博文
Insect frontiers, March 2010 Volume 2 Number 3
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Insect Behaviour
Knowing who's who: nestmate recognition in the facultatively social carpenter bee, Xylocopa virginica
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a Department of Biological Sciences, Brock University, Canada
When animals live in groups, the ability to discriminate group members from nonmembers allows individuals to adjust their behaviour in ways that enhance both individual and group fitness. In social insects, especially bees, this kind of recognition has mainly been studied with reference to colony-based social interactions, but they also interact in other kinds of group contexts. In the facultatively social carpenter bee, Xylocopa virginica, individuals of both sexes interact repeatedly, in such activities as cooperative brood raising by females, territorial competition by males, and matings near nest entrances. In light of these varied interactions, in which the ability to discriminate familiar from unfamiliar individuals might be advantageous, the aim of our study was to determine whether X. virginica adults are capable of nestmate recognition. Nestmates were defined operationally as bees that were caught at the same nest entrance after spending the night together, whereas non-nestmates were from different nests. We used circle tube assays of male–male, female–female and male–female dyads to compare rates of aggressive (pushing, biting and C-postures) and tolerant/cooperative (head-to-head touching and passing) behaviour in nestmates versus non-nestmates. In general, aggression occurred sooner and more frequently among non-nestmates than among nestmates, whereas tolerance was more common among nestmates. This indicates that male and female bees can recognize familiar individuals of both sexes and adjust their behaviour accordingly. Since tested individuals may have been nestmates for less than 24 h, this further suggests that both female and male bees may learn the identities of their nestmates quickly.
Plasticity in mating behaviour drives asymmetric reproductive interference in whiteflies
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a Department of Entomology, University of Arizona, USA
b Department of Entomology, Washington State University, USA
c Department of Zoology, Miami University, USA
Reproductive interference between species with incomplete mate recognition can disrupt the process of mate acquisition. Accordingly, reproductive interference can reduce female and male fitness and lead to sexual exclusion. Here, we tested the hypothesis that flexible mating behaviours could mitigate the fitness-reducing effects of reproductive interference between reproductively incompatible biotypes of the haplodiploid whitefly Bemisia tabaci. We show that females of the globally distributed and invasive B biotype respond to reproductive interference from the Q biotype by increasing their acceptance of copulation attempts from B males. This behavioural plasticity increases the ability of B females to mate successfully and maintain a constant sex ratio in their offspring despite reproductive interference. In contrast, females of competing biotypes have invariant behaviour and produce fewer female offspring because of reproductive interference from the B biotype. Heuristic simulation models incorporating data on behavioural and life history traits of the B and Q biotypes obtained here, and published data on other biotypes, show that this plasticity in mating behaviour of B females could contribute to sexual exclusion of closely related biotypes. Our results demonstrate a powerful link between mating behaviour, reproductive interference and sexual exclusion, suggesting that variation in mating behaviour could determine the effects of reproductive interference and drive sexual exclusion among closely related species or among biotypes of a species.
Assessment of oviposition site quality by aphidophagous hoverflies: reaction to conspecific larvae
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and Eric Haubrugea
a Department of Functional & Evolutionary Entomology, Belgium
b Department of Analytical Chemistry, Gembloux Agro-Bio Tech, University of Liège, Belgium
Aphidophagous predators adapt their foraging behaviour to the presence of conspecific and heterospecific larvae. We studied the effect of the presence of conspecific larvae and their tracks on the oviposition site selection of an aphid-specific predator, Episyrphus balteatus DeGeer (Diptera: Syrphidae), in two-choice experiments using a leaf disc bioassay. Gas chromatography – mass spectrometry analysis was used to identify the volatile chemicals released from odour extracts of E. balteatus larval tracks. The behavioural effects of these volatile substances on hoverfly females were also evaluated. Our experiments demonstrated that E. balteatus females were deterred from ovipositing when presented with a Vicia faba leaf with aphids and conspecific larvae. The oviposition-deterring stimulus was also active when females were presented with a leaf that contained conspecific larval tracks. A mixture of chemical compounds was found in the volatile pattern of odour extracts of larval tracks. The main volatile chemicals were 3-methylbutanoic acid, 2-methylbutanoic acid, 2-methylpropanoic acid, 3-hydroxy-2-butanone, hexanoic acid and phenol. Females also laid significantly fewer eggs in response to odorant volatiles emitted from larval extracts. These results highlight that predatory hoverfly females avoid ovipositing in aphid colonies in which conspecific larvae or their tracks are already present, suggesting that this behaviour constitutes a strategy that enables females to optimize their oviposition site and reduce competition suffered by their offspring.
Effects of queen mandibular pheromone on nestmate recognition in worker honeybees, Apis mellifera
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a Department of Entomology, W. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, U.S.A.
b Department of Genetics, W. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, U.S.A.
The ability to distinguish between members of a social group and unfamiliar individuals is a critical element of social behaviour. Social insects can differentiate between nestmates and non-nestmates via recognition cues, which in most species are cuticular hydrocarbons. Cuticular hydrocarbon patterns are altered by genotype and environmental conditions, but it is unclear whether colony social conditions can also affect nestmate interactions. Honeybee queens produce pheromones that regulate many aspects of worker behaviour, physiology and colony organization. A five-component blend, queen mandibular pheromone (QMP), produces many of the effects of a live queen. We found that QMP treatment alters how resident bees interact with intruder bees, based on standard nestmate recognition assays. However, QMP does not appear to alter the ability of bees to distinguish between nestmates and non-nestmates, or general aggression levels. Rather, QMP exposure significantly alters cuticular hydrocarbon patterns of worker bees, suggesting that QMP-treated nestmates are no longer recognized as nestmates by untreated bees, and vice versa. Thus, queen pheromone can have significant effects on nestmate recognition and interactions in honeybees, which may be important for colony cohesion.
Insect Biochemistry
The Glycerophosphate Cycle in Drosophila melanogaster V. Molecular Analysis of Glycerophosphate Dehydrogenase and Glycerophosphate Oxidase Mutants
Amber Carmon, Jeff Chien, David Sullivan, and Ross MacIntyrerjm18@cornell.edu
From the Department of Molecular Biology and Genetics, 407 Biotechnology Building, Cornell University, Ithaca, NY 14853 (Carmon, Chien, and MacIntyre); and the Department of Biology, Syracuse University, Syracuse, NY (Sullivan)
Two enzymes, glycerophosphate dehydrogenase (GPDH-1) in thecytoplasm and glycerophosphate oxidase (GPO-1) in the mitochondrioncooperate in Drosophila flight muscles to generate the ATP neededfor muscle contraction. Null mutants for either enzyme cannotfly. Here, we characterize 15 ethyl methane sulfonate (EMS)-inducedmutants in GPDH-1 at the molecular level and assess their effectson structural and evolutionarily conserved domains of this enzyme.In addition, we molecularly characterize 3 EMS-induced GPO-1mutants and excisions of a P element insertion in the GPO-1gene. The latter represent the best candidate for null or amorphicmutants in this gene.
Journal of Heredity 2010 101(2):218-224; doi:10.1093/jhered/esp110
The Glycerophosphate Cycle in Drosophila melanogaster VI. Structure and Evolution of Enzyme Paralogs in the Genus Drosophila
Amber Carmon, and Ross MacIntyrerjm18@cornell.edu
From the Department of Molecular Biology and Genetics, 407 Biotechnology Building, Cornell University, Ithaca, NY 14853
The genome sequences of 12 Drosophila species contain 3 paralogsfor glycerophosphate dehydrogenase (GPDH) and for the mitochondrialglycerophosphate oxidase (GPO). These 2 enzymes participatein the glycerophosphate cycle in the adult thoracic flightmuscles. The flight muscle enzymes are encoded by gpdh-1 at26A2 and gpo-1 at 52C8. In this paper, we show that the GPDHparalogs share the same evolutionarily conserved functionaldomains and most intron positions, whereas the GPO paralogsshare only some of the functional domains of mitochondrial oxidoreductases.The GPO paralogs not expressed in the flight muscles essentiallylack introns. GPDH paralogs encoded by gpdh-2 and gpdh-3 andthe GPO paralogs encoded by gpo-2 and gpo-3 are expressed onlyin the testes. Gene trees for the GPDH and GPO paralogs indicatethat the genes expressed in the flight muscles are evolvingvery slowly presumably under strong purifying selection whereasthe paralogs expressed in the testes are evolving more rapidly.The concordance between species and gene trees, dN/dS ratios,phylogenetic analysis by maximum likelihood-based tests, andanalyses of radical and conservative substitutions all indicatethat the additional GPDH and GPO paralogs are also evolvingunder purifying selection.
