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Insect Frontiers, November 2009 Volume 1 Number 1
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Insect Behaviour
- Social competition but not subfertility leads to a division of labour in the facultatively social sweat bee Megalopta genalis (Hymenoptera: Halictidae)
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aSmithsonian Tropical Research Institute, Panama
bDepartment of Ecology & Evolutionary Biology, University of California, Los Angeles, U.S.A.
cAnimal Behavior Area, Department of Psychology, University of Washington, U.S.A.
Insects with facultative social behaviour permit direct examination of factors associated with the expression of division of labour: why do some females remain in their natal nest as nonreproductive foragers, while others disperse? The facultatively social halictid bee Megalopta genalis shows strong reproductive division of labour, associated with body size (foragers tend to be smaller than queens and dispersers). We used M. genalis to test two hypotheses for the expression of worker behaviour: (1) queens suppress reproduction by subordinates, which then forage, and (2) small-bodied females are handicapped as reproductives, and therefore take on a foraging role to assist a more fertile relative (the ‘subfertility’ hypothesis). We removed queens from 19 nests and found that the remaining foragers enlarged their ovaries and reproduced at the same rate as solitary reproductives from unmanipulated (nonremoval) nests. This observation suggests that queen dominance limited reproduction by subordinates, and that foragers were not handicapped reproductives. To investigate the effect of body size variation on reproductive rate in the absence of social interactions, we placed single, newly eclosed females into 31 observation nests. Body size was not correlated with reproductive output or with the females' tenure in the observation nests. Nor was there any correlation between body size and number of brood cells in 21 solitary-female nonremoval nests. Taken together these data show that small females were not inherently poor reproductives. We also found that ovaries of reproductive females from social groups were larger than those of solitary reproductives, suggesting that social structure shapes ovary development.
Animal BehaviourVolume 78, Issue 5, November 2009, Pages 1043-1050
- Female fitness consequences of male harassment and copulation in seed beetles, Callosobruchus maculatus
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aDepartment of Ecology and Evolutionary Biology, University of Toronto
Despite widespread evidence for the benefits of polyandry, there are costs associated with each mating for females, and for many species, it is unknown whether the costs of extra matings outweigh the benefits. In the seed beetle Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae), costs might come from male harassment during mating attempts or from injuries that females sustain during copulation. Benefits of mating might come from nutrients or water transferred in the ejaculate. If mating is costly overall, male presence (sexual harassment) and multiple mating in C. maculatus is expected to reduce female fitness. Females were housed with differing numbers of males (1–4) and differing opportunities for copulation. When females were both harassed by and could remate with more than one male, they had lower lifetime reproductive rates and reduced life span relative to monandrous females. These results indicate that when females are continually exposed to multiple males, the direct benefits of multiple mating do not compensate for the costs.
Animal BehaviourVolume 78, Issue 5, November 2009, Pages 1061-1070
- Jail baits: how and why nymphs mimic adult females of the German cockroach, Blattella germanica
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aDepartment of Entomology and W. M. Keck Center for Behavioral Biology, North Carolina State University, U.S.A.
bPhotosensitive Materials Research Center, Toyo Gosei Co., Ltd, Chiba, Japan
The male German cockroach performs a characteristic courtship behaviour upon contacting a sexually receptive female: he turns away from the female and raises his wings, thereby exposing tergal glands whose reservoirs contain phagostimulatory substances. The female then mounts the male and feeds upon these nuptial secretions; this behaviour places her in the appropriate precopulatory position. The contact sex pheromone on the cuticular surface of the female, responsible for eliciting courtship behaviour in males, consists of a blend of six components that share a common biosynthetic pathway. An excised female antenna can elicit the full courtship display in males. We found that antennae taken from either male or female nymphs of various ages also could elicit the full courtship response in adult males. We extracted lipids from the cuticular surface of nymphs and, guided by behavioural assays, we fractionated the extracts using various chromatography procedures, including flash (column) chromatography, high-performance liquid chromatography and gas chromatography. Mass spectrometry analysis of behaviourally active fractions revealed two classes of courtship-eliciting compounds: all nymphs possessed a novel, still unidentified compound that elicited courtship in adult males. In addition, in last-instar females, we isolated four of the six adult female-specific contact sex pheromone components, consistent with differentiation of the sexes at this stage, and the onset of sexual maturation of the pheromone biosynthetic machinery. Our results support the interpretation that nymphs engage in sexual mimicry to gain access to male-produced nuptial tergal secretions that are exposed and can be secured only during courtship.
Animal BehaviourVolume 78, Issue 5,, November 2009, Pages 1097-1105
- Seasonally adaptive migratory headings mediated by a sun compass in the painted lady butterfly, Vanessa cardui
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aPlant and Invertebrate Ecology, Rothamsted Research, U.K.
bDepartment of Biology, University of York, U.K.
cGibraltar Ornithological and Natural History Society, Gibraltar
Many insects undertake long-distance migrations to exploit seasonally variable conditions at high latitudes, but the mechanisms used by migrants to select and maintain beneficial flight headings are poorly understood. Using computerized flight simulators, we performed controlled experiments to test the ability of an obligate migrant butterfly (Vanessa cardui) to orient in seasonally advantageous directions (i.e. northwards in spring and southwards in autumn). We also investigated the compass mechanism used to select and maintain these headings. Laboratory-reared autumn-generation butterflies flown in the U.K. displayed a highly significant mean orientation towards the south-southwest, consistent with return migration to winter breeding sites. However, seasonally adaptive flight headings were not observed in wild-caught adults flown at the same time. Spring-generation adults caught in Gibraltar (presumed to be migrating from winter breeding sites in North Africa into Europe) showed no evidence of northward flight headings, but produced a wide scatter of flight headings with a mean direction towards the west. Butterflies flown in the simulators when the sky was not visible produced a random scatter of flight headings and less-directed flight tracks, providing evidence that migrating V. cardui use a sun compass to select and maintain their flight headings. However, when butterflies were subjected to a 6 h clock shift, no change in orientation was observed relative to the control group. Field evidence for a return migration in autumn by V. cardui is surprisingly scarce in the literature, but we conclude that the species does attempt such southward movements and that individuals use a sun compass to select their migratory heading.
Animal BehaviourVolume 78, Issue 5, November 2009, Pages 1119-1125
- Copulation reduces the duration of death-feigning behaviour in the sweetpotato weevil, Cylas formicarius
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aOkinawa Prefectural Plant Protection Center, Japan
bRyukyu Sankei Co. Ltd, Japan
Although there have been numerous studies on the effects of mating history on mating behaviour, few studies have reported the relationship between mating history and other contextual behaviours such as foraging and predator avoidance. We examined the effect of mating history on death-feigning behaviour (an antipredator behaviour) in the sweetpotato weevil. Because mating behaviour can be divided into phases, we examined the effects of encounters with the opposite sex, copulation and insemination success on death-feigning behaviour. For females after copulation and males after multiple copulations the duration of death-feigning behaviour was reduced, whereas encounters with the opposite sex had no effect. Insemination success did not affect the duration of death feigning in males, but inseminated females reduced the duration of death feigning. We discuss the implications of these results for the effect of mating history on this antipredator behaviour.
Animal BehaviourVolume 78, Issue 5, November 2009, Pages 1145-1151
- Differences in mate location behaviours between residents and nonresidents in a territorial butterfly
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aDepartment of Zoology, Stockholm University, Sweden
Mate location strategies vary between species. Among butterflies two strategies are recognized: ‘patrolling’ males spend their life on the wing searching for females and ‘perching’ males stay at a specific site waiting to intercept passing females. In the speckled wood butterfly, Pararge aegeria, two alternative male strategies have been described: dominant males adopt a perching strategy monopolizing large sunspots on the forest floor, and subdominant males adopt a patrolling strategy. However, comparative analyses have shown that body design differs between perching and patrolling species, hence constraining opportunity for within-species variation in mate location strategy. We tested whether males differ in their propensity to adopt perching or patrolling behaviour by recording time spent flying during 30 min when alone in a large cage with only one large sunspot and many smaller ones, and whether subdominant males adopt a patrolling strategy by allowing dyads of males to interact in the cage for 60 min and recording the same behaviours again. All males adopted perching behaviour when alone, and subdominant males in dyads spent only a short time in extended flights after losing contests over territory ownership, soon returning to a perching strategy and making the best of a bad job from the vantage point of a small sunspot. We argue that previous descriptions of subdominant male P. aegeria adopting a patrolling strategy are based on too short observation periods, and have mistaken males in temporary transit for males adopting patrolling behaviour.
