Termite queens have disproportionately more DNA in their fat body cells: reproductive division of labor and endoreduplication

Increases in DNA content caused by endoreduplication are widely observed in the metabolically active tissues of plants and animals. During egg production, insect females synthesize very large amounts of vitellogenin in their fat bodies, and female fat bodies of some insects become polyploid to accelerate vitellogenin production. Social insects have developed reproductive division of labor, wherein queens lay most of the eggs while other individuals have reduced fertility and undertake tasks required for maintaining the colony. Therefore, only queens are engaged in vitellogenin synthesis for egg production in social insects. Here, we show that termite queens have disproportionately more DNA in their fat body cells. Our DNA content analysis using flow cytometry demonstrated that more cells contained 4C‐DNA than 2C‐DNA in the fat bodies of Reticulitermes speratus queens. This high level of endoreduplication was not found in the fat body cells of other castes. This caste‐dependent doubling of DNA content in fat body cells suggests that termites exploit endoreduplication to boost egg production, in conjunction with the development of reproductive division of labor. This study highlights nuclear polyploidization as an adaptive strategy in social insects.     

The gene vitellogenin has multiple coordinating effects on social organization

Temporal division of labor and foraging specialization are key characteristics of honeybee social organization. Worker honeybees (Apis mellifera) initiate foraging for food around their third week of life and often specialize in collecting pollen or nectar before they die. Variation in these fundamental social traits correlates with variation in worker reproductive physiology. However, the genetic and hormonal mechanisms that mediate the control of social organization are not understood and remain a central question in social insect biology. Here we demonstrate that a yolk precursor gene, vitellogenin, affects a complex suite of social traits. Vitellogenin is a major reproductive protein in insects in general and a proposed endocrine factor in honeybees. We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity. These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways. Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes.     

The Gene vitellogenin Has Multiple Coordinating Effects on Social Organization

Temporal division of labor and foraging specialization are key characteristics of honeybee social organization. Worker honeybees (Apis mellifera) initiate foraging for food around their third week of life and often specialize in collecting pollen or nectar before they die. Variation in these fundamental social traits correlates with variation in worker reproductive physiology. However, the genetic and hormonal mechanisms that mediate the control of social organization are not understood and remain a central question in social insect biology. Here we demonstrate that a yolk precursor gene, vitellogenin, affects a complex suite of social traits. Vitellogenin is a major reproductive protein in insects in general and a proposed endocrine factor in honeybees. We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity. These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways. Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes.     

Edible insects: Traditional knowledge or western phobia?

With an increasing human population and environmental degradation, the world faces a major problem in providing adequate animal based proteins. Many traditional societies have used or still use insects as a protein source, while westernized societies are reluctant to use insects, despite being the major consumers of animal proteins. We now need to consider insects as a source of food for humans in a manner that acknowledges both the role of entomophagy in indigenous societies and the need for westernized societies to reduce the size of their environmental footprint with regard to food production. The situation on continents such as Africa, Asia, and Central and South America has some parallels to Australia in that there are two forces in operation: the sustainable traditional use of edible insects and the "westernization" of these societies leading to a movement away from entomophagy. However, the potential to reach a compromise is greater in these continents because entomophagy is already accepted. The major challenges will be establishing sustainable production systems that include food safety and security as well as environmental protection. Whether this will happen or not will depend upon: (i) a major change in attitude in westernized societies towards entomophagy; (ii) pressure to conserve remaining habitats in a sustainable manner; (iii) economic impetus to develop food production systems that include insects; and (iv) an acknowledgement that achieving adequate nutrition on a global basis will involve different diets in much of the developed world.     

Reproductive decision-making in the termite, Cryptotermes secundus (Kalotermitidae), under variable food conditions

Relatedness concepts have dominated the discussion on the evolutionand maintenance of eusociality in social insects. In the diploidtermites, explanations based on relatedness asymmetries havebeen less relevant than in the Hymenoptera; ecological factorshave been claimed to be paramount. Yet, relevant quantitativestudies investigating the role of ecological factors are lacking.We examined the influence of ecological factors on reproductivetactics in the drywood termite, Cryptotermes secundus. In thisspecies, caste development is very flexible, with individualshaving the option to remain at the natal nest as helpers/workersor to develop into dispersing reproductives (sexuals). An importantecological factor expected to influence this "decision" is foodavailability; C. secundus nests in a piece of wood that servesas food and shelter, with individuals never leaving the nestto forage. Thus, a reduction in the amount of food parallelsa reduction in the nests' longevity. Therefore, we tested theinfluence of food availability on caste-developmental decisionsin natural colonies, as well as in two experiments in whichwe simulated a gradual and a sudden decline in the amount ofavailable food. In all trials dispersing sexuals occurred moreoften in colonies with diminished food resources than in colonieswith abundant suitable food. Thus, regardless of how food declines,individuals seem to switch their tactic from being a helperto becoming a dispersing reproductive if nest conditions deteriorateand the nests's longevity decline.     

