Loss of males from mixed-sex societies in termites.

BACKGROUND: Sexual reproduction is the norm in almost all animal species, and in many advanced animal societies, both males and females participate in social activities. To date, the complete loss of males from advanced social animal lineages has been reported only in ants and honey bees (Hymenoptera), whose workers are always female and whose males display no helping behaviors even in normal sexual species. Asexuality has not previously been observed in colonies of another major group of social insects, the termites, where the ubiquitous presence of both male and female workers and soldiers indicate that males play a critical role beyond that of reproduction. RESULTS: Here, we report asexual societies in a lineage of the termite Glyptotermes nakajimai. We investigated the composition of mature colonies from ten distinct populations in Japan, finding six asexual populations characterized by a lack of any males in the reproductive, soldier, and worker castes of their colonies, an absence of sperm in the spermathecae of their queens, and the development of unfertilized eggs at a level comparable to that for the development of fertilized eggs in sexual populations of this species. Phylogenetic analyses indicated a single evolutionary origin of the asexual populations, with divergence from sampled sexual populations occurring about 14 million years ago. Asexual colonies differ from sexual colonies in having a more uniform head size in their all-female soldier caste, and fewer soldiers in proportion to other individuals, suggesting increased defensive efficiencies arising from uniform soldier morphology. Such efficiencies may have contributed to the persistence and spread of the asexual lineage. Cooperative colony foundation by multiple queens, the single-site nesting life history common to both the asexual and sexual lineages, and the occasional development of eggs without fertilization even in the sexual lineage are traits likely to have been present in the ancestors of the asexual lineage that may have facilitated the transition to asexuality. CONCLUSIONS: Our findings demonstrate that completely asexual social lineages can evolve from mixed-sex termite societies, providing evidence that males are dispensable for the maintenance of advanced animal societies in which they previously played an active social role.

A Genomic Imprinting Model of Termite Caste Determination: Not Genetic but Epigenetic Inheritance Influences Offspring Caste Fate.

Eusocial insects exhibit the most striking example of phenotypic plasticity. There has been a long controversy over the factors determining caste development of individuals in social insects. Here we demonstrate that parental phenotypes influence the social status of offspring not through genetic inheritance but through genomic imprinting in termites. Our extensive field survey and genetic analysis of the termite Reticulitermes speratus show that its breeding system is inconsistent with a genetic caste determination model. We therefore developed a genomic imprinting model, in which queen- and king-specific epigenetic marks antagonistically influence sexual development of offspring. The model accounts for all known empirical data on caste differentiation of R. speratus and other related species. By conducting colony-founding experiments and additively incorporating relevant socio-environmental factors into our genomic imprinting model, we show the relative importance of genomic imprinting and environmental factors in caste determination. The idea of epigenetic inheritance of sexual phenotypes solves the puzzle of why parthenogenetically produced daughters carrying only maternal chromosomes exclusively develop into queens and why parental phenotypes (nymph- or worker-derived reproductives) strongly influence caste differentiation of offspring. According to our model, the worker caste is seen as a "neuter" caste whose sexual development is suppressed due to counterbalanced maternal and paternal imprinting and opens new avenues for understanding the evolution of caste systems in social insects.

Decoupling of Behavioral Trait Correlation Across Life Stages in Two Holometabolous Insects.

Many animal behaviors have a genetic base, and behavioral traits often correlate with one another. In this study, we tested for a behavioral correlation between tonic immobility and walking distance in the larval and adult stages independently of two holometabolous insects. We confirmed a negative correlation of traits between strains in adults of both the species; however, we did not find it in larvae of either species. This suggests that the negative correlation between tonic immobility and walking is decoupled across life stages from larva to adult. In contrast, previous studies have reported that phenotypic correlations between behavioral traits are maintained from larvae to adults in hemimetabolous insects. In addition, our present results differ from previous results with holometabolous insects. Therefore, our results suggest that metamorphosis can change trade-offs between behavioral traits.

Ant circadian activity associated with brood care type.

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

Apis cerana japonica discriminates between floral color phases of the oriental orchid, Cymbidium floribundum.