Journal of Heredity 2010 101(2):225-234; doi:10.1093/jhered/esp111
Insect Chemoecology
Egg attachment of the asparagus beetle Crioceris asparagi to the crystalline waxy surface of Asparagus officinalis
Plant surfaces covered with crystalline epicuticular waxes are known to be anti-adhesive, hardly wettable and preventing insect attachment. But there are insects that are capable of gluing their eggs to these surfaces by means of proteinaceous secretions. In this study, we analysed the bonding region between the eggs of Crioceris asparagi and the plant surface of Asparagus officinalis using light and cryo-scanning electron microscopy. The wettability of the plant surface by egg secretion was compared with that by Aqua Millipore water, aqueous sugar solution and chicken egg white. Furthermore, the force required to remove C. asparagi eggs from the plant surface was measured, in order to evaluate the egg's bonding strength. Mean pull-off force was 14.7 mN, which is about 8650 times higher than the egg weight. Egg glue was observed spreading over the wax crystal arrays on the plant cladophyll and wetting them. Similar wetting behaviour on the A. officinalis surface was observed for chicken egg white. Our results support the hypothesis that the mechanism of insect egg adhesion on micro- and nanostructured hydrophobic plant surfaces is related to the proteinaceous nature of adhesive secretions of insect eggs. The secretion wets superhydrophobic surfaces and after solidifying builds up a composite, consisting of the solidified glue and wax crystals, at the interface between the egg and plant cuticle.
Proc. R. Soc. B 22 March 2010 vol. 277 no. 1683 895-903
Insect Ecology
Insect overwintering in a changing climate
J. S. Bale* and S. A. L. Haywardj.s.bale@bham.ac.uk
School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK
Insects are highly successful animals inhabiting marine, freshwaterand terrestrial habitats from the equator to the poles. As agroup, insects have limited ability to regulate their body temperatureand have thus required a range of strategies to support lifein thermally stressful environments, including behavioural avoidancethrough migration and seasonal changes in cold tolerance. Withrespect to overwintering strategies, insects have traditionallybeen divided into two main groups: freeze tolerant and freezeavoiding, although this simple classification is underpinnedby a complex of interacting processes, i.e. synthesis of icenucleating agents, cryoprotectants, antifreeze proteins andchanges in membrane lipid composition. Also, in temperate andcolder climates, the overwintering ability of many species isclosely linked to the diapause state, which often increasescold tolerance ahead of temperature-induced seasonal acclimatisation.Importantly, even though most species can invoke one or bothof these responses, the majority of insects die from the effectsof cold rather than freezing. Most studies on the effects ofa changing climate on insects have focused on processes thatoccur predominantly in summer (development, reproduction) andon changes in distributions rather than winter survival perse. For species that routinely experience cold stress, a generalhypothesis would be that predicted temperature increases of1°C to 5°C over the next 50-100 years would increasewinter survival in some climatic zones. However, this is unlikelyto be a universal effect. Negative impacts may occur if climatewarming leads to a reduction or loss of winter snow cover inpolar and sub-polar areas, resulting in exposure to more severeair temperatures, increasing frequency of freeze—thawcycles and risks of ice encasement. Likewise, whilst the dominantdiapause-inducing cue (photoperiod) will be unaffected by globalclimate change, higher temperatures may modify normal ratesof development, leading to a decoupling of synchrony betweendiapause-sensitive life-cycle stages and critical photoperiodsfor diapause induction. In terms of climate warming and potentialheat stress, the most recent predictions of summer temperaturesin Europe of 40°C or higher in 50-75 years, are close tothe current upper lethal limit of some insects. Long-term datasets on insect distributions and the timing of annual migrationsprovide strong evidence for ‘positive’ responsesto higher winter temperatures over timescales of the past 20-50years in North America, Europe and Asia.
Journal of Experimental Biology 213, 980-994 (2010)
A multi-scale study of Orthoptera species richness and human population size controlling for sampling effort
Elena Cantarello1, Claude E. Steck2, Paolo Fontana3, Diego Fontaneto4, Lorenzo Marini3 and Marco Pautasso5 m.pautasso@ic.ac.uk
1 School of Conservation Sciences, Bournemouth University, Talbot Campus, Poole, BH12 5BB Bournemouth, UK
2 Section of Nature Conservation and Historical Ecology, Department of Landscape, Federal Research Institute WSL, 8903 Birmensdorf, Switzerland
3 Department of Environmental Agronomy and Crop Production, University of Padova, 35020 Padova, Italy
4 Department of Invertebrate Zoology, Swedish Museum of Natural History, 10405 Stockholm, Sweden
5 Division of Biology, Imperial College London, Silwood Campus, SL5 7PY Ascot, UK
Recent large-scale studies have shown that biodiversity-rich regions also tend to be densely populated areas. The most obvious explanation is that biodiversity and human beings tend to match the distribution of energy availability, environmental stability and/or habitat heterogeneity. However, the species–people correlation can also be an artefact, as more populated regions could show more species because of a more thorough sampling. Few studies have tested this sampling bias hypothesis. Using a newly collated dataset, we studied whether Orthoptera species richness is related to human population size in Italy’s regions (average area 15,000 km2) and provinces (2,900 km2). As expected, the observed number of species increases significantly with increasing human population size for both grain sizes, although the proportion of variance explained is minimal at the provincial level. However, variations in observed Orthoptera species richness are primarily associated with the available number of records, which is in turn well correlated with human population size (at least at the regional level). Estimated Orthoptera species richness (Chao2 and Jackknife) also increases with human population size both for regions and provinces. Both for regions and provinces, this increase is not significant when controlling for variation in area and number of records. Our study confirms the hypothesis that broad-scale human population–biodiversity correlations can in some cases be artefactual. More systematic sampling of less studied taxa such as invertebrates is necessary to ascertain whether biogeographical patterns persist when sampling effort is kept constant or included in models.
Molecular diagnosis of a previously unreported predator–prey association in coffee: Karnyothrips flavipes Jones (Thysanoptera: Phlaeothripidae) predation on the coffee berry borer
Juliana Jaramillo1, 2 , Eric G. Chapman3, Fernando E. Vega4 and James D. Harwood3 jjaramillo@icipe.org
1 International Centre of Insect Physiology and Ecology (ICIPE), P.O. Box 30772-00100, Nairobi, Kenya
2 Institute of Plant Diseases and Plant Protection, University of Hannover, Herrenhäuser Straße. 2, 30419 Hannover, Germany
3 Department of Entomology, University of Kentucky, S225 Agricultural Science Center North, Lexington, KY 40546-0091, USA
4 Sustainable Perennial Crops Laboratory, US Department of Agriculture, Agricultural Research Service, Building 001, Beltsville, MD 20705, USA
The coffee berry borer, Hypothenemus hampei, is the most important pest of coffee throughout the world, causing losses estimated at US $500 million/year. The thrips Karnyothrips flavipes was observed for the first time feeding on immature stages of H. hampei in April 2008 from samples collected in the Kisii area of Western Kenya. Since the trophic interactions between H. hampei and K. flavipes are carried out entirely within the coffee berry, and because thrips feed by liquid ingestion, we used molecular gut-content analysis to confirm the potential role of K. flavipes as a predator of H. hampei in an organic coffee production system. Species-specific COI primers designed for H. hampei were shown to have a high degree of specificity for H. hampei DNA and did not produce any PCR product from DNA templates of the other insects associated with the coffee agroecosystems. In total, 3,327 K. flavipes emerged from 17,792 H. hampei-infested berries collected from the field between April and September 2008. Throughout the season, 8.3% of K. flavipes tested positive for H. hampei DNA, although at times this figure approached 50%. Prey availability was significantly correlated with prey consumption, thus indicating the potential impact on H. hampei populations.
Electronic supplementary material The online version of this article (doi:10.1007/s00114-009-0641-7) contains supplementary material, which is available to authorized users.
Discovery of mycangia and the associated xylose-fermenting yeasts in stag beetles (Coleoptera: Lucanidae)
Masahiko Tanahashi1 , Kôhei Kubota1, Norihisa Matsushita2 and Katsumi Togashi1kawotuptera@fr.a.u-tokyo.ac.jp
Laboratory of Forest Zoology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan
Laboratory of Forest Botany, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan
Most wood-feeding insects need an association with microbes to utilize wood as food, and some have special organs to store and convey the microbes. We report here the discovery of the microbe-storage organ (mycangium) in stag beetles (Coleoptera: Lucanidae), which develop in decayed wood. The mycangium, which was discovered in the abdomen, is present in all adult females of 22 lucanid species examined in this study, but absent in adult males. By contrast, adult insects of both sexes of selected Passalidae, Geotrupidae, and Scarabaeidae, which are related to Lucanidae, lacked mycangia similar to those of the lucanid species. Yeast-like microbes were isolated from the mycangium of five lucanid species. DNA sequence analyses indicate that the microbes are closely related to the xylose-fermenting yeasts Pichia stipitis, Pichia segobiensis, or Pichia sp. known from the gut of a passalid species.