Ecological and evolutionary consequences of early ontogenies of darters (Etheostomatini)

Synopsis The ecological classification of fishes into reproductive guilds is based on the premises that (1) reproductive styles and early ontogeny are closely related, and (2) both are correlated with the ecology of a species. A comparison of early ontogenies of logperch (Percina caprodes), rainbow darter (Etheostoma caeruleum), and fantail darter (E. flabellare) confirmed these premises, and provided possible explanations for diversity within the Etheostomatini. Young logperch have limited vitelline circulation, hatch while still poorly developed, and therefore must drift from oxygen rich lotic habitats to lentic habitats where small planktonic prey are available. Young rainbow and fantail darters have extensive vitelline plexuses, are well developed at transition to first feeding, and begin feeding on aquatic insects. Thus there is no necessity for a drift interval. As a result, the latter species are adapted for stream life. Interspecific differences in reproductive styles and early ontogenies may have contributed to speciation of darters by allowing partitioning of breeding sites and food resources for young. In addition, reduced drift dispersal and small stream habitation may have indirectly contributed to speciation by reducing genetic exchange among populations.     

Brain biogenic amines and reproductive dominance in bumble bees (Bombus terrestris)

To begin to explore the role of biogenic amines in reproductive division of labor in social insects, brain levels of dopamine, serotonin, and octopamine were measured in bumble bee (Bombus terrestris) workers and queens that differ in behavioral and reproductive state. Levels of all three amines were similar for mated and virgin queens. Young workers that developed with or without a queen had similar amine levels, but in queenright colonies differences in biogenic amine levels were associated with differences in behavior and reproductive physiology. Dominant workers had significantly higher octopamine levels compared with workers of lower dominance status but of similar size, age, and ovary state. High dopamine levels were associated with the last stages of oocyte development irrespective of worker social status and behavior. These results suggest that biogenic amines are involved in behavioral and physiological aspects of regulation of reproduction in bumble bees. Accepted: 10 December 1999     

Colony Membership, Division of Labor, and Genetic Relatedness Among Females of Colonies of Eustenogaster fraterna (Hymenoptera, Vespidae, Stenogastrinae)

To compare the social structure of primitively social wasps with that of communal breeding vertebrates, we used a new technique based on micro videocameras applied to the nest envelope to study the organization of behavior in Malaysian colonies of the stenogastrine wasp Eustenogaster fraterna. The reproductive division of labor in this species appears to be different from that reported so far in other species of Stenogastrinae: it is at a very primitive stage because the helpers work less hard and take fewer risks than the egg-layers. Nevertheless, the very low-risk tasks performed by the helpers (nest guarding and supply of abdominal secretion to the young larvae) are important for the colonies. Behavioral characters and ovarian development of the helpers suggest that females are only temporary helpers and that they wait to start their own production of offspring in the hope of inheriting the nest. Females of the same colony can be highly related, but in some colonies we found low-related individuals. The social organization of these wasps resembles that of vertebrate groups with helpers at the den, i.e., in the small number of individuals, the division of labor with limited reproductive inhibition, and the prolonged external work of the reproductive individuals. However, the main drive to sociality in these insects appears to be different, being based mainly on problems connected with short adult life and long immature brood development.     

Individual experience alone can generate lasting division of labor in ants

Division of labor, the specialization of workers on different tasks, largely contributes to the ecological success of social insects [1, 2]. Morphological, genotypic, and age variations among workers, as well as their social interactions, all shape division of labor [1-12]. In addition, individual experience has been suggested to influence workers in their decision to execute a task [13-18], but its potential impact on the organization of insect societies has yet to be demonstrated [19, 20]. Here we show that, all else being equal, ant workers engaged in distinct functions in accordance with their previous experience. When individuals were experimentally led to discover prey at each of their foraging attempts, they showed a high propensity for food exploration. Conversely, foraging activity progressively decreased for individuals who always failed in the same situation. One month later, workers that previously found prey kept on exploring for food, whereas those who always failed specialized in brood care. It thus appears that individual experience can strongly channel the behavioral ontogeny of ants to generate a lasting division of labor. This self-organized task-attribution system, based on an individual learning process, is particularly robust and might play an important role in colony efficiency.     