Foragers of the Japanese honeybee (Apis cerana japonica) were attracted by flowers of an oriental orchid (Cymbidium floribundum) and were observed to carry the pollinia on their scutella. After the removal of pollinia from the flowers, their labial color changed from white to reddish brown. Both artificial removal of pollinia and ethrel treatment of the flowers also induced this labial color change. Labia in color-changed flowers showed a decreased reflectance of wavelengths less than 670 nm compared to control intact flower. Both reflectance irradiance spectra and ultraviolet photographs showed that only the nectar guide in white (unchanged) flowers reflected ultraviolet light, and that this reflectance decreased with labial color change. Dual choice experiments showed that the honeybee foragers preferentially visited flowers having white labia rather than reddish brown. We suggest that Japanese honeybees discriminate between the floral phases of C. floribundum using color vision.

Transcriptomic analysis of epigenetic modification genes in the termite Reticulitermes speratus.

Eusocial insects display a caste system in which different castes are morphologically and physiologically specialized for different tasks. Recent studies have revealed that epigenetic modifications, including DNA methylation and histone modification, mediate caste determination and differentiation, longevity, and polyethism in eusocial insects. Although there has been a growing interest in the relationship between epigenetic mechanisms and phenotypic plasticity in termites, there is little information about differential expression levels among castes and expression sites for these genes in termites. Here we show royal-tissue-specific expression of epigenetic modification genes in the termite Reticulitermes speratus. Using RNA-seq, we identified 74 genes, including three DNA methyltransferases, seven sirtuins, 48 Trithorax group proteins, and 16 Polycomb group proteins. Among these genes, 15 showed king-specific expression, and 52 showed age-dependent differential expression in kings and queens. Quantitative real-time PCR revealed that DNA methyltransferase 3 is expressed specifically in the king's testis and fat body, whereas some histone modification genes are remarkably expressed in the king's testis and queen's ovary. These findings imply that epigenetic modification plays important roles in the gamete production process in termite kings and queens.

Protein tyrosine phosphatase SHP2 is involved in Semaphorin 4D-induced axon repulsion.

Semaphorin-4D (Sema4D), a member of class 4 membrane-bound Semaphorins, acts as a chemorepellant to the axons of retinal ganglion cells and hippocampal neurons. Plexin-B1, a neuronal Sema4D receptor, associates with either one of receptor tyrosine kinases, c-Met or ErbB2, to mediate Sema4D-signaling. In contrast to this significance, the involvement of protein tyrosine phosphatases in Semaphorin-signaling remains unknown. We here show that Src homology 2-containing protein-tyrosine phosphatase 2 (SHP2) participates in Sema4D-signaling. SHP2 was localized in the growth cones of chick embryonic retinal ganglion neurons. Phenylarsine oxide, a protein tyrosine phosphatase inhibitor, suppressed Sema4D-induced contractile response in COS-7 cells expressing Plexin-B1. Ectopic expression of a phosphatase-inactive mutant of SHP2 in the retinal ganglion cells attenuated Sema4D-induced growth cone collapse response. A SHP1/2 specific inhibitor, 8-hydroxy-7-(6-sulfonaphthalen-2-yl)diazenyl-quinoline-5-sulfonic acid (NSC-87877), also suppressed this collapse response. These results suggest that SHP2-mediated tyrosine dephosphorylation is an important step in Sema4D-induced axon repulsion.

Effects of temperature on circadian rhythm in the Japanese honeybee, Apis cerana japonica.

Temperature influences key aspects of insect circadian rhythms. The locomotor rhythm in foragers of the Japanese honeybee, Apis cerana japonica, was entrained to a skeleton temperature cycle. An initial warm temperature pulse was imposed at the beginning of subjective day and a second was applied at the end of the subjective day. A single warm pulse given every early subjective day in constant darkness (DD) entrained the locomotor rhythm without a second temperature pulse, but a single pulse given in late subjective day allowed a free-running rhythm. When honeybees were kept under a light-dark cycle, their body temperatures increased by 7-8 degrees C with locomotor activity. This temperature elevation remained during the photophase but followed the ambient environmental temperature at night. Body temperature oscillations continued to be circadian in DD, and temperature elevation occurred during the subjective day. In DD, the free-running period tau of locomotor activity increased when the ambient temperature increased from 27 to 37 degrees C, although these changes were within the range of temperature compensation for many organisms. Under continuous light conditions (LL), tau remained constant with more strict temperature compensation. Patterns of brain period mRNA levels of forager bees maintained at different temperatures in LL revealed that the free-running period of per mRNA rhythm was temperature compensated. In addition, temperature strongly influenced the amplitude of the circadian transcriptional rhythms during the free-run period in LL, which may confer temperature compensation. We also discuss the possibility that daily changes in forager body temperatures may act as an internal Zeitgeber by fluctuating hive temperature.

