defense by menopausal female insects.
Current biology : CB, 2010Co-Authors: Keigo Uematsu, Mayako Kutsukake, Takema Fukatsu, Masakazu Shimada, Harunobu ShibaoAbstract:Summary Recent studies have suggested that an extended postreproductive life span, such as life after menopause in human females, will evolve when the indirect (kin-selected) fitness benefits from altruistic behavior are greater than the direct fitness benefits from continuing reproduction [1–4]. Under some conditions in which postreproductive altruism is more beneficial and/or continuing reproduction is more costly, the postreproductive life span can be shaped by natural selection [5, 6]. However, indirect fitness benefits during postreproductive survival have been documented mainly in intelligent mammals such as humans and cetaceans, in which elder females possess enhanced social knowledge through learning [7–10]. Here we show that postreproductive females of the gall-forming aphid Quadrartus yoshinomiyai (Nipponaphidini) can gain indirect fitness benefits through their altruistic Colony Defense. These females cease reproduction around the time of gall opening and defend the Colony by sticking themselves to intruding predators with a waxy secretion that is accumulated in their body with aging. Our results suggest that the presence of an age-related trait for altruistic behavior promotes the evolution of postreproductive altruism in this social insect via kin selection under natural selection imposed by predators.
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Venomous protease of aphid soldier for Colony Defense
Proceedings of the National Academy of Sciences of the United States of America, 2004Co-Authors: Mayako Kutsukake, Harunobu Shibao, Naruo Nikoh, Mizue Morioka, Tomohiro Tamura, Tamotsu Hoshino, Satoru Ohgiya, Takema FukatsuAbstract:In social aphids, morphological, behavioral, and physiological differences between soldiers and normal insects are attributed to differences in gene expression between them, because they are clonal offspring parthenogenetically produced by the same mothers. By using cDNA subtraction, we identified a soldier-specific cysteine protease of the family cathepsin B in a social aphid, Tuberaphis styraci, with a second-instar soldier caste. The cathepsin B gene was specifically expressed in soldiers and first-instar nymphs destined to be soldiers. The cathepsin B protein was preferentially produced in soldiers and showed a protease activity typical of cathepsin B. The cathepsin B mRNA and protein were localized in the midgut of soldiers. For Colony Defense, soldiers attack enemies with their stylet, which causes paralysis and death of the victims. Notably, after soldiers attacked moth larvae, the cathepsin B protein was detected from the paralyzed larvae. Injection of purified recombinant cathepsin B protein certainly killed the recipient moth larvae. From these results, we concluded that the cathepsin B protein is a major component of the aphid venom produced by soldiers of T. styraci. Soldier-specific expression of the cathepsin B gene was found in other social aphids of the genus Tuberaphis. The soldier-specific cathepsin B gene showed an accelerated molecular evolution probably caused by the action of positive selection, which had been also known from venomous proteins of other animals.