Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera)

A key characteristic of eusocial species is reproductive division of labour. Honey bee colonies typically have a single reproductive queen and thousands of sterile workers. Adult queens differ dramatically from workers in anatomy, physiology, behaviour and lifespan. Young female workers can activate their ovaries and initiate egg laying; these 'reproductive' workers differ from sterile workers in anatomy, physiology, and behaviour. These differences, however, are on a much smaller scale than those observed between the queen and worker castes. Here, we use microarrays to monitor expression patterns of several thousand genes in the brains of same-aged virgin queens, sterile workers, and reproductive workers. We found large differences in expression between queens and both worker groups (~2000 genes), and much smaller differences between sterile and reproductive workers (221 genes). The expression patterns of these 221 genes in reproductive workers are more queen-like, and may represent a core group of genes associated with reproductive physiology. Furthermore, queens and reproductive workers preferentially up-regulate genes associated with the nurse bee behavioural state, which supports the hypothesis of an evolutionary link between worker division of labour and molecular pathways related to reproduction. Finally, several functional groups of genes associated with longevity in other species are significantly up-regulated in queens. Identifying the genes that underlie the differences between queens, sterile workers, and reproductive workers will allow us to begin to characterize the molecular mechanisms underlying the evolution of social behaviour and large-scale remodelling of gene networks associated with polyphenisms.     

新元古代陡山沱组具细胞裂殖结构的丝状蓝藻

新元古代陡山沱组丝状蓝藻化石Oscillatoriopsis sp.,具丝状蓝藻化石记录中罕见的细胞分裂结构;其胞壁内陷的二等分裂方式,可能的丝体断裂结构。是现生丝状蓝藻生长和繁殖的典型特征;不具异形胞结构的形态特征,可能与其当时生存的海底表面的缺氧环境有关;这种基底环境,可能有利于Oscillatoriopsis sp。等磷酸盐化化石细节构造的保存。     

Sensory response system of social behavior tied to female reproductive traits

Background

Honey bees display a complex set of anatomical, physiological, and behavioral traits that correlate with the colony storage of surplus pollen (pollen hoarding). We hypothesize that the association of these traits is a result of pleiotropy in a gene signaling network that was co-opted by natural selection to function in worker division of labor and foraging specialization. By acting on the gene network, selection can change a suite of traits, including stimulus/response relationships that affect individual foraging behavior and alter the colony level trait of pollen hoarding. The ‘pollen-hoarding syndrome’ of honey bees is the best documented syndrome of insect social organization. It can be exemplified as a link between reproductive anatomy (ovary size), physiology (yolk protein level), and foraging behavior in honey bee strains selected for pollen hoarding, a colony level trait. The syndrome gave rise to the forager-Reproductive Ground Plan Hypothesis (RGPH), which proposes that the regulatory control of foraging onset and foraging preference toward nectar or pollen was derived from a reproductive signaling network. This view was recently challenged. To resolve the controversy, we tested the associations between reproductive anatomy, physiology, and stimulus/response relationships of behavior in wild-type honey bees.

Methodology/Principal Findings

Central to the stimulus/response relationships of honey bee foraging behavior and pollen hoarding is the behavioral trait of sensory sensitivity to sucrose (an important sugar in nectar). To test the linkage of reproductive traits and sensory response systems of social behavior, we measured sucrose responsiveness with the proboscis extension response (PER) assay and quantified ovary size and vitellogenin (yolk precursor) gene expression in 6–7-day-old bees by counting ovarioles (ovary filaments) and by using semiquantitative real time RT-PCR. We show that bees with larger ovaries (more ovarioles) are characterized by higher levels of vitellogenin mRNA expression and are more responsive to sucrose solutions, a trait that is central to division of labor and foraging specialization.

Conclusions/Significance

Our results establish that in wild-type honey bees, ovary size and vitellogenin mRNA level covary with the sucrose sensory response system, an important component of foraging behavior. This finding validates links between reproductive physiology and behavioral-trait associations of the pollen-hoarding syndrome of honey bees, and supports the forager-RGPH. Our data address a current evolutionary debate, and represent the first direct demonstration of the links between reproductive anatomy, physiology, and behavioral response systems that are central to the control of complex social behavior in insects.     