Potent social synchronization can override photic entrainment of circadian rhythms.

Circadian rhythms in behaviour and physiology are important for animal health and survival. Studies with individually isolated animals in the laboratory have consistently emphasized the dominant role of light for the entrainment of circadian rhythms to relevant environmental cycles. Although in nature interactions with conspecifics are functionally significant, social signals are typically not considered important time-givers for the animal circadian clock. Our results challenge this view. By studying honeybees in an ecologically relevant context and using a massive data set, we demonstrate that social entrainment can be potent, may act without direct contact with other individuals and does not rely on gating the exposure to light. We show for the first time that social time cues stably entrain the clock, even in animals experiencing conflicting photic and social environmental cycles. These findings add to the growing appreciation for the importance of studying circadian rhythms in ecologically relevant contexts.

Monitoring and Detecting the Cigarette Beetle (Coleoptera: Anobiidae) Using Ultraviolet (LED) Direct and Reflected Lights and/or Pheromone Traps in a Laboratory and a Storehouse.

The cigarette beetle, Lasioderma serricorne (F.), is an important stored-product pest worldwide because it damages dry foods. Detection and removal of the female L. serricorne will help to facilitate the control of the insect by removal of the egg-laying populations. In this manuscript, we examined the responses by L. serricorne to direct and reflected light in transparent cube (50 m3) set in a chamber (200 m3) and a stored facility with both direct and reflected UV-LED lights. The study also examined the responses by the beetles to light in the presence or absence of pheromone in traps that are placed at different heights. Reflected light attracted more beetles than the direct light in the experimental chamber, but the direct light traps attracted more beetles than the reflected light traps in the storehouse. Pheromone traps attracted only males; UV-LED traps attracted both sexes. The UV-LED traps with a pheromone, i.e., combined trap, attracted more males than UV-LED light traps without a pheromone, whereas the attraction of UV-LED traps with and without the pheromone was similar in females. The results suggest that UV-LED light trap combined with a sex pheromone is the best solution for monitoring and controlling L. serricorne.

Kinetic simulation of signal transduction system in hippocampal long-term potentiation with dynamic modeling of protein phosphatase 2A.

We modeled and analyzed a signal transduction system of long-term potentiation (LTP) in hippocampal post-synapse. Bhalla and Iyengar [Science 283(1999) 381] have developed a hippocampal LTP model. In the conventional model, the concentration of protein phosphatase 2A (PP2A) was fixed. However, it was reported that dynamic inactivation of PP2A was essential for LTP [J. Neurochem. 74 (2000) 807]. We introduced a dynamic modeling of PP2A; inactivation (phosphorylation) of PP2A by calcium/calmodulin-dependent protein kinase II (CaMKII) in the presence of calcium/calmodulin, self-activation (autodephosphorylation) of PP2A, and inactivation (dephosphorylation) of CaMKII by PP2A. This model includes complex feedback loops; both CaMKII and PP2A are autoactivated, while they inactivate each other. Moreover, we proposed an analysis strategy for model validation by applying the results of sensitivity analysis. In our system, calcineurin (CaN) played an essential role, rather than the activation of protein kinase C (PKC) as documented in the conventional model. From results of the analysis of our model, we found the following robustness as characteristics of bistability in our model: (1). PP2A reactions against calcium ion (Ca(2+)) perturbation; (2). PP2A inactivation against PP2A increase; (3). protein phosphatase 1 (PP1) activation against PF2A increase; and (4). PP2A reactions against PP2A initial concentration. These properties facilitated LTP induction in our system. We showed that another mechanism could introduce bistable behavior by adding dynamic reactions of PP2A.