Policing and punishment across the domains of social evolution

Several decades of research in humans, other vertebrates, and social insects have offered fascinating insights into the dynamics of punishment (and its subset, policing), but authors have only rarely addressed whether there are fundamental joint principles underlying the maintenance of these behaviors. Here we present a punisher/bystander approach rooted in inclusive fitness logic to predict which individuals should take on punishing roles in animal societies. We apply our scheme to societies of eusocial Hymenoptera and nonhuman vertebrate social breeders, and we outline potential extensions for understanding conflict regulation among cells in metazoan bodies and unrelated individuals in human societies. We highlight that: 1) no social unit is expected to express punishment behavior unless it collects positive inclusive fitness benefits that surpass alternative benefits of bystanding; 2) punishment with public good benefits can be maintained through either direct fitness benefits (coercion) or indirect fitness benefits (correction) or both; 3) differences across social systems in the distributions of power, relatedness, and reproductive options drive variation in the extent to which individuals actively punish; and 4) inclusive fitness logic captures many punishment‐relevant evolutionary and ecological variables in a single framework that appears to apply across very different types of social arrangements. Synthesis Researchers have long observed that individuals in animal societies punish (and by extension, police) each other, but they have rarely investigated whether general principles underlie this behavior across social arrangements. In this paper, we present a punisher/bystander approach rooted in inclusive fitness logic to predict which individuals should take on punisher roles in animal societies. We apply the approach to eusocial insects and cooperatively breeding vertebrates and outline extensions towards the control of cancer cell lineages and punishment in human groups. We highlight how variation in specific social variables may drive differences in punishing/policing across the social domains.     

社会性昆虫级型和行为分化机制研究进展

社会性的出现是生物演化过程中的重要革新, 理解社会性的演化和调控机制具有重要的理论和实际意义。社会性昆虫的个体间有着明显的级型分化和劳动分工, 这有利于它们适应复杂的环境变化。理解社会性昆虫如何产生不同的形态、行为和生活史特性, 一直是进化和发育生物学的重要目标。随着测序技术的不断更新及生物信息学的快速发展, 已经有众多关于社会性昆虫级型和行为分化机制的研究报道。本文通过整理社会性昆虫研究的已有成果, 从环境因素、生理调控和分子机制等方面对社会性昆虫级型和行为分化机制相关研究进展进行了综述, 并对未来的研究方向做出了展望。根据现有证据, 社会性昆虫所生活的生物环境(食物营养、信息素、表皮碳氢化合物)和非生物环境(温度、气候等)均能直接或间接影响社会性昆虫级型和行为的分化; 保幼激素、蜕皮激素、类胰岛素及生物胺等内分泌激素和神经激素对社会性昆虫的级型和行为分化也有重要的调控作用; 此外, 遗传因素、新基因等DNA序列或基因组结构上的变化以及表观遗传修饰、基因的差异表达等基因调控机制均能不同程度地影响社会性昆虫的行为分化。本文建议加强昆虫纲其他社会性类群如半翅目蚜虫和缨翅目蓟马等的社会性行为及其演化机制的研究, 以加深对社会性昆虫起源及其行为演化的理解和认识。     

The evolution of parental care in insects: the roles of ecology,life history and the social environment

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Colony size predicts division of labour in attine ants

Division of labour is central to the ecological success of eusocial insects, yet the evolutionary factors driving increases in complexity in division of labour are little known. The size–complexity hypothesis proposes that, as larger colonies evolve, both non-reproductive and reproductive division of labour become more complex as workers and queens act to maximize inclusive fitness. Using a statistically robust phylogenetic comparative analysis of social and environmental traits of species within the ant tribe Attini, we show that colony size is positively related to both non-reproductive (worker size variation) and reproductive (queen–worker dimorphism) division of labour. The results also suggested that colony size acts on non-reproductive and reproductive division of labour in different ways. Environmental factors, including measures of variation in temperature and precipitation, had no significant effects on any division of labour measure or colony size. Overall, these results support the size–complexity hypothesis for the evolution of social complexity and division of labour in eusocial insects. Determining the evolutionary drivers of colony size may help contribute to our understanding of the evolution of social complexity.     