Animal BehaviourVolume 78, Issue 5, November 2009, Pages 1161-1167
- Mechanism of host recognition in Neodohrniphora elongata (Brown) (Diptera: Phoridae)
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aUniversidade Estadual do Norte Fluminense, Brazil
Insects can use different cues derived from their host or habitat to localize and identify an appropriate host. We conducted this study to investigate the mechanisms used by Neodohrniphora elongata (Brown) to localize and recognize the host Atta sexdens rubropilosa Forel. Females of the parasitoid N. elongata were collected in the field and tested individually in an observation box. The effect of chemical and visual stimuli, associated with A. sexdens rubropilosa, on the location and acceptance behaviour of N. elongata was verified. The chemical stimuli of the ant workers alone triggered no behavioural response in the phorid. Visual stimuli of the ant were sufficient to trigger behavioural acts related to host localization and recognition in the phorids. The trail pheromone of A. sexdens rubropilosa associated with host visualization increased the total time of inspection of a potential host. Visual cues in motion increased the inspection period, compared to static visual cues. Moving basic morphological configurations, regardless of the degree of complexity, triggered similar inspection behaviour as that observed towards live hosts in N. elongata. The phorids, however, did not identify these incomplete morphological models as hosts when static.
Animal BehaviourVolume 78, Issue 5, November 2009, Pages 1177-1182
- Honeybee, Apis mellifera, guards use adaptive acceptance thresholds to limit worker reproductive parasitism
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aBehaviour and Genetics of Social Insects Laboratory, School of Biological Sciences A12, University of Sydney, Australia
To protect their colonies from robbing by conspecifics, honeybees have evolved nest-guarding behaviour. Guards adjust their acceptance threshold so that, as the likelihood of robbing increases, fewer non-nestmates are admitted. In addition to the possibility of robbing, queenless colonies may be infiltrated by reproductively parasitic non-nestmates. We tested the hypothesis that queenless colonies would be more discriminatory of non-nestmates than queenright colonies. As predicted, queenless colonies accepted significantly fewer non-nestmates (from queenright colonies) than they did nestmates, whereas queenright colonies did not differentiate significantly between the two sources. This trend continued once laying workers became active in queenless colonies. Thus there is evidence that queenless colonies are more discerning against potential reproductive parasites than queenright colonies. We also tested the hypothesis that as the likelihood of an intruder being a reproductive parasite increased, guards would become less permissive of allowing it entrance to the colony. Queenright colonies accepted significantly more non-nestmates from queenright colonies (no active ovaries) than they did non-nestmates from queenless colonies (many with active ovaries). However, queenless colonies did not make this distinction. We suggest that to queenless colonies all non-nestmates are potential parasites.
Animal BehaviourVolume 78, Issue 5, November 2009, Pages 1205-1211
- Male eyespan and resource ownership affect contest outcome in the stalk-eyed fly, Teleopsis dalmanni
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aThe Galton Laboratory, Department of Genetics, Evolution & Environment, University College London, U.K.
bCoMPLEX, University College London, U.K.
The dominant theory for the evolution of male sexual ornaments is that they act as signals of male quality used by females in their mate choice. But these traits may also be used in male–male competition. In stalk-eyed flies, male eyespan (the distance between the eyes) is already known to play an important role in female mate choice. We investigated the influence of eyespan on male aggression over control of lek mating sites, both under controlled conditions and from field observations. Eyespan positively affected the number of aggressive encounters between two males on a lek. There were more aggressive interactions between large-eyespan males compared with small-eyespan males, and large-eyespan males won proportionately more aggressive interactions. Lek site ownership also influenced the outcome of aggression but to a smaller degree than eyespan. In addition, higher resource value, the number of females on a lek, increased the chance of aggression. The outcome of aggression between males is the control of lek aggregation sites, and this had direct consequences for male reproductive success, as lek owners gained more matings at both dusk and dawn. The importance of male–male competition in shaping sexual selection in stalk-eyed flies is discussed.
Animal BehaviourVolume 78, Issue 5, November 2009, Pages 1213-1220
- Female preference and fitness benefits of mate choice in a species with dissociated sperm transfer
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aDepartment of Evolutionary Biology, University of Siena, Italy
bDepartment of Animal Ecology, VU University Amsterdam, The Netherlands
Female mate preference can have important fitness consequences for females through direct or indirect benefits of mate choice. However, the existence and benefits of mate choice in species that perform dissociated sperm transfer is largely unknown. In the springtail Orchesella cincta, receptive females locate and take up spermatophores deposited in the litter layer by males, without even meeting their partner. We investigated female sexual selection and its benefits in O. cincta. We performed female choice trials with manipulated spermatophore density and diversity to assess female preference for different spermatophore deposition patterns. Furthermore we tested whether females benefit from choosing between spermatophores by measuring several reproductive variables of females assigned to single male (no choice) and double male (choice) mating treatments. Our results show that females chose patches with four spermatophores over patches with a single spermatophore, but did not discriminate between patches of three spermatophores from a single male or from three different males. The mating experiment showed that O. cincta females gained indirect benefits from choosing between spermatophores of different males, because male offspring resulting from the double male treatment produced more spermatophores than the male offspring from females without a choice. No evidence was found for direct benefits of female choice, because there were no differences in clutch size, egg size or offspring survival between treatments. Despite the large number of studies on female mate choice, this is the first time that indirect benefits have been demonstrated in a species with dissociated sperm transfer.
Animal BehaviourVolume 78, Issue 5, November 2009, Pages 1261-1267
Insect Biocontrol
- Regulation of the seasonal population patterns of Helicoverpa armigera moths by Bt cotton planting
Yu-lin Gao1, Hong-qiang Feng2 and Kong-ming Wu1 kmwu@ippcaas.cn
1. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, 100193 Beijing, People’s Republic of China
2. Institute of Plant Protection, Henan Academy of Agricultural Sciences, Zhengzhou, 450002, People’s Republic of China
Transgenic cotton expressing the Bacillus thuringiensis (Bt) Cry1Ac toxin has been commercially cultivated in China since 1997, and by 2000 Bt cotton had almost completely replaced non-transgenic cotton cultivars. To evaluate the impact of Bt cotton planting on the seasonal population patterns of cotton bollworm, Helicoverpa armigera, the dynamics of H. armigera moths were monitored with light traps from four locations (Xiajin, Linqing and Dingtao of Shandong Province; Guantao of Hebei Province) in high Bt density region and five locations (Anci and Xinji of Hebei Province; Dancheng and Fengqiu of Henan Province; Gaomi of Shandong Province) in low Bt density region from 1996 to 2008. A negative correlation was found between moth densities of H. armigera and the planting years of Bt cotton in both high and low Bt density areas. These data indicate that the moth population density of H. armigera was reduced with the introduction of Bt cotton in northern China. Three generations of moths occurred between early June and late September in the cotton regions. Interestingly, second-generation moths decreased and seemed to vanish in recent years in high Bt density region, but this tendency was not found in low Bt density region. The data suggest that the planting of Bt cotton in high Bt density region was effective in controlling the population density of second-generation moths. Furthermore, the seasonal change of moth patterns associated with Bt cotton planting may regulate the regional occurrence and population development of this migratory insect.
Transgenic Research，online: 22 October 2009 10.1007/s11248-009-9337-1
Insect Chemoreception
- Acute olfactory response of Culex mosquitoes to a human- and bird-derived attractant
Department of Entomology, Honorary Maeda-Duffey Laboratory, University of California, Davis, CA 95616
West Nile virus, which is transmitted by Culex mosquitoes while feeding on birds and humans, has emerged as the dominant vector borne disease in North America. We have identified natural compounds from humans and birds, which are detected with extreme sensitivity by olfactory receptor neurons (ORNs) on the antennae of Culex pipiens quinquefasciatus (Cx. quinquefasciatus). One of these semiochemicals, nonanal, dominates the odorant spectrum of pigeons, chickens, and humans from various ethnic backgrounds. We determined the specificity and sensitivity of all ORN types housed in different sensilla types on Cx. quinquefasciatus antennae. Here, we present a comprehensive map of all antennal ORNs coding natural ligands and their dose-response functions. Nonanal is detected by a large array of sensilla and is by far the most potent stimulus; thus, supporting the assumption that Cx. quinquefasciatus can smell humans and birds. Nonanal and CO2 synergize, thus, leading to significantly higher catches of Culex mosquitoes in traps baited with binary than in those with individual lures.
PNAS 2009 106: 18803-18808
13.A Drosophila Gustatory Receptor Essential for Aversive Taste and Inhibiting Male-to-Male Courtship
1. Departments of Biological Chemistry and Neuroscience, Center for Sensory Biology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
2. Department of Oral Biology, Brain Korea 21 Project, Yonsei University College of Dentistry, 250 Seongsanno Seodaemun-gu, Seoul 120-752, Korea
Contact chemosensation is required for several behaviors that promote insect survival. These include evasive behaviors such as suppression of feeding on repellent compounds, known as antifeedants, and inhibition of male-to-male courtship. However, the gustatory receptors (GRs) required for responding to nonvolatile avoidance chemicals are largely unknown. Exceptions include Drosophila GR66a and GR93a, which are required to prevent ingestion of caffeine [1,2], and GR32a, which is necessary for inhibiting male-to-male courtship [3]. However, GR32a is dispensable for normal taste. Thus, distinct GRs may function in sensing avoidance pheromones and antifeedants. Here, we describe the requirements for GR33a, which is expressed widely in gustatory receptor neurons (GRNs) that respond to aversive chemicals. Gr33a mutant flies were impaired in avoiding all nonvolatile repellents tested, ranging from quinine to denatonium, lobeline, and caffeine. Gr33a mutant males also displayed increased male-to-male courtship, implying that it functioned in the detection of a repulsive male pheromone. In contrast to the broadly required olfactory receptor (OR) OR83b, which is essential for trafficking other ORs [4], GR66a and GR93a are localized normally in Gr33a mutant GRNs. Thus, rather than regulating GR trafficking, GR33a may be a coreceptor required for sensing all nonvolatile repulsive chemicals, including tastants and pheromones.
