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。     

Soldier caste influences on candidate primer pheromone levels and juvenile hormone-dependent caste differentiation in workers of the termite Reticulitermes flavipes

Caste systems and the division of labor they make possible are common underlying features of all social insects. Multiple extrinsic factors have been shown to impact caste composition in social insect colonies. Primer pheromones are one type of extrinsic caste-regulatory factor; they are chemical signaling molecules produced by certain colony members to impact developmental physiology of recipient nestmates. However, only limited evidence exists regarding primer pheromones and their actions in eusocial termites. In previous research we identified two soldier-produced terpenes, γ-cadinene (CAD) and γ-cadinenal (ALD), as candidate primer pheromones of the lower termite Reticulitermes flavipes. In the present study we tested hypotheses related to CAD and ALD action in recipient individuals. We examined the influences of terminally developed soldier termites on (1) CAD and ALD levels and (2) caste differentiation in developmentally totipotent workers. Our findings show CAD and ALD (respectively) are caste stimulatory and inhibitory components of chemical blends present in soldier heads, ALD levels increase significantly (10.9×) in workers only in the presence of soldiers, and soldiers can reduce developmental-hormone response thresholds of workers, presumably via ALD action. These findings provide novel evidence supporting that CAD and ALD are authentic caste-regulatory primer pheromones in Reticulitermes.     

Life history and development--a framework for understanding developmental plasticity in lower termites

Termites (Isoptera) are the phylogenetically oldest social insects, but in scientific research they have always stood in the shadow of the social Hymenoptera. Both groups of social insects evolved complex societies independently and hence, their different ancestry provided them with different life-history preadaptations for social evolution. Termites, the 'social cockroaches', have a hemimetabolous mode of development and both sexes are diploid, while the social Hymenoptera belong to the holometabolous insects and have a haplodiploid mode of sex determination. Despite this apparent disparity it is interesting to ask whether termites and social Hymenoptera share common principles in their individual and social ontogenies and how these are related to the evolution of their respective social life histories. Such a comparison has, however, been much hampered by the developmental complexity of the termite caste system, as well as by an idiosyncratic terminology, which makes it difficult for non-termitologists to access the literature.
Here, we provide a conceptual guide to termite terminology based on the highly flexible caste system of the "lower termites". We summarise what is known about ultimate causes and underlying proximate mechanisms in the evolution and maintenance of termite sociality, and we try to embed the results and their discussion into general evolutionary theory and developmental biology. Finally, we speculate about fundamental factors that might have facilitated the unique evolution of complex societies in a diploid hemimetabolous insect taxon. This review also aims at a better integration of termites into general discussions on evolutionary and developmental biology, and it shows that the ecology of termites and their astounding phenotypic plasticity have a large yet still little explored potential to provide insights into elementary evo-devo questions.     

昆虫翅型分化的表型可塑性机制

翅多型现象在昆虫中广泛存在,是昆虫在飞行扩散和繁殖能力之间权衡的一种策略,对种群的环境适应性进化具有重要的意义。目前在植食性昆虫中研究较多,有关寄生蜂的翅型分化鲜见报道。综述了昆虫翅型分化的表型可塑性机制。遗传因素和环境因素均对昆虫翅的发育产生影响,基因型对翅型的决定具有显著作用,外界环境条件,包括温度、光周期、食物质量、自身密度、外源激素等因素对昆虫翅的发育也产生重要的调节作用,从而产生翅的非遗传多型性现象。此外,天敌的寄生或捕食作用可能会诱导某些昆虫的翅型产生隔代表型变化。对昆虫产生翅多型现象的生态学意义及其在生物进化过程中的作用进行了讨论,并探讨了寄生性昆虫翅型分化机制在生物防治上的可能应用途径。功能基因组学和表观遗传学的进一步发展可望为彻底揭示昆虫翅型分化机制提供新的机遇和技术手段。     

Alternative splicing associated with phenotypic plasticity in the bumble bee Bombus terrestris