The alternative Pharaoh approach: stingless bees mummify beetle parasites alive
Mark K. Greco1, 2 , Dorothee Hoffmann3, 6, Anne Dollin4, Michael Duncan2, Robert Spooner-Hart2 and Peter Neumann1, 5mark.greco@alp.admin.ch
Swiss Bee Research Centre, Agroscope Liebefeld-Posieux Research Station ALP, CH-3033 Bern, Switzerland
Centre for Plant and Food Science, School of Natural Sciences, University of Western Sydney, Richmond, NSW, 1797, Australia
Department of Zoology, Martin-Luther-Universität Halle-Wittenberg, Hoher Weg 4, 06099 Halle, Saale, Germany
Australian Native Bee Research Centre, North Richmond, NSW, Australia
Department of Zoology and Entomology, Rhodes University, 61440 Grahamstown, Republic of South Africa
KU Leuven, Laboratory of Aquatic Ecology and Evolutionary Biology, Charles Deberiotstraat 32 - bus 2439, 3000 Leuven, Belgium
Workers from social insect colonies use different defence strategies to combat invaders. Nevertheless, some parasitic species are able to bypass colony defences. In particular, some beetle nest invaders cannot be killed or removed by workers of social bees, thus creating the need for alternative social defence strategies to ensure colony survival. Here we show, using diagnostic radioentomology, that stingless bee workers (Trigona carbonaria) immediately mummify invading adult small hive beetles (Aethina tumida) alive by coating them with a mixture of resin, wax and mud, thereby preventing severe damage to the colony. In sharp contrast to the responses of honeybee and bumblebee colonies, the rapid live mummification strategy of T. carbonaria effectively prevents beetle advancements and removes their ability to reproduce. The convergent evolution of mummification in stingless bees and encapsulation in honeybees is another striking example of co-evolution between insect societies and their parasites.
Activation of the immune system promotes insect dispersal in the wild
Jukka Suhonen1 , Johanna Honkavaara1 and Markus J. Rantala1 juksuh@utu.fi
Section of Ecology, Department of Biology, University of Turku, 20014 Turku, Finland
Dispersal has important ecological and evolutionary consequences but is a poorly understood behaviour. We experimentally tested whether activation of the immune system affects dispersal in male damselflies, Calopteryx virgo, from three natural populations. We show that males that contained an experimentally inserted artificial pathogen, a nylon monofilament implant, had higher dispersal rates and flew further than control males, but not further than sham manipulated males. Our data suggest that dispersal may reduce the risk of further infections if immune system activation indicates high parasite infection risk in the present habitat. We, thus, suggest that parasites may play an important role in the evolution of host dispersal.
Developmental plasticity and reduced susceptibility to natural enemies following host plant defoliation in a specialized herbivore
Glen R. Hood1, 2 and James R. Ott2 JimOtt@txstate.edu
Department of Biological Sciences, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA
Population and Conservation Biology Program, Department of Biology, Texas State University-San Marcos, San Marcos, TX 78666, USA
Host-specific phytophagous insects that are short lived and reliant on ephemeral plant tissues provide an excellent system in which to investigate the consequences of disruption in the timing of resource availability on consumer populations and their subsequent interactions with higher tropic levels. The specialist herbivore, Belonocnema treatae (Hymenoptera: Cynipidae) induces galls on only newly flushed leaves of live oak, Quercus fusiformis. In central Texas (USA) episodic defoliation of the host creates variation in the timing of resource availability and results in heterogeneous populations of B. treatae that initiate development at different times. We manipulated the timing of leaf flush in live oak via artificial defoliation to test the hypothesis that a 6- to 8-week delay in the availability of resources alters the timing of this gall former’s life cycle events, performance and survivorship on its host, and susceptibility to natural enemies. B. treatae exhibits plasticity in development time, as the interval from egg to emergence was significantly reduced when gallers oviposited into the delayed leaf flush. As a consequence, the phenologies of gall maturation and adult emergence remain synchronized in spite of variation in the timing of resource availability. Per capita gall production and gall-former performance are not significantly affected by the timing of resource availability. The timing of resource availability and natural enemies interact, however, to produce strong effects on survivorship: when exposed to natural enemies, B. treatae developing in galls initiated by delayed oviposition exhibited an order-of-magnitude increase in survivorship. Developmental plasticity allows this gall former to circumvent disruptions in resource availability, maintain synchrony of life cycle events, and results in reduced vulnerability to natural enemies following defoliation of the host plant.
Natural enemy diversity reduces temporal variability in wasp but not bee parasitism
Dorthe Veddeler1 , Jason Tylianakis2, Teja Tscharntke3 and Alexandra-Maria Klein3 dorthe.veddeler@web.de
Institute of Ecology, University of Jena, Dornburger Strasse 159, 07743 Jena, Germany
School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, 8020, New Zealand
Department of Crop Science (Agroecology Section), University of Göttingen, Waldweg 26, 37073 Göttingen, Germany
Biodiversity may enhance and stabilise ecosystem functioning, but little evidence exists for diversity–function relationships involving multitrophic interactions in real landscapes. In multitrophic communities diversity may vary at different trophic levels, with either synergistic or antagonistic effects on ecosystem functioning. Intensification of land-use systems is often found to reduce diversity, which in turn may lead to reduced associated ecological functions in natural food webs, such as host-parasite interactions. In this study we investigated the relationship between the number of natural enemy and host species and the mean rate and temporal variability of parasitism (inverse of stability), along an intensification gradient of coffee agroforests in Ecuador. We used standardised trap nests for bees and wasps and their natural enemies in 14 agroforests, and evaluated these monthly over a period of 17 months. We found that parasitism rates of wasps and bees increased with increasing number of enemy species and decreased with increasing number of host species. Temporal variability in parasitism rates decreased with increasing number of enemy species and increased with temporal variability in enemy species richness; however, these effects were restricted to wasp hosts. Intensification of agroforests did not significantly affect species richness of hosts or enemies or their relation to parasitism and its temporal variability. We conclude that high enemy diversity may enhance parasitism rates and that high host diversity may provide resistance against consumption. Furthermore, we show that a diverse and stable enemy community may also have a stabilizing effect on parasitism rates. However, these effects may be host-guild specific, as these relations were restricted to wasps.
Repeated stress exposure results in a survival–reproduction trade-off in Drosophila melanogaster
Department of Biology, The University of Western Ontario, London, Ontario, Canada N6A 5B7
While insect cold tolerance has been well studied, the vast majority of work has focused on the effects of a single cold exposure. However, many abiotic environmental stresses, including temperature, fluctuate within an organism's lifespan. Given that organisms may trade-off survival at the cost of future reproduction, we investigated the effects of multiple cold exposures on survival and fertility in the model organism Drosophila melanogaster. We found that multiple cold exposures significantly decreased mortality compared with the same length of exposure in a single sustained bout, but significantly decreased fecundity (as measured by r, the intrinsic rate of increase) as well, owing to a shift in sex ratio. This change was reflected in a long-term decrease in glycogen stores in multiply exposed flies, while a brief effect on triglyceride stores was observed, suggesting flies are reallocating energy stores. Given that many environments are not static, this trade-off indicates that investigating the effects of repeated stress exposure is important for understanding and predicting physiological responses in the wild.
Proc. R. Soc. B 22 March 2010 vol. 277 no. 1683 963-969
Insect Evolution
ADAPTATION TO DESICCATION FAILS TO GENERATE PRE- AND POSTMATING ISOLATION IN REPLICATE DROSOPHILA MELANOGASTER LABORATORY POPULATIONS
1Department of Biology and Centre for Advanced Research in Environmental Genomics, University of Ottawa, Ottawa, ON, K1N 6N5, Canada 2E-mail:
Many laboratory speciation experiments have raised allopatric populations in different environments to determine whether reproductive isolation evolves as a byproduct of adaptation (a form of ecological speciation). Few, however, have addressed the evolution of both pre- and postmating isolation or investigated the conditions affecting the process. We present results of an evolution experiment in which 12 lines of Drosophila melanogaster were derived from a common population and then independently evolved for more than 57 generations under alternative selection treatments. Six "desiccation" populations had access to food and water removed during a period of their adult lives generating strong desiccation selection, and six "starvation" populations had access to food but not water removed for the same period, generating a mild starvation stress. Substantial divergence of cuticular hydrocarbons occurred between the desiccation and starvation populations, key traits that have been implicated in sexual isolation in Drosophila. Despite this divergence, there was no detectable premating isolation between desiccation and starvation populations and postmating isolation was asymmetrical: the fitness of F1 hybrids was reduced in the desiccation but not the starvation environment. This asymmetry was likely caused by the absence of divergent selection: adaptation to desiccation appears to have come at no cost to performance in the starvation environment. Novel environments are thought to promote the evolution of reproductive isolation. Understanding the conditions that favor or hamper this remains a key challenge for speciation research.