Current Biology, Volume 19, Issue 19, 1623-1627, 17 September 2009
- Neural correlates of behavior in the moth Manduca sexta in response to complex odors
Jeffrey A. Riffell1, H. Lei and John G. Hildebrand1 jeffr@neurobio.arizona.edu or jgh@neurobio.arizona.edu
Department of Neuroscience, University of Arizona, Tucson AZ 85721-0077
With Manduca sexta as a model system, we analyzed how natural odor mixtures that are most effective in eliciting flight and foraging behaviors are encoded in the primary olfactory center in the brain, the antennal lobe. We used gas chromatography coupled with multiunit neural-ensemble recording to identify key odorants from flowers of two important nectar resources, the desert plants Datura wrightii and Agave palmeri, that elicited responses from individual antennal-lobe neurons. Neural-ensemble responses to the A. palmeri floral scent, comprising >60 odorants, could be reproduced by stimulation with a mixture of six of its constituents that had behavioral effectiveness equivalent to that of the complete scent. Likewise, a mixture of three floral volatiles from D. wrightii elicited normal flight and feeding behaviors. By recording responses of neural ensembles to mixtures of varying behavioral effectiveness, we analyzed the coding of behaviorally “meaningful” odors. We considered four possible ensemble-coding mechanisms—mean firing rate, mean instantaneous firing rate, pattern of synchronous ensemble firing, and total net synchrony of firing—and found that mean firing rate and the pattern of ensemble synchrony were best correlated with behavior (R = 41% and 43%, respectively). Stepwise regression analysis showed that net synchrony and mean instantaneous firing rate contributed little to the variation in the behavioral results. We conclude that a combination of mean-rate coding and synchrony of firing of antennal-lobe neurons underlies generalization among related, behaviorally effective floral mixtures while maintaining sufficient contrast for discrimination of distinct scents.
PNASNovember 17, 2009vol. 106 no. 46 19219-19226
Insect Clock
- Temperature Entrainment of Drosophila's Circadian Clock Involves the Gene nocte and Signaling from Peripheral Sensory Tissues to the Brain
Hana Sehadova1, 5, Franz T. Glaser2, 5, Carla Gentile1, 5, Alekos Simoni1, Astrid Giesecke1, 4, Joerg T. Albert3 and Ralf Stanewsky1, 2
4. Present address: MRC Laboratory of Molecular Biology, Structural Biology Division, Hills Road, Cambridge CB2 0QH, UK
5. These authors contributed equally to this work
Circadian clocks are synchronized by the natural day/night and temperature cycles. Our previous work demonstrated that synchronization by temperature is a tissue autonomous process, similar to synchronization by light. We show here that this is indeed the case, with the important exception of the brain. Using luciferase imaging we demonstrate that brain clock neurons depend on signals from peripheral tissues in order to be synchronized by temperature. Reducing the function of the gene nocte in chordotonal organs changes their structure and function and dramatically interferes with temperature synchronization of behavioral activity. Other mutants known to affect the function of these sensory organs also interfere with temperature synchronization, demonstrating the importance of nocte in this process and identifying the chordotonal organs as relevant sensory structures. Our work reveals surprising and important mechanistic differences between light- and temperature-synchronization and advances our understanding of how clock resetting is accomplished in nature.
Neuron, Volume 64, Issue 2, 251-266, 29 October 2009
Insect Development
- Combinatorial binding predicts spatio-temporal cis-regulatory activity
Robert P. Zinzen1,2, Charles Girardot1,2, Julien Gagneur1,2, Martina Braun1 & Eileen E. M. Furlong1 furlong@embl.de
1. European Molecular Biology Laboratory, D-69117 Heidelberg, Germany
2. These authors contributed equally to this work.
Development requires the establishment of precise patterns of gene expression, which are primarily controlled by transcription factors binding to cis-regulatory modules. Although transcription factor occupancy can now be identified at genome-wide scales, decoding this regulatory landscape remains a daunting challenge. Here we used a novel approach to predict spatio-temporal cis-regulatory activity based only on in vivo transcription factor binding and enhancer activity data. We generated a high-resolution atlas of cis-regulatory modules describing their temporal and combinatorial occupancy during Drosophila mesoderm development. The binding profiles of cis-regulatory modules with characterized expression were used to train support vector machines to predict five spatio-temporal expression patterns. In vivo transgenic reporter assays demonstrate the high accuracy of these predictions and reveal an unanticipated plasticity in transcription factor binding leading to similar expression. This data-driven approach does not require previous knowledge of transcription factor sequence affinity, function or expression, making it widely applicable.
Nature 2009 462: 65-70 http://www.nature.com/nature/journal/v462/n7269/abs/nature08531.html
- Autophagy, Not Apoptosis, Is Essential for Midgut Cell Death in Drosophila
Donna Denton1, Bhupendra Shravage2, Rachel Simin2, Kathryn Mills1, Deborah L. Berry3, Eric H. Baehrecke2 and Sharad Kumar1, 4,
1. Department of Haematology, Centre for Cancer Biology, SA Pathology, Frome Road, Adelaide, SA 5000, Australia
2. Department of Cancer Biology, University of Massachusetts Medical School, Worcester, MA 01605, USA
3. Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC 20010, USA
4. Department of Medicine, University of Adelaide, Adelaide, SA 5005, Australia
Most developmentally programmed cell death in metazoans is mediated by caspases. During Drosophila metamorphosis, obsolete tissues, including the midgut and salivary glands, are removed by programmed cell death [1]. The initiator caspase Dronc and its activator Ark are required for the death of salivary glands, but not for midgut removal [2,3]. In addition to caspases, complete removal of salivary glands requires autophagy [4]. However, the contribution of autophagy to midgut cell death has not been explored. Examination of combined mutants of the main initiator and effector caspases revealed that the canonical apoptotic pathway is not required for midgut cell death. Further analyses revealed that the caspase Decay is responsible for most of the caspase activity in dying midguts, yet inhibition of this activity has no effect on midgut removal. By contrast, midgut degradation was severely delayed by inhibition of autophagy, and this occurred without a decrease in caspase activity. Surprisingly, the combined inhibition of caspases and autophagy did not result in an additional delay in midgut removal. Together, our results indicate that autophagy, not caspases, is essential for midgut programmed cell death, providing the first in vivo evidence of caspase-independent programmed cell death that requires autophagy despite the presence of high caspase activity.
Current Biology, Volume 19, Issue 20, 1741-1746, 08 October 2009
Insect Ecology
- Shape transition during nest digging in ants
Etienne Toffina, , David Di Paoloa, Alexandre Campob, Claire Detraina and Jean-Louis Deneubourga etoffin@ulb.ac.be
a. Service d'Écologie Sociale, CP231, Université Libre de Bruxelles, Plaine Campus, Boulevard du Triomphe, 1050 Brussels, Belgium
b. Institut de Recherches Interdisciplinaires et de Développement en Intelligence Artificielle, Computer and Decision Engineering, CP194/6, Université Libre de Bruxelles, 50 Avenue Franklin Roosevelt, 1050 Brussels, Belgium
Nest building in social insects is among the collective processes that show highly conservative features such as basic modules (chambers and galleries) or homeostatic properties. Although ant nests share common characteristics, they exhibit a high structural variability, of which morphogenesis and underlying mechanisms remain largely unknown. We conducted two-dimensional nest-digging experiments under homogeneous laboratory conditions to investigate the shape diversity that emerges only from digging dynamics and without the influence of any environmental heterogeneity. These experiments revealed that, during the excavation, a morphological transition occurs because the primary circular cavity evolves into a ramified structure through a branching process. Such a transition is observed, whatever the number of ants involved, but occurs more frequently for a larger number of workers. A stochastic model highlights the central role of density effects in shape transition. These results indicate that nest digging shares similar properties with various physical, chemical, and biological systems. Moreover, our model of morphogenesis provides an explanatory framework for shape transitions in decentralized growing structures in group-living animals.