Phenotypic plasticity is when one genome can produce more than one phenotype. The caste system found in many social insects is an important example of plasticity. Several studies have examined gene expression in social insect developmental and caste differences. Changes in gene expression, however, are not the only source of phenotypic plasticity. Here, we investigate the role of alternative splicing in the buff‐tailed bumble bee Bombus terrestris. We found that 5,458 genes in B. terrestris (40%) express more than one isoform. Larvae have the lowest level of splicing events, followed by adults and then pupae. We found that when an isoform is expressed in a given caste in the larval stage, it tends to be expressed in all castes at the larval stage. The same is true at the pupal stage. However, we see more complicated interactions between the adult castes with reproductive females showing different isoform expression compared to nonreproductive females and male adults showing the most distinct patterns. We found 455 isoform switching genes, that is genes, where one developmental stage, sex or caste uses a specific isoform and another type uses a different isoform. Among genes displaying isoform switching are some involved in the ecdysteriod pathway, an important system in insect behaviour.     

Genomic imprinting and evolution of insect societies

Reproductive division of labor is a hallmark of social insect societies where individuals follow different developmental pathways resulting in distinct morphological castes. There has been a long controversy over the factors determining caste fate of individuals in social insects. Increasing evidence in the last two decades for heritable influences on division of labor put an end to the assumption that social insect broods are fully totipotent and environmental factors alone determine castes. Nevertheless, the genes that underlie hereditary effects on division of labor have not been identified in any social insects. Studies investigating the hereditary effects on caste determination might have overlooked non-genetic inheritance, while transmission to offspring of factors other than DNA sequences including epigenetic states can also affect offspring phenotype. Genomic imprinting is one of the most informative paradigms for understanding the consequences of interactions between the genome and the epigenome. Recent studies of genomic imprinting show that genes can be differentially marked in egg and sperm and inheritance of these epigenetic marks cause genes to be expressed in a parental-origin-specific manner in the offspring. By reviewing both the eusocial Hymenoptera and termites, I highlight the current theoretical and empirical evidence for genomic imprinting in eusocial insects and discuss how genomic imprinting acts in caste determination and social behavior and challenges for future studies. I also introduce the new idea that genomic imprinting plays an essential role in the origin of eusociality.     

Gene expression patterns associated with caste and reproductive status in ants: worker‐specific genes are more derived than queen‐specific ones

Variation in gene expression leads to phenotypic diversity and plays a central role in caste differentiation of eusocial insect species. In social Hymenoptera, females with the same genetic background can develop into queens or workers, which are characterized by divergent morphologies, behaviours and lifespan. Moreover, many social insects exhibit behaviourally distinct worker castes, such as brood‐tenders and foragers. Researchers have just started to explore which genes are differentially expressed to achieve this remarkable phenotypic plasticity. Although the queen is normally the only reproductive individual in the nest, following her removal, young brood‐tending workers often develop ovaries and start to reproduce. Here, we make use of this ability in the ant Temnothorax longispinosus and compare gene expression patterns in the queens and three worker castes along a reproductive gradient. We found the largest expression differences between the queen and the worker castes (~2500 genes) and the smallest differences between infertile brood‐tenders and foragers (~300 genes). The expression profile of fertile workers is more worker‐like, but to a certain extent intermediate between the queen and the infertile worker castes. In contrast to the queen, a high number of differentially expressed genes in the worker castes are of unknown function, pointing to the derived status of hymenopteran workers within insects.     