Seasonal Energetic Stress in a Tropical Forest Primate: Proximate Causes and Evolutionary Implications

Animals facing seasonal variation in food availability experience selective pressures that favor behavioral adjustments such as migration, changes in activity, or shifts in diet. Eclectic omnivores such as many primates can process low-quality fallback food when preferred food is unavailable. Such dietary flexibility, however, may be insufficient to eliminate constraints on reproduction even for species that live in relatively permissive environments, such as moist tropical forests. Focusing on a forest-dwelling primate with a flexible diet (Cercopithecus mitis) we investigated whether females experience seasonal energetic stress and how it may relate to reproductive seasonality. We used fecal glucocorticoids (fGCs) as an indicator of energetic stress, controlling for the potentially confounding effects of social interactions and reproductive state. We modeled within-female fGC variation with General Linear Mixed Models, evaluating changes in feeding behavior and food availability as main effects. Regardless of reproductive state, fGCs increased when females shifted their diet towards fallback foods (mature leaves and other non-preferred items) and when they spent more time feeding, while fGCs decreased with feeding time on preferred items (insects, fruits, young leaves) and with the availability of young leaves. Changes in fruit availability had no general effects on fGCs, likely because fruits were sought out regardless of availability. As predicted, females in the energetically demanding stages of late pregnancy and early lactation showed greater increases in fGCs between periods of low versus high availability of fruits and young leaves than females in other reproductive states. Potential social stressors had no measurable effects on fGCs. Preliminary evidence suggests that seasonal energetic stress may affect the timing of infant independence from mothers and contribute to unusually long inter-birth intervals compared to closely related species of similar body size. Our findings highlight how the study of stress responses can provide insights into the proximate control of reproductive strategies.     

Is top‐down control by predators driving insect abundance and herbivory rates in fragmented forests?

The effects of forest fragmentation on ecological interactions and particularly on food webs have scarcely been analysed. There is usually less herbivory in forest fragments than in continuous forests. Here we hypothesize that forest fragmentation enhances top‐down control of herbivory through an increase in insectivorous birds and a decrease in herbivorous insects, with a consequent decrease in plant reproductive success in small forest fragments. In the Maulino forest in central Chile, we experimentally excluded birds from Aristotelia chilensis (Elaeocarpaceae) trees in both forest fragments and continuous forest, and analysed herbivore insect abundance, herbivory and plant reproductive success during two consecutive growing seasons. We expected that insect abundance and herbivory would increase, and reproductive success would decrease in A. chilensis from which birds have been excluded, particularly in forest fragments where bird abundance and predation pressure on insects is higher. The abundance of herbivorous insects was lower in the forest fragments than in the continuous forest only in the first season, and herbivory was lower in forest fragments than in the continuous forest throughout the study. Moreover, during the second growing season herbivory was greater in the excluded trees than in the control trees, and as expected, there was a greater difference in the fragments than in the continuous forest, but this was not statistically significant. Exclusion of birds did not affect the reproductive success of A. chilensis. Our results, after 2 years of study, demonstrate that birds affect the levels of herbivory on A. chilensis in the Maulino forest, but do not support our hypothesis of enhanced top‐down control in fragmented forests, as the strength of the effect of excluding birds did not vary with fragmentation.     

Selection on defensive traits in a sterile caste – caste evolution: a mechanism to overcome life‐history trade‐offs?

SUMMARY During development and evolution individuals generally face a trade-off between the development of weapons and gonads. In termites, characterized by reproductive division of labor, a caste evolved—the soldiers—which is completely sterile and which might be released from developmental trade-offs between weapons and testes. These soldiers are exclusively dedicated to defense. First, we investigated whether defensive traits are under selection in sterile termite soldiers using allometric analyses. In soldiers of the genus Cryptotermes phragmotic traits such as a sculptured and foreshortened head evolve rapidly but were also lost twice. Second, we compared the scaling relationships of these weapons with those in solitary insects facing a trade-off between weapons and gonads. Defensive traits consistently had lower slopes than nondefensive traits which supports the existence of stabilizing selection on soldier phragmotic traits in order to plug galleries. Moreover, soldier head widths were colony specific and correlated with the minimum gallery diameter of a colony. This can proximately be explained by soldiers developing from different instars. The scaling relationships of these termite soldiers contrast strikingly with those of weapons of solitary insects, which are generally exaggerated (i.e., overscaling) male traits. These differences may provide important insights into trait evolution. Trade-offs constraining the development of individuals may have been uncoupled in termites by evolving different castes, each specialized for one function. When individuals in social insect are "released" from developmental constraints through the evolution of castes, this certainly contributed to the ecological and evolutionary success of social insects.     