Early signs of disruption of wheat anther development associated with the induction of male sterility by meiotic-stage water deficit

 Water deficit during meiosis in microspore mother cells of wheat (Triticum aestivum L.) induces male sterility, which reduces grain yield. In plants stressed during meiosis and then re-watered, division of microspore mother cells seems to proceed normally, but subsequent pollen development is arrested. Stress-affected anthers generally lack starch. We employed light microscopy in conjunction with histochemistry to compare the developmental anatomy of water-stress-affected and normal anthers. The earliest effects of stress, detectable between meiosis and young microspore stages, were the degeneration of meiocytes, loss of orientation of the reproductive cells, and abnormal vacuolization of tapetal cells. Other effects observed during subsequent developmental stages were deposition of starch in the connective tissue where it is normally not present, hypertrophy of the middle layer or endothecial cells, and deposition of sporopollenin-like substances in the anther loculus. The resulting pollen grains lacked both starch and intine. These results suggest that abnormal degeneration of the tapetum in water-stressed anthers coupled with a loss of orientation of the reproductive cells could be part of early events leading to abortion of microspores. Received: 19 July 1996 / Revision accepted: 6 November 1996     

蜜蜂卵巢激活研究进展

蜜蜂Apis作为典型的社会性昆虫,最重要的特征就是生殖劳动分工。卵巢激活是蜜蜂发挥生殖能力的重要影响因素。本文对蜜蜂卵巢激活的影响因素、蜜蜂卵巢激活相关的基因表达及microRNA在蜜蜂卵巢激活过程中的可能作用进行了介绍,为研究蜜蜂级型分化和生殖劳动分工的分子机制提供依据。     

Alligators and Endocrine Disrupting Contaminants: A Current Perspective

Many xenobiotic compounds introduced into the environment byhuman activity have been shown to adversely affect wildlife.Reproductive disorders in wildlife include altered fertility,reduced viability of offspring, impaired hormone secretion oractivity and modified reproductive anatomy. It has been hypothesizedthat many of these alterations in reproductive function aredue to the endocrine disruptive effects of various environmentalcontaminants. The endocrine system exhibits an organizationaleffect on the developing embryo. Thus, a disruption of the normalhormonal signals can permanently modify the organization andfuture function of the reproductive system. We have examinedthe reproductive and developmental endocrinology of severalpopulations of American alligator (Alligator mississippiensis)living in contaminated and reference lakes and used this speciesas a sentinel species in field studies. We have observed thatneonatal and juvenile alligators living in pesticide-contaminatedlakes have altered plasma hormone concentrations, reproductivetract anatomy and hepatic functioning. Experimental studiesexposing developing embryos to various persistent and nonpersistentpesticides, have produced alterations in gonadal steroidogenesis,secondary sex characteristics and gonadal anatomy. These experimentalstudies have begun to provide the causal relationships betweenembryonic pesticide exposure and reproductive abnormalitiesthat have been lacking in pure field studies of wild populations.An understanding of the developmental consequences of endocrinedisruption in wildlife can lead to new indicators of exposureand a better understanding of the most sensitive life stagesand the consequences of exposure during these periods.     

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.     

Sperm competition and the evolution of male reproductive anatomy in rodents

Sperm competition is a pervasive selective force in evolution, shaping reproductive anatomy, physiology and behaviour. Here, we present comparative evidence that varying sperm competition levels account for variation in the male reproductive anatomy of rodents, the largest and most diverse mammalian order. We focus on the sperm-producing testes and the accessory reproductive glands, which produce the seminal fluid fraction of the ejaculate. We demonstrate a positive association between relative testis size and the prevalence of within-litter multiple paternity, consistent with previous analyses in which relative testis size has been found to correlate with sperm competition levels inferred from social organization and mating systems. We further demonstrate an association between sperm competition level and the relative size of at least two accessory reproductive glands: the seminal vesicles and anterior prostate. The size of the major product of these glands-the copulatory plug-is also found to vary with sperm competition level. Our findings thus suggest that selection for larger plugs under sperm competition may explain variation in accessory gland size, and highlight the need to consider both sperm and non-sperm components of the male ejaculate in the context of post-copulatory sexual selection.     