蜜蜂级型分化机理

蜜蜂Apis spp.能有效地为多种植物及农作物授粉, 具有重要的经济和生态价值; 蜜蜂作为高度真社会性昆虫, 已成为社会生物学研究的模式生物。社会性昆虫的生殖劳动分工具有重要的进化意义, 而级型分化是形成生殖劳动分工的基础。近年来, 关于蜜蜂级型分化的研究已取得诸多重要成果, 其机理也得到了较为深入的阐释。营养差异引发蜜蜂幼虫的级型分化。蜂王浆中的主要蛋白组分之一--Royalactin是诱导蜂王发育的关键营养因子, 而脂肪体细胞的表皮生长因子受体介导了Royalactin的这种蜂王诱导作用。DNA甲基化是重要的表观遗传机制之一, 且与个体发育和疾病发生紧密相关, 近来的研究表明DNA甲基化在蜜蜂级型分化过程中发挥重要的调控作用。此外, 越来越多的研究进一步深化了人们对内分泌系统调节级型分化作用的认识。本文从关键营养因子调控、 表观遗传调控和内分泌调节3方面综述蜜蜂级型分化的机理, 并对未来的研究提出可能的方向。     

Developmental regulation of caste-specific characters in social-insect polyphenism

Phenotypes of organisms are not determined completely genetically, but vary according to environmental factors (phenotypic plasticity). Some organisms express several discrete adaptive phenotypes (polyphenism). Social insects possess a few types of individuals (castes) in their colonies, to which specific tasks are allocated. Here, I review studies on caste polyphenism in ants and termites, in terms of the developmental mechanisms of caste-specific characters, such as alate wings and soldier mandibles. In ants, the developmental fate of caste is probably determined by the pattern-formation genes in the early stage of postembryonic development, but apoptotic degeneration occurs in the wing primordia of future workers. As apoptotic wing degeneration has been observed in two phylogenetically distant groups of ants, this phenomenon is suggested to be conserved in many ant species. On the other hand, all termite species possess distinct sterile soldiers with specific morphologies suitable for defense. Recent studies using molecular techniques isolated genes related to soldier differentiation and analyzed the expression profiles of those genes in order to understand the mechanism of caste differentiation and the link between molecular and social evolution. In this review, I focus on these studies, in terms of the alteration of body plan in response to environmental signals, and discuss the evolutionary process of the interaction between ontogeny and environment.     

Gene expression and the evolution of phenotypic diversity in social wasps

Background  

Organisms are capable of developing different phenotypes by altering the genes they express. This phenotypic plasticity provides a means for species to respond effectively to environmental conditions. One of the most dramatic examples of phenotypic plasticity occurs in the highly social hymenopteran insects (ants, social bees, and social wasps), where distinct castes and sexes all arise from the same genes. To elucidate how variation in patterns of gene expression affects phenotypic variation, we conducted a study to simultaneously address the influence of developmental stage, sex, and caste on patterns of gene expression in Vespula wasps. Furthermore, we compared the patterns found in this species to those found in other taxa in order to investigate how variation in gene expression leads to phenotypic evolution.     

Maternal effect on female caste determination in a social insect

Caste differentiation and division of labor are the hallmarks of social insect colonies [1, 2]. The current dogma for female caste differentiation is that female eggs are totipotent, with morphological and physiological differences between queens and workers stemming from a developmental switch during the larval stage controlled by nutritional and other environmental factors (e.g., [3-8]). In this study, we tested whether maternal effects influence caste differentiation in Pogonomyrmex harvester ants. By conducting crossfostering experiments we identified two key factors in the process of caste determination. New queens were produced only from eggs laid by queens exposed to cold. Moreover, there was a strong age effect, with development into queens occurring only in eggs laid by queens that were at least two years old. Biochemical analyses further revealed that the level of ecdysteroids was significantly lower in eggs developing into queens than workers. By contrast, we found no significant effect of colony size or worker exposure to cold, suggesting that the trigger for caste differentiation may be independent of the quantity and quality of resources provided to larvae. Altogether these data demonstrate that the developmental fate of female brood is strongly influenced by maternal effects in ants of the genus Pogonomyrmex.     