FEATURE THEORY AND THE TWO-STEP HYPOTHESIS OF MÜLLERIAN MIMICRY EVOLUTION
Alexandra Catherine VictoriaBalogh 1,2 , Gabriella Gamberale-Stille 1 , Birgitta Sillén Tullberg 1 , and Olof Leimar 1 alexandra.balogh@zoologi.su.se
1Department of Zoology, Stockholm University, S-10691 Stockholm, Sweden 2E-mail:
The two-step hypothesis of Müllerian mimicry evolution states that mimicry starts with a major mutational leap between adaptive peaks, followed by gradual fine-tuning. The hypothesis was suggested to solve the problem of apostatic selection producing a valley between adaptive peaks, and appears reasonable for a one-dimensional phenotype. Extending the hypothesis to the realistic scenario of multidimensional phenotypes controlled by multiple genetic loci can be problematic, because it is unlikely that major mutational leaps occur simultaneously in several traits. Here we consider the implications of predator psychology on the evolutionary process. According to feature theory, single prey traits may be used by predators as features to classify prey into discrete categories. A mutational leap in such a trait could initiate mimicry evolution. We conducted individual-based evolutionary simulations in which virtual predators both categorize prey according to features and generalize over total appearances. We found that an initial mutational leap toward feature similarity in one dimension facilitates mimicry evolution of multidimensional traits. We suggest that feature-based predator categorization together with predator generalization over total appearances solves the problem of applying the two-step hypothesis to complex phenotypes, and provides a basis for a theory of the evolution of mimicry rings.
Insect Heredity
Population dynamics and rapid spread of Cardinium, a bacterial endosymbiont causing cytoplasmic incompatibility in Encarsia pergandiella (Hymenoptera: Aphelinidae)
L R Harris1, S E Kelly2, M S Hunter2 and S J Perlman1 leanner.harris@gmail.com
1Department of Biology, University of Victoria, Victoria, British Columbia, Canada
2Department of Entomology, The University of Arizona, Tucson, AZ, USA
Cytoplasmic incompatibility (CI) is a common phenotype of maternally inherited bacterial symbionts of arthropods; in its simplest expression, uninfected females produce few or no viable progeny when mated to infected males. Infected females thus experience a reproductive advantage relative to that of uninfected females, with the potential for the symbiont to spread rapidly. CI population dynamics are predicted to depend primarily on the strength of incompatibility, the fitness cost of the infection and how faithfully symbionts are inherited. Although the bacterial symbiont lineage Wolbachia has been most identified with the CI phenotype, an unrelated bacterium, Cardinium may also cause CI. In the first examination of population dynamics of CI-inducing Cardinium, we used population cages of the parasitic wasp Encarsia pergandiella (Hymenoptera: Aphelinidae) with varying initial infection frequencies to test a model of invasion. Cardinium was found to spread rapidly in all populations, even in cases where the initial infection frequency was well below the predicted invasion threshold frequency. The discrepancy between the modeled and actual results is best explained by weaker CI than measured in the lab and a cryptic fitness benefit to the infection.
Heredity (2010) 104, 239–246 http://www.nature.com/hdy/journal/v104/n3/abs/hdy2009130a.html
The cys-loop ligand-gated ion channel gene superfamily of the parasitoid wasp, Nasonia vitripennis
A K Jones1, A N Bera1, K Lees1 and D B Sattelle1 andrew.jones@dpag.ox.ac.uk
1MRC Functional Genomics Unit, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, UK
Members of the cys-loop ligand-gated ion channel (cysLGIC) superfamily mediate chemical neurotransmission and are studied extensively as potential targets of drugs used to treat neurological disorders, such as Alzheimer's disease. Insect cys-loop LGICs also have central roles in the nervous system and are targets of highly successful insecticides. Here, we describe the cysLGIC superfamily of the parasitoid wasp, Nasonia vitripennis, which is emerging as a highly useful model organism and is deployed as a biological control of insect pests. The wasp superfamily consists of 26 genes, which is the largest insect cysLGIC superfamily characterized, whereas Drosophila melanogaster, Apis mellifera and Tribolium castaneum have 23, 21 and 24, respectively. As with Apis, Drosophila and Tribolium, Nasonia possesses ion channels predicted to be gated by acetylcholine, γ-amino butyric acid, glutamate and histamine, as well as orthologues of the Drosophila pH-sensitive chloride channel (pHCl), CG8916 and CG12344. Similar to other insects, wasp cysLGIC diversity is broadened by alternative splicing and RNA A-to-I editing, which may also serve to generate species-specific receptor isoforms. These findings on N. vitripennis enhance our understanding of cysLGIC functional genomics and provide a useful basis for the study of their function in the wasp model, as well as for the development of improved insecticides that spare a major beneficial insect species.
Heredity (2010) 104, 247–259
Evolution of sex-specific wing shape at the widerwing locus in four species of Nasonia
D W Loehlin1, L S Enders2 and J H Werren1 dloehlin@mail.rochester.edu
1Department of Biology, University of Rochester, Rochester, NY, USA
2Department of Biology, University of California at Riverside, Riverside, CA, USA
How do morphological differences between species evolve at the genetic level? This study investigates the genetic basis of recent divergence in male wing size between species of the model parasitoid wasp Nasonia. The forewings of flightless Nasonia vitripennis males are 2.3 times smaller than males of their flighted sister species N. giraulti. We describe a major genetic contributor to this difference: the sex-specific widerwing (wdw) locus, which we have backcrossed from N. giraulti into N. vitripennis and mapped to an 0.9 megabase region of chromosome 1. This introgression of wdw from large-winged N. giraulti into small-winged N. vitripennis increases male but not female forewing width by 30% through wing region-specific size changes. Indirect evidence suggests that cell number changes across the wing explain the majority of the wdw wing-size difference, whereas changes in cell size are important in the center of the wing. Introgressing the same locus from the other species in the genus, N. longicornis and N. oneida, into N. vitripennis produces intermediate and large male wing sizes. To our knowledge, this is the first study to introgress a morphological quantitative trait locus (QTL) from multiple species into a common genetic background. Epistatic interactions between wdw and other QTL are also identified by introgressing wdw from N. vitripennis into N. giraulti. The main findings are (1) the changes at wdw have sex- and region-specific effects and could, therefore, be regulatory, (2) the wdw locus seems to be a co-regulator of cell size and cell number, and (3) the wdw locus has evolved different wing width effects in three species.
Heredity (2010) 104, 260–269
The genetic basis of interspecies host preference differences in the model parasitoid Nasonia
C A Desjardins1, F Perfectti1,2, J D Bartos1, L S Enders1,3 and J H Werren1 cdesjar3@mail.rochester.edu
1Department of Biology, University of Rochester, Rochester, NY, USA
The genetic basis of host preference has been investigated in only a few species. It is relevant to important questions in evolutionary biology, including sympatric speciation, generalist versus specialist adaptation, and parasite–host co-evolution. Here we show that a major locus strongly influences host preference in Nasonia. Nasonia are parasitic wasps that utilize fly pupae; Nasonia vitripennis is a generalist that parasitizes a diverse set of hosts, whereas Nasonia giraulti specializes in Protocalliphora (bird blowflies). In laboratory choice experiments using Protocalliphora and Sarcophaga (flesh flies), N. vitripennis shows a preference for Sarcophaga, whereas N. giraulti shows a preference for Protocalliphora. Through a series of interspecies crosses, we have introgressed a major locus affecting host preference from N. giraulti into N. vitripennis. The N. giraulti allele is dominant and greatly increases preference for Protocalliphora pupae in the introgression line relative to the recessive N. vitripennis allele. Through the utilization of a Nasonia genotyping microarray, we have identified the introgressed region as 16 Mb of chromosome 4, although a more complete analysis is necessary to determine the exact genetic architecture of host preference in the genus. To our knowledge, this is the first introgression of the host preference of one parasitoid species into another, as well as one of the few cases of introgression of a behavioral gene between species.
Heredity (2010) 104, 270–277
Behavioral and genetic characteristics of a new species of Nasonia
R Raychoudhury1, C A Desjardins1, J Buellesbach2,3, D W Loehlin1, B K Grillenberger4, L Beukeboom4, T Schmitt2,3 and J H Werren1 rraychou@mail.rochester
1Department of Biology, University of Rochester, Rochester, NY, USA
2Faculty of Biology I, Department of Evolutionary Biology and Animal Ecology, University of Freiburg, Freiburg, Germany
3Spemann Graduate School of Biology and Medicine (SGBM), University of Freiburg, Freiburg, Germany
4Center for Ecological and Evolutionary Studies, University of Groningen, Haren, The Netherlands
Nasonia (Hymenoptera: Pteromalidae) is a genus of parasitoid wasps, which is fast emerging as a model system for evolutionary, genetic, developmental and host–endosymbiont interaction studies. In this study, we report a new species, Nasonia oneida, distinguish its behavioral, genetic and morphological features, and characterize its pre-mating and post-mating isolation with the other Nasonia species. Phylogenetic analyses indicate that N. oneida is the sister species to Nasonia giraulti with its own uniquely distinct cuticular hydrocarbon profiles, behavioral characteristics and subtle morphological differences. An important characteristic of N. oneida is the strong mate discrimination shown by the females against all the other Nasonia species. A genetic analysis of this phenotype by interspecies hybridization indicates that this strong discriminating phenotype is recessive. A formal species description of N. oneida Raychoudhury & Desjardins is also provided.