PNAS 2009 106:18616-18620
- Chemical niche differentiation among sympatric species of orchid bees
Yvonne Zimmermann1, Santiago R. Ramírez2, and Thomas Eltz1 eltz@uni-duesseldorf.de
1. Department of Neurobiology, Sensory Ecology Group, University of Düsseldorf, Universitätstr. 1, 40225 Düsseldorf, Germany
2. Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138 USA
Male Neotropical orchid bees (Euglossini) collect volatile substances (fragrances) from flowers and other sources (e.g., decaying wood) and store them in specialized hind tibial pockets. The accumulated chemicals are later emitted during courtship display, presumably to lure conspecific females for mating. We analyzed tibial fragrances of males of 15 sympatric Panamanian species in the genus Euglossa to test whether communities of euglossine bees are chemically structured, and to elucidate whether male fragrance signals evolve to convey premating isolation. Our analysis revealed substantial chemical disparity among all lineages. Disparity was mediated by compounds that were exclusive to certain species but also by differences in relative quantity of shared compounds. We mapped tibial fragrance compounds present in each species on a DNA-based phylogeny (reconstructed using partial sequences of COI, EF1-α, ArgK, and Pol-II) and found that most dominant compounds were highly homoplasious. In an analysis of chemical differentiation in relation to phylogenetic divergence through time, disparity was greater than expected from a null model at any point during evolutionary history, suggesting that diversifying selection has shaped fragrance phenotypes. Notably, chemical disparity was greater within recently diverged lineages than among them, suggesting that chemical preferences in orchid bees evolved rapidly in the early stages of species divergence. We postulate communication interference as the possible mechanism behind the observed fragrance differentiation, which may be the product of reproductive character (fragrance) displacement. Our findings are consistent with the hypothesis that male fragrance signals evolve to convey premating isolation.
Ecology: 2009 Vol. 90, No. 11, pp. 2994-3008.
- Ecologically dependent postmating isolation between sympatric host forms of Neochlamisus bebbianae leaf beetles
Ecological speciation is the promotion of reproductive isolation via the divergent adaptation of populations to alternative environments. A prediction peculiar to ecological speciation is that hybrids between such populations should be adapted poorly to parental environments, yielding reduced fitness and postmating isolation. However, F1 analyses alone cannot demonstrate that ecological (“extrinsic”) factors contribute to such isolation. Rather, this requires documenting a “switch” in the relative fitnesses of reciprocal backcrosses between environments. Specifically, each backcross should exhibit higher fitness in the environment of its pure parent, with which it shares the most genes, including environment-specific ones. In contrast, because genetic proportions are expected to be similar for all backcrosses (≈¾ from one parental type and ≈¼ from the other), the more general genetic incompatibilities responsible for “intrinsic” isolation predict no such environment-specific fitness switches. Thus, although intrinsic isolation may contribute to the fitness reduction and variation underlying such patterns, it offers an insufficient explanation for them. Here, we present a quantitative genetic “backcross” analysis of sympatric Neochlamisus bebbianae leaf beetle populations adapted to maple versus willow host plants. Results statistically supported ecological speciation predictions, notably the switch in relative fitness for backcross types, the expected rank order of cross type fitnesses, and appreciable extrinsic isolation. We additionally documented genetic variation in host-associated fitness, ruled out nongenetic maternal effects, and discuss the maintenance of ecological differentiation in sympatry. In summary, our study provides a rare and strongly supported demonstration of genetically based, ecologically dependent postmating isolation during ecological speciation.
PNASNovember 17, 2009vol. 106 no. 46 19426-19431
- High Symbiont Relatedness Stabilizes Mutualistic Cooperation in Fungus-Growing Termites
Duur K. Aanen,1,* Henrik H. de Fine Licht,2 Alfons J. M. Debets,1 Niels A. G.
Kerstes,1 Rolf F. Hoekstra,1 Jacobus J. Boomsma2 duur.aanen@wur.nl
1 Laboratory of Genetics, Wageningen University, 6700 AH Wageningen, Netherlands.
2 Centre for Social Evolution, Department of Biology, University of Copenhagen, 2100 Copenhagen, Denmark
2 Centre for Social Evolution, Department of Biology, University of Copenhagen, 2100 Copenhagen, Denmark
It is unclear how mutualistic relationships can be stable whenpartners disperse freely and have the possibility of formingassociations with many alternative genotypes. Theory predictsthat high symbiont relatedness should resolve this problem,but the mechanisms to enforce this have rarely been studied.We show that African fungus-growing termites propagate singlevariants of their Termitomyces symbiont, despite initiatingcultures from genetically variable spores from the habitat.High inoculation density in the substrate followed by fusionamong clonally related mycelia enhances the efficiency of sporeproduction in proportion to strain frequency. This positivereinforcement results in an exclusive lifetime association ofeach host colony with a single fungal symbiont and hinders theevolution of cheating. Our findings explain why vertical symbionttransmission in fungus-growing termites is rare and evolutionarilyderived.
Science 20 November 2009 Vol. 326. no. 5956, pp. 1103 - 1106
22.Rapidly Shifting Sex Ratio across a Species Range
1. School of Biological Sciences, University of Liverpool, Liverpool L69 7ZB, UK
2. Laboratoire de Biometrie et Biologie Evolutive, University of Lyon 1, 69622 Villeurbanne, France
3. School of Biosciences, University of Exeter, Cornwall Campus, Penryn TR10 9EZ, UK
4. Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK
Sex ratios are subject to distortion by a range of inherited parasites [1]. Although it has been predicted that the presence of these elements will result in spatial and temporal variation in host sex ratio [2,3,4], testing of this hypothesis has been constrained by availability of historical data. We here determine spatial and temporal variation in sex ratio in a interaction between a butterfly and male-killing Wolbachia bacteria [5] by assaying infection presence in museum specimens, and from this inferring infection prevalence and phenotype in historical populations. Comparison of contemporary and museum samples revealed profound change in four of five populations examined. Two populations become extremely female biased, associated with spread of the male-killer bacterium. One evolved from extremely female biased to a sex ratio near parity, resulting from the infection losing male-killing activity. The final population fluctuated widely in sex ratio, associated with varying frequency of the male killer. We conclude that asynchronous invasion and decline of sex-ratio distorters combines with the evolution of host suppressors to produce a rapidly changing mosaic of sex ratio. As a consequence, the reproductive ecology of the host species is likely to be fundamentally altered over short time scales [6]. Further, the study demonstrates the utility of museum specimens as “silent witnesses” of evolutionary change.
Current Biology, Volume 19, Issue 19, 1628-1631, 10 September 2009
Insect Evolution
- Caterpillars evolved from onychophorans by hybridogenesis
I reject the Darwinian assumption that larvae and their adults evolved from a single common ancestor. Rather I posit that, in animals that metamorphose, the basic types of larvae originated as adults of different lineages, i.e., larvae were transferred when, through hybridization, their genomes were acquired by distantly related animals. “Caterpillars,” the name for eruciforms with thoracic and abdominal legs, are larvae of lepidopterans, hymenopterans, and mecopterans (scorpionflies). Grubs and maggots, including the larvae of beetles, bees, and flies, evolved from caterpillars by loss of legs. Caterpillar larval organs are dismantled and reconstructed in the pupal phase. Such indirect developmental patterns (metamorphoses) did not originate solely by accumulation of random mutations followed by natural selection; rather they are fully consistent with my concept of evolution by hybridogenesis. Members of the phylum Onychophora (velvet worms) are proposed as the evolutionary source of caterpillars and their grub or maggot descendants. I present a molecular biological research proposal to test my thesis. By my hypothesis 2 recognizable sets of genes are detectable in the genomes of all insects with caterpillar grub- or maggot-like larvae: (i) onychophoran genes that code for proteins determining larval morphology/physiology and (ii) sequentially expressed insect genes that code for adult proteins. The genomes of insects and other animals that, by contrast, entirely lack larvae comprise recognizable sets of genes from single animal common ancestors.
PNASNovember 24, 2009vol. 106 no. 47 19901-19905
- Caterpillars did not evolve from onychophorans by hybridogenesis
bCollege of Biological Sciences and Center for Population Biology, University of California, Davis, CA 95616
The evolution and loss of distinctive larval forms in animal life cycles have produced complex patterns of similarity and difference among life-history stages and major animal lineages. One example of this similarity is the morphological forms of Onychophora (velvet worms) and the caterpillar-like larvae of some insects. Williamson [(2009) Proc Natl Acad Sci USA 106:15786–15790] has made the astonishing and unfounded claim that the ancestors of the velvet worms directly gave rise to insect caterpillars via hybridization and that evidence of this ancient “larval transfer” could be found in comparisons among the genomes of extant onychophorans, insects with larvae, and insects without larvae. Williamson has made a series of predictions arising from his hypothesis and urged genomicists to test them. Here, we use data already in the literature to show these predictions to be false. Hybridogenesis between distantly related animals does not explain patterns of morphological and life-history evolution in general, and the genes and genomes of animals provide strong evidence against hybridization or larval transfer between a velvet worm and an insect in particular.