Genetic determination of female castes in a hybridogenetic desert ant

In most social insects, the brood is totipotent and environmental factors determine whether a female egg will develop into a reproductive queen or a functionally sterile worker. However, genetic factors have been shown to affect the female's caste fate in a few ant species. The desert ant Cataglyphis hispanica reproduces by social hybridogenesis. All populations are characterized by the coexistence of two distinct genetic lineages. Queens are almost always found mated with a male of the alternate lineage than their own. Workers develop from hybrid crosses between the genetic lineages, whereas daughter queens are produced asexually via parthenogenesis. Here, we show that the association between genotype and caste in this species is maintained by a ‘hard‐wired’ genetic caste determination system, whereby nonhybrid genomes have lost the ability to develop as workers. Genetic analyses reveal that, in a rare population with multiple‐queen colonies, a significant proportion of nestmate queens are mated with males of their own lineage. These queens fail to produce worker offspring; they produce only purebred daughter queens by sexual reproduction. We discuss how the production of reproductive queens through sexual, intralineage crosses may favour the stability of social hybridogenesis in this species.     

昆虫触角转录组研究进展

昆虫通过信息交流感受内外坏境的变化,影响着昆虫定位、搜索食物源、寻找产卵地点和选择配偶等行为。在昆虫中,触角分布着较多的嗅觉感受器,可以感知挥发性分子、气味和激素,是昆虫重要的嗅觉器官,参与信息交流。综述和展望昆虫触角转录组的研究进展,有利于促进害虫管理、害虫防治和社会性昆虫级型分化与劳动分工的研究,也能为昆虫触角后续研究和昆虫触角仿生的应用提供参考。     

Disruptive selection as a driver of evolutionary branching and caste evolution in social insects

Theory suggests that evolutionary branching via disruptive selection may be a relatively common and powerful force driving phenotypic divergence. Here, we extend this theory to social insects, which have novel social axes of phenotypic diversification. Our model, built around turtle ant (Cephalotes) biology, is used to explore whether disruptive selection can drive the evolutionary branching of divergent colony phenotypes that include a novel soldier caste. Soldier evolution is a recurrent theme in social insect diversification that is exemplified in the turtle ants. We show that phenotypic mutants can gain competitive advantages that induce disruptive selection and subsequent branching. A soldier caste does not generally appear before branching, but can evolve from subsequent competition. The soldier caste then evolves in association with specialized resource preferences that maximize defensive performance. Overall, our model indicates that resource specialization may occur in the absence of morphological specialization, but that when morphological specialization evolves, it is always in association with resource specialization. This evolutionary coupling of ecological and morphological specialization is consistent with recent empirical evidence, but contrary to predictions of classical caste theory. Our model provides a new theoretical understanding of the ecology of caste evolution that explicitly considers the process of adaptive phenotypic divergence and diversification.     

Conserved roles of Osiris genes in insect development,polymorphism and protection

Much of the variation among insects is derived from the different ways that chitin has been moulded to form rigid structures, both internal and external. In this study, we identify a highly conserved expression pattern in an insect‐only gene family, the Osiris genes, that is essential for development, but also plays a significant role in phenotypic plasticity and in immunity/toxicity responses. The majority of Osiris genes exist in a highly syntenic cluster, and the cluster itself appears to have arisen very early in the evolution of insects. We used developmental gene expression in the fruit fly, Drosophila melanogaster, the bumble bee, Bombus terrestris, the harvester ant, Pogonomyrmex barbatus, and the wood ant, Formica exsecta, to compare patterns of Osiris gene expression both during development and between alternate caste phenotypes in the polymorphic social insects. Developmental gene expression of Osiris genes is highly conserved across species and correlated with gene location and evolutionary history. The social insect castes are highly divergent in pupal Osiris gene expression. Sets of co‐expressed genes that include Osiris genes are enriched in gene ontology terms related to chitin/cuticle and peptidase activity. Osiris genes are essential for cuticle formation in both embryos and pupae, and genes co‐expressed with Osiris genes affect wing development. Additionally, Osiris genes and those co‐expressed seem to play a conserved role in insect toxicology defences and digestion. Given their role in development, plasticity, and protection, we propose that the Osiris genes play a central role in insect adaptive evolution.     