Heredity (2010) 104, 278–288
Behavioral and spermatogenic hybrid male breakdown in Nasonia
1Department of Biology, University of Rochester, Rochester, NY, USA
Several reproductive barriers exist within the Nasonia species complex, including allopatry, premating behavioral isolation, postzygotic inviability and Wolbachia-induced cytoplasmic incompatibility. Here we show that hybrid males suffer two additional reproductive disadvantages, an inability to properly court females and decreased sperm production. Hybrid behavioral sterility, characterized by a reduced ability of hybrids to perform necessary courtship behaviors, occurs in hybrids between two species of Nasonia. Hybrid males produced in crosses between N. vitripennis and N. giraulti courted females at a reduced frequency (23–69%), compared with wild-type N. vitripennis and N. giraulti males (>93%). Reduced courtship frequency was not a simple function of inactivity among hybrids. A strong effect of cytoplasmic (mitochondrial) background was also found in N. vitripennis and N. giraulti crosses; F2 hybrids with giraulti cytoplasm showing reduced ability at most stages of courtship. Hybrids produced between a younger species pair, N. giraulti and N. longicornis, were behaviorally fertile. All males possessed motile sperm, but sperm production is greatly reduced in hybrids between the older species pair, N. vitripennis and N. giraulti. This effect on hybrid males, lowered sperm counts rather than nonfunctional sperm, is different from most described cases of hybrid male sterility, and may represent an earlier stage of hybrid sperm breakdown. The results add to previous studies of F2 hybrid inviability and behavioral sterility, and indicate that Wolbachia-induced hybrid incompatibility has arisen early in species divergence, relative to behavioral sterility and spermatogenic infertility.
Heredity (2010) 104, 289–301
A comparison of recombination frequencies in intraspecific versus interspecific mapping populations of Nasonia
L W Beukeboom1, O Niehuis2,3, B A Pannebakker1,4, T Koevoets1, J D Gibson2, D M Shuker4,5, L van de Zande1 and J Gadau2 l.w.beukeboom@rug.nl
1Evolutionary Genetics, Centre for Ecological and Evolutionary Studies, University of Groningen, Haren, The Netherlands
2School of Life Sciences, Arizona State University, Tempe, AZ, USA
3Behavioural Biology, University of Osnabrück, Osnabrück, Germany
4Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, UK
We present the first intraspecific linkage map for Nasonia vitripennis based on molecular markers. The map consists of 36 new microsatellite markers, extracted from the Nasonia genome sequence, and spans 515 cM. The five inferred linkage groups correspond to the five chromosomes of Nasonia. Comparison of recombination frequencies of the marker intervals spread over the whole genome (N=33 marker intervals) between the intraspecific N. vitripennis map and an interspecific N. vitripennis × N. giraulti map revealed a slightly higher (1.8%) recombination frequency in the intraspecific cross. We further considered an N. vitripennis × N. longicornis map with 29 microsatellite markers spanning 430 cM. Recombination frequencies in the two interspecific crosses differed neither between reciprocal crosses nor between mapping populations of embryos and adults. No major chromosomal rearrangements were found for the analyzed genomic segments. The observed differential F2 hybrid male mortality has no significant effect on the genome-wide recombination frequency in Nasonia. We conclude that interspecific crosses between the different Nasonia species, a hallmark of Nasonia genetics, are generally suitable for mapping quantitative and qualitative trait loci for species differences.
Heredity (2010) 104, 302–309
Contrasting patterns of selective constraints in nuclear-encoded genes of the oxidative phosphorylation pathway in holometabolous insects and their possible role in hybrid breakdown in Nasonia
1School of Life Sciences, Arizona State University, Tempe, AZ, USA
2Center for Evolutionary Functional Genomics, The Biodesign Institute, Arizona State University, Tempe, AZ, USA
The principal energy generating system in animals is the oxidative phosphorylation (OXPHOS) pathway, which depends on the tight interaction of nuclear- and mitochondrial-encoded genes to function properly. Mitochondrial genes accumulate substitutions more quickly than nuclear genes, yet the impact of selection on mitochondrial genes is significantly reduced relative to nuclear genes because of the non-recombining nature of the mitochondrial genome and its predicted smaller effective population size. It has therefore been hypothesized that the nuclear-encoded genes of the OXPHOS pathway are under strong selective pressure to compensate for the accumulation of deleterious nucleotide substitutions in mitochondrial-encoded OXPHOS genes, a process known as compensatory co-adaptation. We evaluated this hypothesis by analyzing nuclear-encoded OXPHOS genes for signatures of positive selection as well as evolutionary constraints at amino acid sites. We considered OXPHOS genes of six holometabolous insects and their orthologs from three Nasonia parasitoid wasps, the hybrids of which suffer from an increased mortality rate caused by cytonuclear genic incompatibilities. Although nuclear OXPHOS genes are typically highly conserved, we found significant evidence for elevated amino acid divergence in 4 of the 59 studied nuclear-encoded OXPHOS genes. We also found that three of these four genes, as well as six other OXPHOS genes, contain amino acid substitutions between Nasonia species at evolutionarily constrained sites. It is possible that these genes account for the reported incompatibility in Nasonia hybrids and their characterization may lead to a better understanding of the role of positive selection in the genetics of speciation.
Heredity (2010) 104, 310–317
Phylogeography of Nasonia vitripennis (Hymenoptera) indicates a mitochondrial–Wolbachia sweep in North America
R Raychoudhury1,4, B K Grillenberger2,4, J Gadau3, R Bijlsma2, L van de Zande2, J H Werren1,5 and L W Beukeboom2,5 rraychou@mail.rochester.edu
1Department of Biology, University of Rochester; Rochester, NY, USA
2Evolutionary Genetics, Centre for Ecological and Evolutionary Studies, University of Groningen, Haren, The Netherlands
3School of Life Sciences, Arizona State University, Tempe, AZ, USA
Here we report evidence of a mitochondrial–Wolbachia sweep in North American populations of the parasitoid wasp Nasonia vitripennis, a cosmopolitan species and emerging model organism for evolutionary and genetic studies. Analysis of the genetic variation of 89 N. vitripennis specimens from Europe and North America was performed using four types of genetic markers: a portion of the mitochondrial cytochrome oxidase I gene, nine polymorphic nuclear microsatellites, sequences from 11 single-copy nuclear markers and six Wolbachia genes. The results show that the European populations have a sevenfold higher mitochondrial sequence variation than North American populations, but similar levels of microsatellite and nuclear gene sequence variation. Variation in the North American mitochondria is extremely low (π=0.31%), despite a highly elevated mutation rate (~35–40 times higher than the nuclear genes) in the mitochondria of Nasonia. The data are indicative of a mitochondrial sweep in the North American population, possibly due to Wolbachia infections that are maternally co-inherited with the mitochondria. Owing to similar levels of nuclear variation, the data could not resolve whether N. vitripennis originated in the New or the Old World.
Heredity (2010) 104, 318–326
Insect Migration
A single wind-mediated mechanism explains high-altitude ‘non-goal oriented’ headings and layering of nocturnally migrating insects
Andy M. Reynolds1,*, Don R. Reynolds2,1, Alan D. Smith1 and Jason W. Chapman1 andy.reynolds@bbsrc.ac.uk
1Rothamsted Research,Harpenden, Hertfordshire AL5 2JQ, UK
2Natural Resources Institute, University of Greenwich,Chatham, Kent ME4 4TB, UK
Studies made with both entomological and meteorological radars over the last 40 years have frequently reported the occurrence of insect layers, and that the individuals forming these layers often show a considerable degree of uniformity in their headings—behaviour known as ‘common orientation’. The environmental cues used by nocturnal migrants to select and maintain common headings, while flying in low illumination levels at great heights above the ground, and the adaptive benefits of this behaviour have long remained a mystery. Here we show how a wind-mediated mechanism accounts for the common orientation patterns of ‘medium-sized’ nocturnal insects. Our theory posits a mechanism by which migrants are able to align themselves with the direction of the flow using a turbulence cue, thus adding their air speed to the wind speed and significantly increasing their migration distance. Our mechanism also predicts that insects flying in the Northern Hemisphere will typically be offset to the right of the mean wind line when the atmosphere is stably stratified, with the Ekman spiral in full effect. We report on the first evidence for such offsets, and show that they have significant implications for the accurate prediction of the flight trajectories of migrating nocturnal insects.