PNAS November 24, 2009 vol. 106 no. 4719906-19909
Insect Genetics
- Polymorphic Butterfly Reveals the Missing Link in Ecological Speciation
Nicola L. Chamberlain,1,* Ryan I. Hill,1,* Durrell D. Kapan,2 Lawrence E. Gilbert,3 Marcus R. Kronforst1, mkronforst@cgr.harvard.edu
1. Faculty of Arts and Sciences Center for Systems Biology, Harvard University, Cambridge, MA 02138, USA.
2. Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI 96822, USA.
3. Section of Integrative Biology, University of Texas, Austin, TX 78712, USA.
Ecological speciation occurs when ecologically based, divergent selection causes the evolution of reproductive isolation. There are many empirical examples of this process; however, there exists a poorly characterized stage during which the traits that distinguish species ecologically and reproductively segregate in a single population. By using a combination of genetic mapping, mate-choice experiments, field observations, and population genetics, we studied a butterfly population with a mimetic wing color polymorphism and found that the butterflies exhibited partial, color-based, assortative mate preference. These traits represent the divergent, ecologically based signal and preference components of sexual isolation that usually distinguish incipient and sibling species. The association between behavior and recognition trait in a single population may enhance the probability of speciation and provides an example of the missing link between an interbreeding population and isolated species.
Science 2009 326: 847 – 850
26.Homology of Dipteran Bristles and Lepidopteran Scales: Requirement for the Bombyx mori achaete-scute Homologue ASH2
Qingxiang Zhou*,, Linlin Yu*, Xingjia Shen, Yinü Li*, Weihua Xu, Yongzhu Yiand Zhifang Zhang*,1 zhifangzhang@yahoo.com
* The Biotechnology Research Institute, National Engineering of Crop Germplasm and Genetic Improvement, Chinese Academy of Agricultural Sciences, Beijing 100081, China
The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang City, Jiangsu Province 212018, China
State Key Laboratory for Biocontrol and Institute of Entomology, School of Life Sciences, Sun Yat-Sen University, Guangzhou
Lepidopteran wing scales and Drosophila bristles are consideredhomologous structures on the basis of the similarities in theircell lineages. However, the molecular mechanisms underlyingscale development are essentially unknown as analysis of genefunction in Lepidoptera is sorely limited. In this study, weused the Bombyx mori mutant scaleless (sl), which displays anearly complete loss of wing scales, to explore the mechanismof lepidopteran wing-scale formation. We found that Bm-ASH2,one of four Bombyx achaete-scute homologs, is highly expressedin early pupal wings of wild-type silkworms, but its expressionis severely reduced in sl pupal wings. Through molecular characterizationof the mutant locus using luciferase and gel shift assays, geneticanalysis of recombining populations, and in vivo rescue experiments,we provide evidence that a 26-bp deletion within the Bm-ASH2promoter is closely linked to the sl locus and leads to lossof Bm-ASH2 expression and the scaleless-wings phenotype. Thus,the Bm-ASH2 appears to play a critical role in scale formationin B. mori. This finding supports the proposed homology of lepidopteranscales and dipteran bristles and provides evidence for conservationof the genetic pathway in scale/bristle development at the levelof gene function.
Genetics, Vol. 183, 619-627, October 2009
27.Imprinting of the Y Chromosome Influences Dosage Compensation in roX1 roX2 Drosophila melanogaster
Debashish U. Menon and Victoria H. Meller1 vmeller@biology.biosci.wayne.edu
Department of Biological Sciences, Wayne State University, Detroit, Michigan 48202
Drosophila melanogaster males have a well-characterized regulatorysystem that increases X-linked gene expression. This essentialprocess restores the balance between X-linked and autosomalgene products in males. A complex composed of the male-specificlethal (MSL) proteins and RNA is recruited to the body of transcribedX-linked genes where it modifies chromatin to increase expression.The RNA components of this complex, roX1 and roX2 (RNA on theX1, RNA on the X2), are functionally redundant. Males mutatedfor both roX genes have dramatically reduced survival. We showthat reversal of sex chromosome inheritance suppresses lethalityin roX1 roX2 males. Genetic tests indicate that the effect onmale survival depends upon the presence and source of the Ychromosome, revealing a germ line imprint that influences dosagecompensation. Conventional paternal transmission of the Y chromosomeenhances roX1 roX2 lethality, while maternal transmission ofthe Y chromosome suppresses lethality. roX1 roX2 males withboth maternal and paternal Y chromosomes have very low survival,indicating dominance of the paternal imprint. In an otherwisewild-type male, the Y chromosome does not appreciably affectdosage compensation. The influence of the Y chromosome, clearlyapparent in roX1 roX2 mutants, thus requires a sensitized geneticbackground. We believe that the Y chromosome is likely to actthrough modulation of a process that is defective in roX1 roX2mutants: X chromosome recognition or chromatin modificationby the MSL complex.
Genetics, Vol. 183, 811-820, November 2009
28.Evolution of Sex-Dependent Gene Expression in Three Recently Diverged Species of Drosophila
Zi-Feng Jiang and Carlos A. Machado1 machado@umd.edu
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721 and Department of Biology, University of Maryland, College Park, Maryland 20742
Sexual dimorphism in morphological, physiological, and behavioraltraits is pervasive in animals, as is the observation of strongsexual dimorphism in genomewide patterns of gene expressionin the few species where this has been studied. Studies of transcriptomedivergence show that most interspecific transcriptional divergenceis highly sex dependent, an observation consistent with theaction of sex-dependent natural selection during species divergence.However, few transcriptome evolution studies have been conductedbetween recently diverged species (<1 MY). Here, we presentanalyses of sex-biased transcriptome divergence in sexuallymature adults of three recently diverged species of Drosophila:Drosophila pseudoobscura, D. persimilis, and D. pseudoobscurabogotana. Data were collected using a custom designed Agilentoligonucleotide. Expression was detected in 12,507 genes. About80% of the expressed genes show sex-biased expression in eachspecies. Across species, 21% of the transcriptome shows switchesbetween nonsex bias and sex bias, and just 0.9% of the transcriptomeshows reversals of sex-biased expression. Over 80% of the expressiondivergence between species is due to changes in one sex only.About 15% of the expression divergence between species is dueto changes in the same direction in both sexes and just 2% isdue to changes in both sexes but in opposite directions. Inagreement with previous studies, we observe a high level ofsex-dependent transcriptome divergence and strong demasculinizationof the two arms of the X chromosome in all species. However,in contrast to previous studies we find that male-biased genesdo not have higher levels of expression divergence than non-sex-biasedgenes, and sex-biased genes show higher levels of expressiondivergence in the alternate sex, suggesting that sex-biasedgenes endure stronger selection when expressed in the alternatesex.
Genetics, Vol. 183, 1175-1185, November 2009
29.Removal of the Bloom Syndrome DNA Helicase Extends the Utility of Imprecise Transposon Excision for Making Null Mutations in Drosophila
* Department of Biology, Tufts University, Medford, Massachusetts 02155 and Program in Genetics, Tufts Sackler School of Graduate Biomedical Sciences, Boston, Massachusetts 02111
Transposable elements are frequently used in Drosophila melanogasterfor imprecise excision screens to delete genes of interest.However, these screens are highly variable in the number andsize of deletions that are recovered. Here, we show that conductingexcision screens in mus309 mutant flies that lack DmBlm, theDrosophila ortholog of the Bloom syndrome protein, increasesthe percentage and overall size of flanking deletions recoveredafter excision of either P or Minos elements.
Genetics, Vol. 183, 1187-1193, November 2009
30.A Gain-of-Function Screen Identifying Genes Required for Growth and Pattern Formation of the Drosophila melanogaster Wing
Cristina Cruz, Alvaro Glavic1, Mar Casado and Jose F. de Celis2 jfdecelis@cbm.uam.es
Centro de Biología Molecular "Severo Ochoa" (CBMSO), Consejo Superior de Investigaciones Científicas and Universidad Autónoma de Madrid, Cantoblanco, Madrid 28049, Spain
The Drosophila melanogaster wing is a model system for analyzingthe genetic control of organ size, shape, and pattern formation.The formation of the wing involves a variety of processes, suchas cell growth, proliferation, pattern formation, and differentiation.These developmental processes are under genetic control, andmany genes participating in specific aspects of wing developmenthave already being characterized. In this work, we aim to identifynovel genes regulating wing growth and patterning. To this end,we have carried out a gain-of-function screen generating novelP-UAS (upstream activating sequences) insertions allowing forcedgene expression. We produced 3340 novel P-UAS insertions andisolated 300 that cause a variety of wing phenotypes in combinationwith a Gal4 driver expressed exclusively in the central domainof the presumptive wing blade. The mapping of these P-UAS insertionsites allowed us to identify the gene that causes the gain-of-functionphenotypes. We show that a fraction of these phenotypes arerelated to the induction of cell death in the domain of ectopicgene expression. Finally, we present a preliminary characterizationof a gene identified in the screen, the function of which isrequired for the development of the L5 longitudinal vein.