Sonographic assessment of nongravid female macaques (Macaca mulatta and Macaca fascicularis).

Sonographic monitoring of the reproductive tract in the nongravid female macaque provides a means for assessing normal anatomy and pathologic change involving the uterus and adnexal structures. Animals with reduced reproductive potential can be identified and diagnoses frequently confirmed with the use of ultrasound-guided aspiration/biopsy. The importance of these observations is twofold: (1) for the maintenance of a healthy reproductive colony, and (2) as a means of identifying animals for use as models for human health problems, such as endometriosis.     

The making of a social insect: developmental architectures of social design

We marvel at the social complexity of insects, marked by anatomically and behaviorally distinguishable castes, division of labor and specialization—but how do such systems evolve? Insect societies are composed of individuals, each undergoing its own developmental process and each containing its own genetic information and experiencing its own developmental and experiential environment. Yet societies appear to function as if the colonies themselves are individuals with novel “social genes” and novel social developmental processes. We propose an alternative hypothesis. The origins of complex social behavior, from which insect societies emerge, are derived from ancestral developmental programs. These programs originated in ancient solitary insects and required little evolutionary remodeling. We present evidence from behavioral assays, selective breeding, genetic mapping, functional genomics and endocrinology, and comparative anatomy and physiology. These insights explain how complex social behavior can evolve from heterochronic changes in reproductive signaling systems that govern ubiquitous and ancient relationships between behavior and ovarian development. BioEssays 29:334–343, 2007. © 2007 Wiley Periodicals, Inc.     

银杏雌雄配子体发育及胚胎形成的研究进展

银杏(Ginkgo biloba)是现存最古老的裸子植物之一, 其生殖过程表现出许多原始特征和独特性状, 长期以来备受国内外专家的关注。经过近100年的研究取得了显著成果: (1) 银杏雄配子体发育周期长, 经历了从平周分裂到斜背式分裂,并最终垂周分裂形成带有鞭毛的游动精子; (2) 银杏雌配子体发育经历较长的游离核期和细胞化期, 分化形成颈卵器母细胞并经平周分裂、垂周分裂和斜向分裂形成成熟的颈卵器(包括有4个颈细胞和1个卵细胞); (3) 推测其精细胞中的液泡状结构为受精过程中的遗传物质载体; (4) 原胚的形成经历了游离核期和细胞化期。该文针对国内外最新银杏生殖生物学方面的研究进展, 对银杏雌雄配子体发育、受精过程以及胚胎形成等方面进行较为系统全面的分析和总结, 为进一步的银杏生殖生物学研究提供有价值的参考资料。     

Differential gene expression between adult queens and workers in the ant Lasius niger

Ants and other social insects forming large societies are generally characterized by marked reproductive division of labour. Queens largely monopolize reproduction whereas workers have little reproductive potential. In addition, some social insect species show tremendous lifespan differences between the queen and worker caste. Remarkably, queens and workers are usually genotypically identical, meaning that any phenotypic differences between the two castes arise from caste-specific gene expression. Using a combination of differential display, microarrays and reverse Northern blots, we found 16 genes that were differentially expressed between adult queens and workers in the ant Lasius niger, a species with highly pronounced reproductive division of labour and a several-fold lifespan difference between queens and workers. RNA ligase mediated rapid amplification of cDNA ends (RLM-RACE) and gene walking were used to further characterize these genes. On the basis of the molecular function of their nearest homologues, three genes appear to be involved in reproductive division of labour. Another three genes, which were exclusively overexpressed in queens, are possibly involved in the maintenance and repair of the soma, a candidate mechanism for lifespan determination. In-depth functional analyses of these genes are now needed to reveal their exact role.     