Proc. R. Soc. B 7 March 2010 vol. 277 no. 1682 765-772
Insect Molecular Ecology
Spatial and temporal changes in genetic structure of greenhouse and field populations of cabbage looper, Trichoplusia ni
*Department of Zoology, University of British Columbia, 2370-6270 University Blvd., Vancouver, BC, Canada V6T 1Z4 , †Department of Forest Sciences, Genetic Data Centre, University of British Columbia, 3611-2424 Main Mall, Vancouver, BC, Canada V6T 1Z4
Trichoplusia ni is a subtropical moth that migrates annually from southern California to southern British Columbia, Canada where it invades vegetable greenhouses and field crops. The heated greenhouse environment has altered the natural extinction–recolonization dynamics of T. ni populations, and allows year-round persistence in some locations. In addition, the extensive use of the biopesticide, Bacillus thuringiensis subspecies kurstaki (Bt) in some greenhouses has selected for resistance. Here we investigated the genetic structure of T. ni populations in British Columbia greenhouses and in field populations in California and British Columbia using amplified fragment length polymorphisms (AFLP) as related to patterns of Bt resistance. The majority of British Columbia field populations were similar to the California field populations, the potential source of migrants. However populations in two geographic areas with high concentrations of greenhouses showed local genetic differentiation. Some of these populations experienced severe bottlenecks over-winter and following Bt sprays. Greenhouse populations showed a pattern of isolation by distance and a strong positive relationship between genetic differentiation and levels of Bt resistance. These patterns indicate that greenhouses that sometimes support year-round populations of T. ni and the ensuing strong bottlenecking effects following winter cleanups and Bt application cause genetic differentiation of T. ni populations. Long distance migrants to field populations contribute to genetic homogeneity of these.
Changes in reproductive roles are associated with changes in gene expression in fire ant queens
Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland
In species with social hierarchies, the death of dominant individuals typically upheaves the social hierarchy and provides an opportunity for subordinate individuals to become reproductives. Such a phenomenon occurs in the monogyne form of the fire ant, Solenopsis invicta, where colonies typically contain a single wingless reproductive queen, thousands of workers and hundreds of winged nonreproductive virgin queens. Upon the death of the mother queen, many virgin queens shed their wings and initiate reproductive development instead of departing on a mating flight. Workers progressively execute almost all of them over the following weeks. To identify the molecular changes that occur in virgin queens as they perceive the loss of their mother queen and begin to compete for reproductive dominance, we collected virgin queens before the loss of their mother queen, 6 h after orphaning and 24 h after orphaning. Their RNA was extracted and hybridized against microarrays to examine the expression levels of approximately 10 000 genes. We identified 297 genes that were consistently differentially expressed after orphaning. These include genes that are putatively involved in the signalling and onset of reproductive development, as well as genes underlying major physiological changes in the young queens.
Geographic parthenogenesis and the common tea-tree stick insect of New Zealand
*Ecology Group, Allan Wilson Center for Molecular Ecology and Evolution, INR, Massey University, Palmerston North, New Zealand , †Department of Conservation, Wellington, New Zealand
Worldwide, parthenogenetic reproduction has evolved many times in the stick insects (Phasmatidae). Many parthenogenetic stick insects show the distribution pattern known as geographic parthenogenesis, in that they occupy habitats that are at higher altitude or latitude compared with their sexual relatives. Although it is often assumed that, in the short term, parthenogenetic populations will have a reproductive advantage over sexual populations; this is not necessarily the case. We present data on the distribution and evolutionary relationships of sexual and asexual populations of the New Zealand stick insect, Clitarchus hookeri. Males are common in the northern half of the species' range but rare or absent elsewhere, and we found that most C. hookeri from putative-parthenogenetic populations share a common ancestor. Female stick insects from bisexual populations of Clitarchus hookeri are capable of parthenogenetic reproduction, but those insects from putative-parthenogenetic populations produced few offspring via sexual reproduction when males were available. We found similar fertility (hatching success) in mated and virgin females. Mated females produce equal numbers of male and female offspring, with most hatching about 9–16 weeks after laying. In contrast, most eggs from unmated females took longer to hatch (21–23 weeks), and most offspring were female. It appears that all C. hookeri females are capable of parthenogenetic reproduction, and thus could benefit from the numerical advantage this yields. Nevertheless, our phylogeographic evidence shows that the majority of all-female populations over a wide geographic area originate from a single loss of sexual reproduction.
Characterization of a hotspot for mimicry: assembly of a butterfly wing transcriptome to genomic sequence at the HmYb/Sb locus
LAURA FERGUSON*, SIU FAI LEE¶, NICOLA CHAMBERLAIN†, NICOLA NADEAU*, MATHIEU JORON‡, SIMON BAXTER*, PAUL WILKINSON**, ALEXIE PAPANICOLAOU**, SUJAI KUMAR§, THUAN-JIN KEE¶, RICHARD CLARK††, CLAIRE DAVIDSON††, REBECCA GLITHERO††, HELEN BEASLEY††, HEIKO VOGEL‡‡, RICHARD FFRENCH-CONSTANT** and CHRIS JIGGINS* cj107@cam.ac.uk
* Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK , † Harvard FAS Center for Systems Biology, Northwest Lab Building, 52 Oxford Street, Cambridge, MA 02138, USA , ‡ CNRS UMR5202, Case postale 29, 16, rue Buffon, 75005 Paris, France , § Ashworth Laboratories, University of Edinburgh, West Mains Road, EH9 3JT Scotland , ¶ Department of Genetics, Bio21 Institute, University of Melbourne, 30 Flemington Road, Parkville, Melbourne, Australia , ** School of Biosciences, University of Exeter in Cornwall, Penryn, Cornwall TR10 9EZ, UK , †† The Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK , ‡‡ Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, D-07745 Jena, Germany
The mimetic wing patterns of Heliconius butterflies are an excellent example of both adaptive radiation and convergent evolution. Alleles at the HmYb and HmSb loci control the presence/absence of hindwing bar and hindwing margin phenotypes respectively between divergent races of Heliconius melpomene, and also between sister species. Here, we used fine-scale linkage mapping to identify and sequence a BAC tilepath across the HmYb/Sb loci. We also generated transcriptome sequence data for two wing pattern forms of H. melpomene that differed in HmYb/Sb alleles using 454 sequencing technology. Custom scripts were used to process the sequence traces and generate transcriptome assemblies. Genomic sequence for the HmYb/Sb candidate region was annotated both using the MAKER pipeline and manually using transcriptome sequence reads. In total, 28 genes were identified in the HmYb/Sb candidate region, six of which have alternative splice forms. None of these are orthologues of genes previously identified as being expressed in butterfly wing pattern development, implying previously undescribed molecular mechanisms of pattern determination on Heliconius wings. The use of next-generation sequencing has therefore facilitated DNA annotation of a poorly characterized genome, and generated hypotheses regarding the identity of wing pattern at the HmYb/Sb loci.
Genetic association of physically unlinked islands of genomic divergence in incipient species of Anopheles gambiae
BRADLEY J. WHITE*, CHANGDE CHENG*, FREDERIC SIMARD†, CARLO COSTANTINI‡ and NORA J. BESANSKY* nbesansk@nd.edu
*Department of Biological Sciences, Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN 46556, USA , †Institut de Recherche pour le Développement (IRD), UR016, and Institut de Recherche en Sciences de la Santé (IRSS) B.P. 171, Bobo Dioulasso, Burkina Faso , ‡Institut de Recherche pour le Développement (IRD), UR016, and Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), B.P. 288, Yaoundé, Cameroon
Previous efforts to uncover the genetic underpinnings of ongoing ecological speciation of the M and S forms of the African malaria vector Anopheles gambiae revealed two centromere-proximal islands of genetic divergence on X and chromosome 2. Under the assumption of considerable ongoing gene flow between M and S, these persistently divergent genomic islands were widely considered to be 'speciation islands'. In the course of microarray-based divergence mapping, we discovered a third centromere-associated island of divergence on chromosome 3, which was validated by targeted re-sequencing. To test for genetic association between the divergence islands on all three chromosomes, SNP-based assays were applied in four natural populations of M and S spanning West, Central and East Africa. Genotyping of 517 female M and S mosquitoes revealed nearly complete linkage disequilibrium between the centromeres of the three independently assorting chromosomes. These results suggest that despite the potential for inter-form gene flow through hybridization, actual (realized) gene flow between M and S may be substantially less than commonly assumed and may not explain most shared variation. Moreover, the possibility of very low gene flow calls into question whether diverged pericentromeric regions—characterized by reduced levels of variation and recombination—are in fact instrumental rather than merely incidental to the speciation process.