熊蜂级型分化研究进展

熊蜂是众多野生植物及农作物的有效授粉昆虫,具有重要的经济和生态价值。熊蜂复杂的生长发育过程及社会性使其成为社会生物学研究的最佳模式生物之一。社会性昆虫的生殖劳动分工具有重要的进化意义,而级型分化是形成生殖劳动分工的基础。蜜蜂级型分化的研究已取得诸多重要成果,其机理也得到了较为深入的阐释,而熊蜂的社会性研究尚未形成系统,与蜜蜂研究相差甚远。近来的研究表明,饲喂频率或者饲喂总量的差异能够引起熊蜂级型分化的发生。保幼激素和蜕皮激素与熊蜂幼虫的发育紧密联系,在熊蜂级型分化的过程中发挥重要作用。一些参与蜜蜂级型分化的基因,在熊蜂级型间也存在差异表达。此外,群体间的相互作用以及蜂王和工蜂间的竞争也是促进熊蜂级型分化发生的重要因素。本文从营养、激素调控、群体发展及相互作用等方面综述熊蜂级型分化机制,并对未来的研究提出可能方向。     

Environmental and genetic influences on queen and worker body size in the social wasp Vespula maculifrons

Many social insects exhibit morphologically distinct worker and queen castes that perform different functions. These functional differences may generate unique selection regimes operating on body size. For example, queens may be under directional selection for large body size, whereas directional selection on worker body size may be limited. Such contrasting selection pressures may differentially affect levels of genetic variation associated with size variation in the two castes. This study sought to determine if genetic effects underlying phenotypic differences varied between the worker and queen castes of the social wasp Vespula maculifrons. We predicted that directional selection would remove genetic variation associated with size differences in the queen caste, whereas a lack of directional selection would tend to maintain genetic variation associated with size differences in the worker caste. We thus (1) calculated broad and narrow sense heritabilities for several morphological traits, (2) examined whether some paternal genotypes produced more morphologically diverse offspring than others, and (3) determined whether trait size variation was associated with genetic variation within colonies. We found that few morphological traits were significantly heritable, indicating that little genetic variance for those traits existed within our study population. We also found that some patrilines produced more morphologically variable offspring than others, suggesting a role of genotype in phenotypic plasticity. And finally, no significant correlations between genetic diversity arising from multiple mating by queens within colonies and trait variation in either caste were found. Overall, our findings indicate a weak effect of genotype on both worker and queen body size variation and are suggestive of a large environmental influence on morphological trait size. Moreover, our results do not indicate that levels of genetic variation underlying size variation differ substantially between castes in this species.     

植物与草食动物之间的协同适应及进化

通常协同进化是指一个物种 (或种群 )的遗传结构由于回应于另一个物种 (或种群 )遗传结构的变化而发生的相应改变。广义的理解 ,协同进化是相互作用的物种之间的互惠进化。生物之间、特别是植物与草食动物之间的协同适应与进化 ,已经成为生物进化、生态、遗传等学科十分关注的问题 ,可能成为生物学中各学科研究的交汇点或结点。作者具体阐述了 :(1)生物之间协同进化的研究意义 ,包括对生物学与生态学的价值 ;(2 )生物之间协同进化研究的限制或困难 ,诸如时间、研究对象、进化等级尺度和研究方法的限制 ;(3)植物与草食动物之间协同进化的主要研究对象 (系统 ) ,即昆虫传粉系统、昆虫诱导植物反应系统、种子散布系统、以及大型草食动物采食与植物反应系统 ;(4 )植物与草食动物之间协同进化的主要研究内容 ,包括适应特征 (性状 )——物种的可塑性 ,以及适应机制——物种适应过程与策略两个方面 ;(5 )植物与草食动物之间协同进化研究的存在问题及研究方向