The ecosystem services provided by social insects: traits,management tools and knowledge gaps

Social insects, i.e. ants, bees, wasps and termites, are key components of ecological communities, and are important ecosystem services (ESs) providers. Here, we review the literature in order to (i) analyse the particular traits of social insects that make them good suppliers of ESs; (ii) compile and assess management strategies that improve the services provided by social insects; and (iii) detect gaps in our knowledge about the services that social insects provide. Social insects provide at least 10 ESs; however, many of them are poorly understood or valued. Relevant traits of social insects include high biomass and numerical abundance, a diversity of mutualistic associations, the ability to build important biogenic structures, versatile production of chemical defences, the simultaneous delivery of several ESs, the presence of castes and division of labour, efficient communication and cooperation, the capacity to store food, and a long lifespan. All these characteristics enhance social insects as ES providers, highlighting their potential, constancy and efficiency as suppliers of these services. In turn, many of these traits make social insects stress tolerant and easy to manage, so increasing the ESs they provide. We emphasise the need for a conservation approach to the management of the services, as well as the potential use of social insects to help restore habitats degraded by human activities. In addition, we stress the need to evaluate both services and disservices in an integrated way, because some species of social insects are among the most problematic invasive species and native pests. Finally, we propose two areas of research that will lead to a greater and more efficient use of social insects as ES providers, and to a greater appreciation of them by producers and decision‐makers.     

Specialization Does Not Predict Individual Efficiency in an Ant

The ecological success of social insects is often attributed to an increase in efficiency achieved through division of labor between workers in a colony. Much research has therefore focused on the mechanism by which a division of labor is implemented, i.e., on how tasks are allocated to workers. However, the important assumption that specialists are indeed more efficient at their work than generalist individuals—the “Jack-of-all-trades is master of none” hypothesis—has rarely been tested. Here, I quantify worker efficiency, measured as work completed per time, in four different tasks in the ant Temnothorax albipennis: honey and protein foraging, collection of nest-building material, and brood transports in a colony emigration. I show that individual efficiency is not predicted by how specialized workers were on the respective task. Worker efficiency is also not consistently predicted by that worker''s overall activity or delay to begin the task. Even when only the worker''s rank relative to nestmates in the same colony was used, specialization did not predict efficiency in three out of the four tasks, and more specialized workers actually performed worse than others in the fourth task (collection of sand grains). I also show that the above relationships, as well as median individual efficiency, do not change with colony size. My results demonstrate that in an ant species without morphologically differentiated worker castes, workers may nevertheless differ in their ability to perform different tasks. Surprisingly, this variation is not utilized by the colony—worker allocation to tasks is unrelated to their ability to perform them. What, then, are the adaptive benefits of behavioral specialization, and why do workers choose tasks without regard for whether they can perform them well? We are still far from an understanding of the adaptive benefits of division of labor in social insects.     

Social learning about egg-laying substrates in fruitflies

Social learning, defined as learning from other individuals, has had dramatic effects on some species, including humans, in whom it has generated a rich culture. As a first step in examining the evolution of and mechanisms underlying social learning in insects, we tested for social learning in fruitflies (Drosophila melanogaster). Focal females (observers) that experienced novel food together with mated females (models), who had laid eggs on that food, subsequently exhibited a stronger preference for laying eggs on that food over another novel food compared with focal females that experienced the food alone. We observed no social learning, however, when observers experienced food with potentially more ambiguous social information provided by the presence of either virgin models or aggregation pheromone. This first documentation of social learning about egg-laying substrates in fruitflies builds on recent data indicating intricate use of social information by fruitflies and opens up exciting avenues for research on the evolution and neurogenetics of social learning using biology''s major model system.     

生态因素对蛾类昆虫交配与生殖的影响

对于两性生殖的昆虫而言,两性交配过程是产生后代及维持种群繁衍的必要环节。然而,昆虫的生殖行为经常受到一系列的内部生理因素和外部生态因素的影响,最终导致昆虫的生殖适合度产生差异。本文以蛾类昆虫为例,通过检索国内外文献,分析比较了气候因素(温度、湿度和光照)、生物因素(寄主植物、天敌和共生菌)和农事活动等生态因素对这类昆虫交配行为和生殖适合度的影响。结果表明,这些因子不但影响该类昆虫的交配行为(包括求偶与交配高峰、交配成功率、交配次数和交配持续时间等),还影响其生殖适合度(如产卵前期、产卵期、产卵量、孵化率和寿命等)。这些研究为深入开展蛾类昆虫的生殖行为生态学研究提供理论基础,同时为揭示蛾类昆虫的种群暴发机制以及该类害虫的科学防控提供线索。