Insect Neuroscience
Phenotypic plasticity in number of glomeruli and sensory innervation of the antennal lobe in leaf-cutting ant workers (A. vollenweideri)
Christina Kelber, Wolfgang Rössler, Christoph Johannes Kleineidam * kleineidam@biozentrum.uni-wuerzburg.de
Department of Behavioral Physiology and Sociobiology, Biozentrum, University of Würzburg, Würzburg, Germany
In the leaf-cutting ant Atta vollenweideri, the worker caste exhibits a pronounced size-polymorphism, and division of labor is dependent on worker size (alloethism). Behavior is largely guided by olfaction, and the olfactory system is highly developed. In a recent study, two different phenotypes of the antennal lobe of Atta vollenweideri workers were found: MG- and RG-phenotype (with/without a macroglomerulus). Here we ask whether the glomerular numbers are related to worker size. We found that the antennal lobes of small workers contain 390 glomeruli (low-number; LN-phenotype), and in large workers we found a substantially higher number of 440 glomeruli (high-number; HN-phenotype). All LN-phenotype workers and some small HN-phenotype workers do not possess an MG (LN-RG-phenotype and HN-RG-phenotype), and the remaining majority of HN-phenotype workers do possess an MG (HN-MG-phenotype). Using mass-staining of antennal olfactory receptor neurons we found that the sensory tracts divide the antennal lobe into six clusters of glomeruli (T1-T6). In LN-phenotype workers, 50 glomeruli are missing in the T4-cluster. Selective staining of single sensilla and their associated receptor neurons revealed that T4-glomeruli are innervated by receptor neurons from the main type of olfactory sensilla, the Sensilla trichodea curvata. The other type of olfactory sensilla (Sensilla basiconica) exclusively innervates T6-glomeruli. Quantitative analyses of differently sized workers revealed that the volume of T6 glomeruli scales with the power of 2.54 to the number of Sensilla basiconica. The results suggest that developmental plasticity leading to antennal-lobe phenotypes promotes differences in olfactory-guided behavior and may underlie task specialization within ant colonies. © 2009 Wiley Periodicals, Inc.
Develop Neurobiol 70: 222-234, 2010.
Localization of a GABA transporter to glial cells in the developing and adult olfactory pathway of the moth Manduca sexta
Lynne A. Oland *, Nicholas J. Gibson, Leslie P. Tolbert lao@neurobio.arizona.edu
Department of Neuroscience, University of Arizona, Tucson, Arizona 85721
Glial cells have several critical roles in the developing and adult olfactory (antennal) lobe of the moth Manduca sexta. Early in development, glial cells occupy discrete regions of the developing olfactory pathway and processes of -aminobutyric acid (GABA)ergic neurons extend into some of these regions. Because GABA is known to have developmental effects in a variety of systems, we explored the possibility that the glial cells express a GABA transporter that could regulate GABA levels to which olfactory neurons and glial cells are exposed. By using an antibody raised against a characterized high-affinity M. sexta GABA transporter with high sequence homology to known mammalian GABA transporters (Mbungu et al. [[1995]] Arch. Biochem. Biophys. 318:489-497; Umesh and Gill [[2002]] J. Comp. Neurol. 448:388-398), we found that the GABA transporter is localized to subsets of centrally derived glial cells during metamorphic adult development. The transporter persists into adulthood in a subset of the neuropil-associated glial cells, but its distribution pattern as determined by light-and electron-microscopic-level immunocytochemistry indicates that it could not serve to regulate GABA concentration in the synaptic cleft. Instead, its role is more likely to regulate extracellular GABA levels within the glomerular neuropil. Expression in the sorting zone glial cells disappears after the period of olfactory receptor axon ingrowth, but may be important during ingrowth if GABA regulates axon growth. Glial cells take up GABA, and that uptake can be blocked by L-2,4-diaminobutyric acid (DABA). This is the first molecular evidence that the central glial cell population in this pathway is heterogeneous.
J. Comp. Neurol. 518:815-838, 2010
Insect Neurothology
Wide-field motion tuning in nocturnal hawkmoths
Nocturnal hawkmoths are known for impressive visually guided behaviours in dim light, such as hovering while feeding from nectar-bearing flowers. This requires tight visual feedback to estimate and counter relative motion. Discrimination of low velocities, as required for stable hovering flight, is fundamentally limited by spatial resolution, yet in the evolution of eyes for nocturnal vision, maintenance of high spatial acuity compromises absolute sensitivity. To investigate these trade-offs, we compared responses of wide-field motion-sensitive neurons in three species of hawkmoth: Manduca sexta (a crepuscular hoverer), Deilephila elpenor (a fully nocturnal hoverer) and Acherontia atropos (a fully nocturnal hawkmoth that does not hover as it feeds uniquely from honey in bees' nests). We show that despite smaller eyes, the motion pathway of D. elpenor is tuned to higher spatial frequencies and lower temporal frequencies than A. atropos, consistent with D. elpenor's need to detect low velocities for hovering. Acherontia atropos, however, presumably evolved low-light sensitivity without sacrificing temporal acuity. Manduca sexta, active at higher light levels, is tuned to the highest spatial frequencies of the three and temporal frequencies comparable with A. atropos. This yields similar tuning to low velocities as in D. elpenor, but with the advantage of shorter neural delays in processing motion.
Proc. R. Soc. B 22 March 2010 vol. 277 no. 1683 853-860
Insect Olfaction
Expression Analysis of the 3 G-Protein Subunits, G, Gβ, and G, in the Olfactory Receptor Organs of Adult Drosophila melanogaster
Tamara Boto, Carolina Gomez-Diaz and Esther Alcorta
Department of Functional Biology, Faculty of Medicine, University of Oviedo, Julian Claveria s/n, 33006 Oviedo, Spain
Correspondence to be sent to: Esther Alcorta, Department of Functional Biology, Faculty of Medicine, University of Oviedo, Julian Claveria s/n, 33006 Oviedo, Spain. e-mail: ealcorta@uniovi.es
In many species, olfactory transduction is triggered by odorantmolecules that interact with olfactory receptors coupled toheterotrimeric G-proteins. The role of G-protein–linkedtransduction in the olfaction of Drosophila is currently understudy. Here, we supply a thorough description of the expressionin the olfactory receptor organs (antennae and maxillary palps)of all known Drosophila melanogaster genes that encode for G-proteins.Using RT-polymerase chain reaction, we analyzed 6 G(Gs, Gi,Gq, Go, Gf, and concertina), 3 Gβ (Gβ5, Gβ13F,and Gβ76C), and 2 Ggenes (G1 and G30A). We found thatall Gprotein-encoding genes showed expression in both olfactoryorgans, but Gf mRNA was not detected in palps. Moreover, allthe Gβ and Ggenes are expressed in antennae and palps,except for Gβ76C. To gain insight into the hypothesis ofdifferent G-protein subunits mediating differential signalingin olfactory receptor neurons (ORNs), we performed immunohistochemicalstudies to observe the expression of several Gand Gβ proteins.We found that Gs, Gi, Gq, and Gβ13F subunits displayedgeneralized expression in the antennal tissue, including ORNssupport cells and glial cells. Finally, complete coexpressionwas found between Gi and Gq, which are mediators of the cyclicadenosine monophosphate and IP3 transduction cascades, respectively.
Chemical Senses 2010 35(3):183-193; doi:10.1093/chemse/bjp095
Characterization of the Antennal Olfactory System of the Bed Bug (Cimex lectularius)
Vincent Harraca1,2, Rickard Ignell2, Christer Löfstedt1 and Camilla Ryne1 camilla.ryne@ekol.lu.se
1 Division of Chemical Ecology, Department of Ecology, Ecology Building, Lund University, SE-223 62 Lund, Sweden 2 Division of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Box 102, SE-230 53 Alnarp, Sweden
The common bed bug Cimex lectularius (Hemiptera; Cimicidae)is a temporary ectoparasite on humans that is currently reinvadingthe developed countries. Like other haematophagous arthropods,host seeking and orientation in C. lectularius is partiallymediated by olfaction. In this study, we reconfirmed the distributionof the 44 olfactory sensilla and identified 3 different sensillumtypes located at the distal tip of C. lectularius antenna byexternal morphology mapping. Using a panel of relevant odorantspreviously reported to be bioactive in various haematophagousarthropods, we correlated the morphological mapping with anelectrophysiological characterization of the olfactory receptorneurons housed in each specific sensillum. We found that all9 grooved peg sensilla responded specifically in a dose-dependentmanner to ammonia, whereas (E)-2-hexenal, (E)-2-octenal, dimethyltrisulfide, 6-methyl-5-hepten-2-one, -pinene, indole, and ethylbutyrate evoked dose-dependent responses within the 6 smoothpeg sensilla. Based on the pattern of response to the testedcompounds, we were able to separate the 6 smooth peg sensillaof the bed bug into 3 distinct functional classes. We compareour results with previous electrophysiological recordings madewith these compounds on other haematophagous arthropods.