Seasonally Variable Eusocially Selected Traits in the Paper Wasp, Mischocyttarus mexicanus

The expression of alternative traits that benefit eusocial individuals but are not directly involved in reproductive differences among those individuals, which I call ‘eusocially selected traits’, may vary in response to environmental changes if this increases an individual's inclusive fitness. In this study, I describe traits that separate individuals within the reproductive division of labor of Mischocyttarus mexicanus, a eusocial paper wasp, and determine whether observed eusocially selected traits vary across seasons. I examined M. mexicanus because females initiate new nests throughout most of the year where they experience different conditions depending on the season. Findings from this study suggest two main conclusions: (1) phenotypic differences among M. mexicanus females are mixed, showing specialized, generalized, and context‐dependent eusocially selected traits and (2) a female's position within the reproductive division of labor may be influenced by its state. The presence of context‐dependent traits, e.g. large females initiated solitary nests in the spring and grouped nests during the summer, suggests that the payoff for pursuing different positions within the reproductive division of labor changes across seasons. The expression of context‐dependent eusocially selected traits also suggests that, roles, instead of castes, may better reflect the reproductive division of labor among individuals of eusocial species like M. mexicanus.     

Cinematographic documentation of enchytraeid morphology and reproductive biology

This paper summarizes the processing of small enchytraeid species for cinematographic documentation and covers the main details of a film on their locomotion, food uptake, anatomy and reproductive biology. This includes copulation, shedding of the cocoon and hatching of the young, characteristic reproductive patterns for all clitellate worms.     

Leaf anatomy and relationships of Dietes (Iridaceae)

The leaf anatomy of Dietes is described, including all 6 species. Characters support the morphological evidence that Dietes is a distinct genus and related to other Iridoideae. Certain features, notably the epidermal structure and sheath vasculature, distinguish it from other Iridaceous genera, although the sheath vasculature indicates a relationship with some New World Iridoideae. The leaf margin type is similar to that of other Old World Iridoideae. Many leaf anatomical characters in Dietes are associated with xeromorphy. Leaf anatomy supports the division of Dietes into 2 subgenera.     

长足大竹象生殖系统的形态解剖研究

解剖研究了长足大竹象雌雄虫牛殖系统的构造.该虫的雌性生殖系统包括一对卵巢、一对侧输卵管、中输卵管、交配囊、受精囊、生殖腔、产卵器;雄性生殖系统由一对睾九、一对输精管、一对附腺、射精管和交配器组成.     

Juvenile hormone accelerates ovarian development and does not affect age polyethism in the primitively eusocial wasp,Ropalidia marginata

Juvenile hormone modulates post-imaginal reproductive division of labor in primitively eusocial species and promotes the production of queens (e.g., Polistes) while it modulates age polyethism and promotes the production of foragers in highly eusocial species (e.g., the honey bee). Ropalidia marginata is a primitively eusocial wasp that shows both post-imaginal regulation of reproductive division of labor as well as age polyethism. Hence, R.marginata is a particularly interesting model system to study the effect of juvenile hormone. We demonstrate here that a single, topical application of 100 micro g of juvenile hormone-III per female wasp accelerates ovarian development of wasps held in isolation. Similar application to wasps released back on to their natal nests has no effect on their rate of behavioral development as witnessed from the age of first performance of feed larva, build, bring pulp and bring food. We conclude therefore that in R.marginata, juvenile hormone has retained its function of modulating reproductive division of labor and has not acquired the function of modulating age polyethism.     

银杏雌雄配子体发育及胚胎形成的研究进展

银杏（Ginkgo biloba）是现存最古老的裸子植物之一, 其生殖过程表现出许多原始特征和独特性状, 长期以来备受国内外专家的关注。经过近100年的研究取得了显著成果： （1） 银杏雄配子体发育周期长, 经历了从平周分裂到斜背式分裂,并最终垂周分裂形成带有鞭毛的游动精子; （2） 银杏雌配子体发育经历较长的游离核期和细胞化期, 分化形成颈卵器母细胞并经平周分裂、垂周分裂和斜向分裂形成成熟的颈卵器（包括有4个颈细胞和1个卵细胞）; （3） 推测其精细胞中的液泡状结构为受精过程中的遗传物质载体; （4） 原胚的形成经历了游离核期和细胞化期。该文针对国内外最新银杏生殖生物学方面的研究进展, 对银杏雌雄配子体发育、受精过程以及胚胎形成等方面进行较为系统全面的分析和总结, 为进一步的银杏生殖生物学研究提供有价值的参考资料。     

Laboratory management of the ferret for biomedical research

Ferrets have become an increasingly important animal in biological research. This paper discusses unique aspects of the ferret's anatomy, reproductive behavior, husbandry, and diseases as they relate to the research use of this animal.