Genetics, Vol. 183, 1005-1026, November 2009
Insect Memory
31.Social Facilitation of Long-Lasting Memory Retrieval in Drosophila
1. Genes and Dynamics of Memory Systems, Neurobiology Unit, Centre National de la Recherche Scientifique, École Supérieure de Physique et de Chimie Industrielles, 10 rue Vauquelin, 75005 Paris, France
2. Développement, Evolution, et Plasticité du Système Nerveux, Centre National de la Recherche Scientifique, 1 Avenue de la Terrasse, 91198 Gif-sur-Yvette Cedex, France
3. Institut National de la Recherche Agronomique Centre de Versailles-Grignon, UMR 1272, Physiologie de l'Insecte Signalisation et Communication, Route de St Cyr, 78026 Versailles Cedex, France
4. Present address: Institut de Recherche pour la Développement, UR 072, Laboratoire Evolution, Génomes, et Spéciation, UPR 9034, Centre National de la Recherche Scientifique, 1 Avenue de la Terrasse, 91198 Gif-sur-Yvette Cedex, France
5. These authors contributed equally to the work.
Recent studies demonstrate that social interactions can have a profound influence on Drosophila melanogaster behavior [1,2,3,4,5,6,7,8] and cuticular pheromone patterns [8,9,10]. Olfactory memory performance has mostly been investigated in groups, and previous studies have reported that grouped flies do not interact with each other and behave in the same way as individual flies during short-term memory retrieval [11,12,13]. However, the influence of social effects on the two known forms of Drosophila long-lasting associative memory, anesthesia-resistant memory (ARM) and long-term memory (LTM), has never been reported. We show here that ARM is displayed by individual flies but is socially facilitated; flies trained for ARM interact within a group to improve their conditioned performance. In contrast, testing shows LTM improvement in individual flies rather than in a group. We show that the social facilitation of ARM during group testing is independent of the social context of training and does not involve nonspecific aggregation. Furthermore, we demonstrate that social interactions facilitate ARM retrieval. We also show that social interactions necessary for this facilitation are specifically generated by trained flies: when single flies trained for ARM are mixed with groups of naive flies, they display poor retrieval, whereas mixing with groups trained either for ARM or LTM enhances performance.
Current Biology, Volume 19, Issue 19, 1654-1659, 24 September 2009
Insect Molecular Biology
- Extension of Drosophila Life Span by RNAi of the Mitochondrial Respiratory Chain
Jeffrey M. Copeland1, Jaehyoung Cho1, Thomas Lo1, Jae H. Hur1, Sepehr Bahadorani1, Tagui Arabyan1, Jason Rabie1, Jennifer Soh1 and David W. Walker1, 2
1. Department of Physiological Science, University of California, Los Angeles, Los Angeles, CA 90095, USA
2. Molecular Biology Institute, University of California, Los Angeles, Los Angeles, CA 90095, USA
Mitochondria have long been proposed to play an important role in the aging process. In the nematode Caenorhabditis elegans, genes important for mitochondrial electron transport chain (ETC) function stand out as a principal group of genes affecting life span. However, it has been suggested that this may be a peculiarity of nematode biology. In the present study, we have used an in vivo RNA interference (RNAi) strategy to inactivate ETC genes in Drosophila melanogaster and examine the impact on longevity. Here, we report that RNAi of five genes encoding components of mitochondrial respiratory complexes I, III, IV, and V leads to increased life span in flies. Long-lived flies with reduced expression of ETC genes do not consistently show reduced assembly of respiratory complexes or reduced ATP levels. In addition, extended longevity is not consistently correlated with reduced fertility or increased resistance to the free-radical generator paraquat. Targeted RNAi of two complex I genes in adult tissues or in neurons alone is sufficient to extend life span. Our data suggest that the role of mitochondrial ETC function in modulating animal aging is evolutionarily conserved and might also operate in humans. Furthermore, our findings suggest that the longer life span of flies with reduced ETC gene expression cannot simply be attributed to reduced energy production leading to decreased “rate of living.”
Current Biology, Volume 19, Issue 19, 1591-1598, 10 September 2009
33. Neprilysin 4, a novel endopeptidase from Drosophila melanogaster, displays distinct substrate specificities and exceptional solubility states
Heiko Meyer1, Mareike Panz1, Monika Zmojdzian2, Krzysztof Jagla2 and Achim Paululat1,*paululat@biologie.uni-osnabrueck.de
1. Department of Zoology/Developmental Biology, University of Osnabrück, Barbarastraße 11, 49069 Osnabrück, Germany
2. Unité Mixte de Recherche, CNRS 6247-GreD, Clermont-Ferrand University, INSERM Clermont-Ferrand, 28 Place Henri Dunant, F-63000 Clermont-Ferrand, France
Proteins belonging to the family of neprilysins are typicallymembrane bound M13 endopeptidases responsible for the inactivationand/or activation of peptide ignalling events on cell surfaces.Mammalian neprilysins are known to be involved in the metabolismof various regulatory peptides especially in the nervous, immune,cardiovascular and inflammatory systems. Although there is stillmuch to learn about their participation in various diseases,they are potential therapeutic targets. Here we report on theidentification and first characterization of neprilysin 4 (NEP4)from Drosophila melanogaster. Reporter lines as well as in situhybridization combined with immunolocalization demonstratedNEP4 expression during embryogenesis in pericardial cells, musclefounder cells, glia cells and male gonads. Western blot analysisconfirmed the prediction of one membrane bound and one soluble isoform,a finding quite unusual among neprilysins with presumably strong physiologicalrelevance. At least one NEP4 isoform was found in every developmentalstage indicating protein activities required throughout the wholelife cycle of Drosophila. Heterologously expressed NEP4 exhibitedsubstrate preferences comparable to human neprilysin 2 withdistinct cleavage of substance P and angiotensin I.
Journal of Experimental Biology 212, 3673-3683 (2009) October 30, 2009
http://jeb.biologists.org/cgi/content/abstract/212/22/3673
http://jeb.biologists.org/cgi/content/abstract/212/22/3673
- Transcriptional and Developmental Functions of the H3.3 Histone Variant in Drosophila
Akiko Sakai, Brian E. Schwartz, Sara Goldstein and Kami Ahmad,
Department of BCMP, Harvard Medical School, 240 Longwood Avenue, Boston, MA 02115, USA
Changes in chromatin composition accompany cellular differentiation in eukaryotes. Although bulk chromatin is duplicated during DNA replication, replication-independent (RI) nucleosome replacement occurs in transcriptionally active chromatin and during specific developmental transitions where the genome is repackaged [1,2]. In most animals, replacement uses the conserved H3.3 histone variant [3], but the functions of this variant have not been defined. Using mutations for the two H3.3 genes in Drosophila, we identify widespread transcriptional defects in H3.3-deficient animals. We show that mutant animals compensate for the lack of H3.3 in two ways: they upregulate the expression of the major histone H3 genes, and they maintain chromatin structure by using H3 protein for RI nucleosome replacement at active genes. Rescue experiments show that increased expression of H3 is sufficient to relieve transcriptional defects. In contrast, H3.3 is essential for male fertility, and germline cells specifically require the histone variant. Defects without H3.3 first occur around meiosis, resulting in a failure to condense, segregate, and reorganize chromatin. Rescue experiments with mutated transgenes demonstrate that H3.3-specific residues involved in RI nucleosome assembly—but not major histone modification sites—are required for male fertility. Our results imply that the H3.3 variant plays an essential role in chromatin transitions in the male germline.
Current Biology, Volume 19, Issue 21, 1816-1820, 24 September 2009
- Drosophila Dgt6 Interacts with Ndc80, Msps/XMAP215, and γ-Tubulin to Promote Kinetochore-Driven MT Formation
Elisabetta Bucciarelli1, 2, Claudia Pellacani1, 2, Valeria Naim1, 3, Antonella Palena1, Maurizio Gatti1 and Maria Patrizia Somma1,
Istituto Pasteur-Fondazione Cenci Bolognetti and Istituto di Biologia e Patologia Molecolari del Consiglio Nazionale delle Ricerche (CNR), Dipartimento di Genetica e Biologia Molecolare, Università di Roma “La Sapienza,” P.A. Moro 5, 00185 Roma, Italy
In centrosome-containing cells, spindle assembly relies on microtubules (MTs) nucleated from both centrosomes and chromosomes [1,2]. Recent work has suggested that additional spindle MTs can be nucleated by γ-tubulin ring complexes (γ-TuRCs) that associate laterally with preexisting spindle MTs, leading to spindle amplification. It has been proposed that in Drosophila S2 cells, γ-TuRCs are anchored to the spindle MTs by augmin, a multiprotein complex that contains at least eight subunits [3,4,5]. Here we show that the Dgt6 component of augmin is primarily required for kinetochore fiber (k-fiber) formation. An analysis of MT regrowth after cold exposure showed that formation of kinetochore-driven k-fibers is severely impaired in Dgt6-depleted cells. In control cells, these fibers are enriched in Dgt6, γ-tubulin, and Msps/XMAP215. Consistent with these results, Dgt6 coprecipitates with Msps, D-TACC, γ-tubulin, Ndc80, and Nuf2. However, RNA interference (RNAi)-mediated inhibition of γ-tubulin, Msps/XMAP215, or Ndc80/Hec1 reduced but did not abolish k-fiber regrowth. These results indicate that Dgt6 plays a pivotal role in kinetochore-driven k-fiber formation, mediating nucleation and/or initial stabilization of chromosome-induced MTs. We propose that Dgt6 binds and stabilizes nascent chromatin-induced MTs, facilitating their interaction with the Ndc80-Nuf2 complex. Dgt6 may also promote elongation of kinetochore-driven k-fibers through its interaction with γ-tubulin and Msps.