Chemical Senses 2010 35(3):195-204; doi:10.1093/chemse/bjp096
Perfusion with cAMP analogue affects pheromone-sensitive trichoid sensilla of the hawkmoth Manduca sexta in a time-dependent manner
1 Biologie, Tierphysiologie, Philipps-Universität Marburg, 35032 Marburg, Germany
2 Biologie, Tierphysiologie, Universität Kassel, 34132 Kassel, Germany
2 Biologie, Tierphysiologie, Universität Kassel, 34132 Kassel, Germany
Octopamine causes time-dependent disadaptation of pheromone-sensitiveolfactory receptor neurons (ORNs) of Manduca sexta. Becausethe majority of insect octopamine receptors are positively coupledto adenylyl cyclases we examined whether cyclic adenosine monophosphate(cAMP) mimics octopamine-dependent modulation of pheromone transductionin a time-dependent manner. Long-term tip recordings of singletrichoid sensilla of Manduca sexta were performed during threezeitgeber times (ZTs, ZT 0=lights on), while stimulating thesensilla with two doses of the main pheromone component bombykalin a non-adapting protocol. The membrane-permeable cAMP analogue8bcAMP increased the normalized sensillar potential amplitudein a time- and bombykal dose-dependent way. At the higher bombykaldose only, the applied 8bcAMP antagonized an endogenous decreasein the mean sensillar potential amplitude at ZT 1-4 and ZT 8-11when ORNs were adapted but not at ZT 22-1, when ORNs were sensitized.In contrast to octopamine, 8bcAMP did not consistently affectthe initial pheromone-dependent action potential frequency,the phasic/tonic response pattern, or the time-dependent shiftto lower mean action potential frequencies at ZT 8-11. Furthermore,8bcAMP increased the spontaneous action potential frequencytime dependently, but differently from octopamine. In conclusion,our results show that cAMP only partly mimics the octopamine-dependentdisadaptation of olfactory receptor neurons during photophase,apparently due to another missing octopamine-dependent synergisticfactor such as defined intracellular calcium levels.
Journal of Experimental Biology 213, 842-852 (2010)
http://jeb.biologists.org/cgi/content/abstract/213/5/842
http://jeb.biologists.org/cgi/content/abstract/213/5/842
Insect Pathology
Mixed genotype transmission bodies and virions contribute to the maintenance of diversity in an insect virus
Gabriel Clavijo1,2, Trevor Williams3, Delia Muñoz1,2, Primitivo Caballero1,2 and Miguel López-Ferber4,*miguel.lopez-ferber@mines-ales.fr
Laboratorio de Entomología Agrícola y Patología de Insectos, epartamento de Producción Agraria, Universidad Pública de Navarra, Pamplona, Spain
2Instituto de Agrobiotecnología, CSIC, Gobierno de Navarra, Mutilva Baja, Spain
3Instituto de Ecología AC,Xalapa, Veracruz, Mexico
4 Laboratoire de Gènie de l'Environnement Industriel, Ecole des Mines d'Alès, Alès, France
An insect nucleopolyhedrovirus naturally survives as a mixture of at least nine genotypes. Infection by multiple genotypes results in the production of virus occlusion bodies (OBs) with greater pathogenicity than those of any genotype alone. We tested the hypothesis that each OB contains a genotypically diverse population of virions. Few insects died following inoculation with an experimental two-genotype mixture at a dose of one OB per insect, but a high proportion of multiple infections were observed (50%), which differed significantly from the frequencies predicted by a non-associated transmission model in which genotypes are segregated into distinct OBs. By contrast, insects that consumed multiple OBs experienced higher mortality and infection frequencies did not differ significantly from those of the non-associated model. Inoculation with genotypically complex wild-type OBs indicated that genotypes tend to be transmitted in association, rather than as independent entities, irrespective of dose. To examine the hypothesis that virions may themselves be genotypically heterogeneous, cell culture plaques derived from individual virions were analysed to reveal that one-third of virions was of mixed genotype, irrespective of the genotypic composition of the OBs. We conclude that co-occlusion of genotypically distinct virions in each OB is an adaptive mechanism that favours the maintenance of virus diversity during insect-to-insect transmission.
Proc. R. Soc. B 22 March 2010 vol. 277 no. 1683 943-951
Insect Society
Colony fusion and worker reproduction after queen loss in army ants
Daniel J. C. Kronauer*†, Caspar Schöning‡, Patrizia d'Ettorre and Jacobus J. Boomsmadkron@fas.harvard.edu
Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark
Theory predicts that altruism is only evolutionarily stable if it is preferentially directed towards relatives, so that any such behaviour towards seemingly unrelated individuals requires scrutiny. Queenless army ant colonies, which have anecdotally been reported to fuse with queenright foreign colonies, are such an enigmatic case. Here we combine experimental queen removal with population genetics and cuticular chemistry analyses to show that colonies of the African army ant Dorylus molestus frequently merge with neighbouring colonies after queen loss. Merging colonies often have no direct co-ancestry, but are on average probably distantly related because of overall population viscosity. The alternative of male production by orphaned workers appears to be so inefficient that residual inclusive fitness of orphaned workers might be maximized by indiscriminately merging with neighbouring colonies to increase their reproductive success. We show that worker chemical recognition profiles remain similar after queen loss, but rapidly change into a mixed colony Gestalt odour after fusion, consistent with indiscriminate acceptance of alien workers that are no longer aggressive. We hypothesize that colony fusion after queen loss might be more widespread, especially in spatially structured populations of social insects where worker reproduction is not profitable.
Proc. R. Soc. B 7 March 2010 vol. 277 no. 1682 755-763
Insect Review
A meta-analysis of insect pest behavioral manipulation with plant volatiles
Rutgers, The State University of New Jersey, P.E. Marucci Center for Blueberry and Cranberry Research and Extension, 125A Lake Oswego Road, Chatsworth, NJ 08019, USA
Many insect pests utilize plant volatiles for host location and untangling the mechanisms of this process can provide tools for pest management. Numerous experimental results have been published on the effect of plant volatiles on insect pests. We used a meta-analysis to summarize this knowledge and to look for patterns. Our goal was to identify herbivore and plant traits that might explain the herbivores' behavioral response to plant volatiles in field applications. We scored a total of 374 unique plant volatile-insect herbivore interactions obtained from 34 published studies investigating 50 herbivore pest species. Attractants had a significant effect on insect herbivore abundance but repellents did not; this latter result could be a result of the comparatively small number of field studies that tested plant volatiles as repellents (3%). Females were significantly more attracted to plant volatile baits than males. The diet breadth of herbivores was independent of a behavioral response to plant volatiles, but more case studies show effects of volatiles on chewers, followed by wood-borers and sap-feeders. There are more demonstrations of attraction to plant volatiles in Lepidoptera than in Thysanoptera. The method of plant volatile application had a significant effect on herbivore abundance and increasing the number of chemicals in individual baits attracted more herbivores. The magnitude of the response of herbivores to plant volatiles in forest and agricultural habitats was similar. We explore consistent patterns and highlight areas needing research in using plant volatiles to manage insect pests.
Olfactory signalling in vertebrates and insects: differences and commonalities
Center of Advanced European Studies and Research, Ludwig-Erhard-Allee 2, 53175 Bonn, Germany.
Vertebrates and insects have evolved complex repertoires of chemosensory receptors to detect and distinguish odours. With a few exceptions, vertebrate chemosensory receptors belong to the family of G protein-coupled receptors that initiate a cascade of cellular signalling events and thereby electrically excite the neuron. Insect receptors, which are structurally and genetically unrelated to vertebrate receptors, are a complex of two distinct molecules that serves both as a receptor for the odorant and as an ion channel that is gated by binding of the odorant. Metabotropic signalling in vertebrates provides a rich panoply of positive and negative regulation, whereas ionotropic signalling in insects enhances processing speed.
Nature Reviews Neuroscience 11, 188-200 (March 2010)
Insect Frontiers Mar 2010 Vol2 No3 PDF final
Insect Frontiers, February 2010 Volume 2 Number 2 http://www.sciencenet.cn/m/user_content.aspx?id=276423Insect Frontiers, January 2010 Volume 2 Number 1 http://www.sciencenet.cn/m/user_content.aspx?id=276422
Insect Frontiers, December 2009 Volume 1 Number2 http://www.sciencenet.cn/m/user_content.aspx?id=274511
Insect Frontiers, November 2009 Volume 1 Number 1 http://www.sciencenet.cn/m/user_content.aspx?id=270398
https://blog.sciencenet.cn/blog-278346-298300.html
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