Current Biology, Volume 19, Issue 21, 1839-1845, 15 October 2009
- Assembly of Endogenous oskar mRNA Particles for Motor-Dependent Transport in the Drosophila Oocyte
1 Developmental Biology Unit, European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany
oskar mRNA localization at the oocyte posterior pole is essential for correct patterning of the Drosophila embryo. Here we show at the ultrastructural level that endogenous oskar ribonucleoprotein complexes (RNPs) assemble sequentially with initial recruitment of Hrp48 and the exon junction complex (EJC) to oskar transcripts in the nurse cell nuclei, and subsequent recruitment of Staufen and microtubule motors, following transport to the cytoplasm. oskar particles are non-membrane-bound structures that coalesce as they move from the oocyte anterior to the posterior pole. Our analysis uncovers a role for the EJC component Barentsz in recruiting Tropomyosin II (TmII) to oskar particles in the ooplasm and reveals that TmII is required for kinesin binding to the RNPs. Finally, we show that both kinesin and dynein associate with oskar particles and are the primary microtubule motors responsible for transport of the RNPs within the oocyte.
Cell, Volume 139, Issue 5, 983-998, 25 November 2009
Insect Neuroscience
- Reconstruction of virtual neural circuits in an insect brain
Shigehiro Namiki 1, 2, Shuichi S . Haupt 1, Tomoki Kazawa 1, Akira Takashima 1, Hidetoshi Ikeno 3 and Ryohei Kanzaki 1* kanzaki@rcast.u-tokyo.ac.jp
1. Research Center for Advanced Science and Technology, The University of Tokyo, Japan
2. School of Human Science and Environment, University of Hyogo, Japan
3. Graduate School of Life and Environmental Sciences, University of Tsukuba, Japan
The reconstruction of large-scale nervous systems represents a major scientific and engineering challenge in current neuroscience research that needs to be resolved in order to understand the emergent properties of such systems. We focus on insect nervous systems because they represent a good compromise between architectural simplicity and the ability to generate a rich behavioral repertoire. In insects, several sensory maps have been reconstructed so far. We provide an overview over this work including our reconstruction of population activity in the primary olfactory network, the antennal lobe. Our reconstruction approach, that also provides functional connectivity data, will be refined and extended to allow the building of larger scale neural circuits up to entire insect brains, from sensory input to motor output.
Front. Neurosci. 2009 3: 206-213
- Dynamics of Learning-Related cAMP Signaling and Stimulus Integration in the Drosophila Olfactory Pathway
1 Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA
2 Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, TX 77030, USA
3 W.M. Keck Center for Interdisciplinary Bioscience Training, Houston, TX 77005, USA
2 Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, TX 77030, USA
3 W.M. Keck Center for Interdisciplinary Bioscience Training, Houston, TX 77005, USA
Functional imaging with genetically encoded calcium and cAMP reporters was used to examine the signal integration underlying learning in Drosophila. Dopamine and octopamine modulated intracellular cAMP in spatially distinct patterns in mushroom body neurons. Pairing of neuronal depolarization with subsequent dopamine application revealed a synergistic increase in cAMP in the mushroom body lobes, which was dependent on the rutabaga adenylyl cyclase. This synergy was restricted to the axons of mushroom body neurons, and occurred only following forward pairing with time intervals similar to those required for behavioral conditioning. In contrast, forward pairing of neuronal depolarization and octopamine produced a subadditive effect on cAMP. Finally, elevating intracellular cAMP facilitated calcium transients in mushroom body neurons, suggesting that cAMP elevation is sufficient to induce presynaptic plasticity. These data suggest that rutabaga functions as a coincidence detector in an intact neuronal circuit, with dopamine and octopamine bidirectionally influencing the generation of cAMP.
Neuron, Volume 64, Issue 4, 510-521, 25 November 2009
- Two Different Forms of Arousal in Drosophila Are Oppositely Regulated by the Dopamine D1 Receptor Ortholog DopR via Distinct Neural Circuits
Tim Lebestky1, 3, Jung-Sook C. Chang1, 3, Heiko Dankert1, 2, Lihi Zelnik2, Young-Cho Kim4, Kyung-An Han4, Fred W. Wolf5, Pietro Perona2 and David J. Anderson1, 3
1 Division of Biology 216-76, California Institute of Technology, Pasadena, CA 91125, USA
2 Division of Engineering and Applied Science 136-93, California Institute of Technology, Pasadena, CA 91125, USA
3 Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125, USA
4 Department of Biology, The Huck Institute, Pennsylvania State University, University Park, PA 16802, USA
5 Ernest Gallo Clinic and Research Center, University of California, San Francisco, Emeryville, CA 94608, USA
2 Division of Engineering and Applied Science 136-93, California Institute of Technology, Pasadena, CA 91125, USA
3 Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125, USA
4 Department of Biology, The Huck Institute, Pennsylvania State University, University Park, PA 16802, USA
5 Ernest Gallo Clinic and Research Center, University of California, San Francisco, Emeryville, CA 94608, USA
Arousal is fundamental to many behaviors, but whether it is unitary or whether there are different types of behavior-specific arousal has not been clear. In Drosophila, dopamine promotes sleep-wake arousal. However, there is conflicting evidence regarding its influence on environmentally stimulated arousal. Here we show that loss-of-function mutations in the D1 dopamine receptor DopR enhance repetitive startle-induced arousal while decreasing sleep-wake arousal (i.e., increasing sleep). These two types of arousal are also inversely influenced by cocaine, whose effects in each case are opposite to, and abrogated by, the DopR mutation. Selective restoration of DopR function in the central complex rescues the enhanced stimulated arousal but not the increased sleep phenotype of DopR mutants. These data provide evidence for at least two different forms of arousal, which are independently regulated by dopamine in opposite directions, via distinct neural circuits.
Neuron, Volume 64, Issue 4, 522-536, 25 November 2009
Insect Nutrition
- Water- and nutrient-dependent effects of dietary restriction on Drosophila lifespan
William W. Jaa, Gil B. Carvalhoa, Brian M. Zida, Elizabeth M. Maka, Ted Brummelb and Seymour Benzera billja@its.caltech.edu
a. Division of Biology, California Institute of Technology, Pasadena, CA 91125
b. Department of Biology, Long Island University, Brookville, NY 11548
Dietary restriction (DR) is a widely conserved intervention leading to lifespan extension. Despite considerable effort, the mechanisms underlying DR remain poorly understood. In particular, it remains unclear whether DR prolongs life through conserved mechanisms in different species. Here, we show that, in the most common experimental conditions, lifespan extension by DR is abolished by providing Drosophila with ad libitum water, without altering food intake, indicating that DR, as conventionally studied in flies, is fundamentally different from the phenomenon studied in mammals. We characterize an alternative dietary paradigm that elicits robust lifespan extension irrespective of water availability, and thus likely represents a more relevant model for mammalian DR. Our results support the view that protein:carbohydrate ratio is the main dietary determinant of fly lifespan. These findings have broad implications for the study of lifespan and nutrition.
PNAS 2009 106:18633-18637
Insect Palaeontology
- A Probable Pollination Mode Before Angiosperms: Eurasian, Long-Proboscid Scorpionflies
Dong Ren,1 Conrad C. Labandeira,2,3,* Jorge A. Santiago-Blay,2,4 Alexandr Rasnitsyn,5,6 ChungKun Shih,1 Alexei Bashkuev,5 M. Amelia V. Logan,7 Carol L. Hotton,2,8 David Dilcher2,9labandec@si.edu
1. College of Life Sciences, Capital Normal University, Beijing 100048, China
2. Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013, USA
3. Department of Entomology, University of Maryland, College Park, MD 20742, USA.
4. Department of Biology, Gallaudet University, Washington, DC 20003, USA.
5. Paleontological Institute, Russian Academy of Sciences, Moscow 117997, Russia.
6. Department of Palaeontology, Natural History Museum, London SW7 5BD, UK.
7. Department of Mineral Sciences, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013, USA.
8. National Center for Biotechnology Information, National Library of Medicine, Bethesda, MD 20892, USA.
9. Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA.
The head and mouthpart structures of 11 species of Eurasian scorpionflies represent three extinct and closely related families during a 62-million-year interval from the late Middle Jurassic to the late Early Cretaceous. These taxa had elongate, siphonate (tubular) proboscides and fed on ovular secretions of extinct gymnosperms. Five potential ovulate host-plant taxa co-occur with these insects: a seed fern, conifer, ginkgoopsid, pentoxylalean, and gnetalean. The presence of scorpionfly taxa suggests that siphonate proboscides fed on gymnosperm pollination drops and likely engaged in pollination mutualisms with gymnosperms during the mid-Mesozoic, long before the similar and independent coevolution of nectar-feeding flies, moths, and beetles on angiosperms. All three scorpionfly families became extinct during the later Early Cretaceous, coincident with global gymnosperm-to-angiosperm turnover.
Science 2009 326: 840 - 847
Insect Pharmacology: serotonin
42. Effects of serotonergic agents on survival and hemolymph composition of the larval mosquito Aedes aegypti (Diptera: Culicidae, L.) in vivo: does serotonin regulate hemolymph acid–base homeostasis?
T. M. Clark*, J. L. Lawecki, J. J. Shepherd, A. N. Hirschler and T. R. Samandu tclark2@iusb.edu
Indiana University South Bend, 1700 Mishawaka Avenue, South Bend, IN 46634-1700, USA
The role of serotonin in the regulation of larval Aedes aegypti hemolymphcomposition was investigated in vivo using two reuptake inhibitors(SSRIs), alaproclate HCl and 6-nitroquipazine maleate, and the receptorantagonist methiothepin mesylate. Larvae were placed in media differingin pH and salinity in the presence and absence of serotonergic agents.The toxicity of each agent was strongly influenced by ambientpH. For each agent, toxicity was negligible in acidic media,intermediate in neutral media and greatest in alkaline media.By contrast, toxicity of all agents was independent of salinity.No effects on mass-specific body water or hemolymph volume wereobserved whereas hemolymph osmotic pressure, Na+ concentrationsand pH differed significantly among treatments. 6-nitroquipazinecaused a decrease in Na+ from 115±1.7 to 103±0.9mmol l–1, and alaproclate caused alkalosis of the hemolymphfrom pH 7.55±0.026 to pH 7.72±0.044. Methiothepin decreasedhemolymph osmotic pressure from 329±9.9 to 304±8.8and showed the greatest overall toxicity. Control larvae excretednet base in pH 4 media (1.4 µmol g–1 h–1)and net acid in pH 7 (1.2 µmol g–1 h–1) andpH 11 (5.1 µmol g–1 h–1) media. In pH 4 media, alaproclateand methiothepin caused a shift to net H+ excretion (1.1 and1.5 µmol g–1 h1, respectively) whereas these agentsdid not influence acid excretion rates in pH 7 or pH 11 media. Thehypothesis that serotonin is involved in hemolymph acid–basebalance is discussed.
Journal of Experimental Biology 212, 3728-3736 (2009) October 30, 2009
http://jeb.biologists.org/cgi/content/abstract/212/22/3728
http://jeb.biologists.org/cgi/content/abstract/212/22/3728
Insect Photoreception
43. Different photoreceptor organs are used for photoperiodism in the larval and adult stages of the carabid beetle, Leptocarabus kumagaii
Yoshinori Shintani, Sakiko Shiga and Hideharu Numata shintani@nankyudai.ac.jp
Department of Biology and Geosciences, Graduate School of Science, Osaka City University, Osaka 558-8585, Japan
The role of the two distinct retinal photoreceptor organs inphotoreception for photoperiodism was examined in the carabidbeetle, Leptocarabus kumagaii, by surgical removal. This beetleshows long-day and short-day photoperiodic responses in thelarval and adult stages, respectively. Larval diapause in thefinal instar is induced under short-day conditions whereas pupationoccurs without diapause under long-day conditions. Adult reproductive diapauseis terminated under short-day conditions but maintained under long-dayconditions. The stemmata of the larvae and compound eyes ofthe adults were removed and the responses of the animals tophotoperiod were compared to those of intact beetles. When allthe stemmata were removed, larvae pupated without entering diapauseunder both long-day and short-day conditions, indicating thatthe larvae lacking stemmata were incapable of photoreceptionfor photoperiodism. As in other holometabolous insects, the stemmatamigrated into the brain during metamorphosis and remained rudimentarilyin the optic lobe of the adult brain. However, these stemmata-derivedorgans were found to be no longer necessary for photoperiodism,because adults lacking the stemmata-derived organs responded tophotoperiod normally. By contrast, removal of the compound eyesin adults resulted in the termination of reproductive diapauseunder both long-day and short-day conditions, indicating thatphotoreception for photoperiodism in the adult stage is performedby the compound eyes. Therefore, the site of photoperiodic photoreceptionin L. kumagaii appear to change from the stemmata to the compoundeyes during metamorphosis.
Journal of Experimental Biology 212, 3651-3655 (2009) October 30, 2009
Insect Society
- Prudent sperm use by leaf-cutter ant queens
Susanne P. A. den Boer1,*, Boris Baer2,3, Stephanie Dreier1, Serge Aron4, David R. Nash1 and Jacobus J. Boomsma1 spadenboer@bio.ku.dk
1. Centre for Social Evolution, Department of Biology , University of Copenhagen, Universitetsparken 15, 2100 Copenhagen , Denmark
2. ARC Centre of Excellence in Plant Energy Biology, MCS Building M310, The University of Western Australia 6009, Crawley, Australia
3. Centre for Evolutionary Biology, School of Animal Biology (MO92), The University of Western Australia 6009, Crawley, Australia
4. Behavioural and Evolutionary Ecology, Université Libre de Bruxelles, Avenue F. D. Roosevelt 50, 1050 Brussels, Belgium
In many species, females store sperm between copulation and egg fertilization, but the consequences of sperm storage and patterns of sperm use for female life history and reproductive success have not been investigated in great detail. In hymenopteran insect societies (ants, bees, wasps), reproduction is usually monopolized by one or relatively few queens, who mate only during a brief period early in life and store sperm for later use. The queens of some ants are particularly long-lived and have the potential to produce millions of offspring during their life. To do so, queens store many sperm cells, and this sperm must remain viable throughout the years of storage. Queens should also be under strong selection to use stored sperm prudently when fertilizing eggs. We used the leaf-cutter ant Atta colombica to investigate the dynamics of sperm use during egg fertilization. We show that queens are able to fertilize close to 100 per cent of the eggs and that the average sperm use per egg is very low, but increases with queen age. The robustness of stored sperm was found to decrease with years of storage, signifying that senescence affects sperm either directly or indirectly via the declining glandular secretions or deteriorating sperm-storage organs. We evaluate our findings with a heuristic model, which suggests that the average queen has sperm for almost 9 years of normal colony development. We discuss the extent to which leaf-cutter ant queens have been able to optimize their sperm expenditure and infer that our observed averages of sperm number, sperm robustness and sperm use are consistent with sperm depletion being a significant cause of mortality of mature colonies of Atta leaf-cutter ants.
Proc. R. Soc. B 22 November 2009 vol. 276 no. 16753945-3953
- Termites eavesdrop to avoid competitors
Theodore A. Evans1,*, Ra Inta1,2,†, Joseph C. S. Lai2, Stefan Prueger2, Nyuk Wei Foo2, Eugene Wei'en Fu2 and Michael Lenz1theo.evans@csiro.au
1. Division of Entomology, Commonwealth Scientific and Industrial Research Organization, Clunies Ross Street, Canberra ACT 2600, Australia
2. School Engineering and Information Technology, Australian Defence Force Academy, University of New South Wales, Canberra ACT 2600, Australia
Competition exclusion, when a single species dominates resources due to superior competitiveness, is seldom observed in nature. Termites compete for resources with deadly consequences, yet more than one species can be found feeding in the same wooden resource. This is especially surprising when drywood species, with colonies of a few hundred, are found cohabiting with subterranean species, with colonies of millions. Termites communicate vibro-acoustically and, as these signals can travel over long distances, they are vulnerable to eavesdropping. We investigated whether drywood termites could eavesdrop on vibration cues from subterranean species. We show, using choice experiments and recordings, that the drywood termite Cryptotermes secundus can distinguish its own species from the dominant competitor in the environment, the subterranean termite Coptotermes acinaciformis. The drywood termite was attracted to its own vibration cues, but was repelled by those of the subterranean species. This response increased with decreasing wood size, corresponding with both increased risk and strength of the cue. The drywood termites appear to avoid confrontation by eavesdropping on the subterranean termites; these results provide further evidence that vibro-acoustic cues are important for termite sensory perception and communication.
Proc. R. Soc. B 22 November 2009 vol. 276 no. 16754035-4041
https://blog.sciencenet.cn/blog-278346-270398.html
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