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Aphids are important agricultural pests and also biological models for studies of insect-plant interactions, symbiosis, virus vectoring, and the developmental causes of extreme phenotypic plasticity. Here we present the 464 Mb draft genome assembly of the pea aphid Acyrthosiphon pisum. This first published whole genome sequence of a basal hemimetabolous insect provides an outgroup to the multiple published genomes of holometabolous insects. Pea aphids are host-plant specialists, they can reproduce both sexually and asexually, and they have coevolved with an obligate bacterial symbiont. Here we highlight findings from whole genome analysis that may be related to these unusual biological features. These findings include discovery of extensive gene duplication in more than 2000 gene families as well as loss of evolutionarily conserved genes. Gene family expansions relative to other published genomes include genes involved in chromatin modification, miRNA synthesis, and sugar transport. Gene losses include genes central to the IMD immune pathway, selenoprotein utilization, purine salvage, and the entire urea cycle. The pea aphid genome reveals that only a limited number of genes have been acquired from bacteria; thus the reduced gene count of Buchnera does not reflect gene transfer to the host genome. The inventory of metabolic genes in the pea aphid genome suggests that there is extensive metabolite exchange between the aphid and Buchnera, including sharing of amino acid biosynthesis between the aphid and Buchnera. The pea aphid genome provides a foundation for post-genomic studies of fundamental biological questions and applied agricultural problems.

Climate change can affect species directly and indirectly by altering interactions between species within communities. These indirect effects can ramify through a community and affect many species, including some that may not have been directly affected by the perturbation. Identifying these chains of indirect effects is difficult, and most studies only follow indirect effects across two or three species. Here, we use a factorial field experiment to demonstrate that precipitation affects spotted aphids through a complex chain of indirect interactions that are mediated by other herbivores and a generalist predator. We experimentally simulated drought, which reduced water content in alfalfa plants. While water stress in alfalfa had no direct effect on spotted aphids, it lowered the population growth rate of pea aphids, another common alfalfa pest. Because ladybeetle predators were attracted to high pea aphid densities, predator densities were lower in drought treatments. Consequently, spotted aphid densities were released from top-down control (apparent competition) in drought treatments and reached densities three times higher than spotted aphids in ambient treatments with high pea aphid densities. Thus, drought affected spotted aphids in the interaction chain: drought → alfalfa → pea aphids → predators → spotted aphids. This result illustrates the lengthy path that indirect effects of climate change may take through a community, as well as the importance of community-level experiments in determining the net effect of climate change.

Almost all aphids harbour an endosymbiotic bacterium, Buchnera aphidicola, in bacteriocytes. Buchnera synthesizes essential nutrients and supports growth and reproduction of the host. Over the long history of endosymbiosis, many essential genes have been lost from the Buchnera genome, resulting in drastic genome reduction and the inability to live outside the host cells. In turn, when deprived of Buchnera, the host aphid suffers retarded growth and sterility. Buchnera and the host aphid are often referred to as highly integrated almost inseparable mutualistic partners. However, we discovered that, even after complete elimination of Buchnera, infection with a facultative endosymbiotic γ-proteobacterium called pea aphid secondary symbiont (PASS) enabled survival and reproduction of the pea aphid. In the Buchnera-free aphid, PASS infected the cytoplasms of bacteriocytes that normally harbour Buchnera, establishing a novel endosymbiotic system. These results indicate that PASS can compensate for the essential role of Buchnera by physiologically and cytologically taking over the symbiotic niche. By contrast, PASS negatively affected the growth and reproduction of normal host aphids by suppressing the essential symbiont Buchnera. These findings illuminate complex symbiont-symbiont and host-symbiont interactions in an endosymbiotic system, and suggest a possible evolutionary route to novel obligate endosymbiosis by way of facultative endosymbiotic associations.

Background Although sexual reproduction is dominant within eukaryotes, asexual reproduction is widespread and has evolved independently as a derived trait in almost all major taxa. How asexuality evolved in sexual organisms is unclear. Aphids, such as Acyrthosiphon pisum , alternate between asexual and sexual reproductive means, as the production of parthenogenetic viviparous females or sexual oviparous females and males varies in response to seasonal photoperiodism. Consequently, sexual and asexual development in aphids can be analyzed simultaneously in genetically identical individuals. Results We compared the transcriptomes of aphid embryos in the stages of development during which the trajectory of oogenesis is determined for producing sexual or asexual gametes. This study design aimed at identifying genes involved in the onset of the divergent mechanisms that result in the sexual or asexual phenotype. We detected 33 genes that were differentially transcribed in sexual and asexual embryos. Functional annotation by gene ontology (GO) showed a biological signature of oogenesis, cell cycle regulation, epigenetic regulation and RNA maturation. In situ hybridizations demonstrated that 16 of the differentially-transcribed genes were specifically expressed in germ cells and/or oocytes of asexual and/or sexual ovaries, and therefore may contribute to aphid oogenesis. We categorized these 16 genes by their transcription patterns in the two types of ovaries; they were: i) expressed during sexual and asexual oogenesis; ii) expressed during sexual and asexual oogenesis but with different localizations; or iii) expressed only during sexual or asexual oogenesis. Conclusions Our results show that asexual and sexual oogenesis in aphids share common genetic programs but diverge by adapting specificities in their respective gene expression profiles in germ cells and oocytes.

Transitions from sexual to asexual reproduction are common in eukaryotes, but the underlying mechanisms remain poorly known. The pea aphid--Acyrthosiphon pisum--exhibits reproductive polymorphism, with cyclical parthenogenetic and obligate parthenogenetic lineages, offering an opportunity to decipher the genetic basis of sex loss. Previous work on this species identified a single 840 kb region controlling reproductive polymorphism and carrying 32 genes. With the aim of identifying the gene(s) responsible for sex loss and the resulting consequences on the genetic programs controlling sexual or asexual embryogenesis, we compared the transcriptomic response to photoperiod shortening--the main sex-inducing cue--of a sexual and an obligate asexual lineage of the pea aphid, focusing on heads (where the photoperiodic cue is detected) and embryos (the final target of the cue). Our analyses revealed that four genes (one expressed in the head, and three in the embryos) of the region responded differently to photoperiod in the two lineages. We also found that the downstream genetic programs expressed during embryonic development of a future sexual female encompass \\1600 genes, among which miRNAs, piRNAs and histone modification pathways are overrepresented. These genes mainly co-localize in two genomic regions enriched in transposable elements (TEs). Our results suggest that the causal polymorphism(s) in the 840 kb region somehow impair downstream epigenetic and post-transcriptional regulations in obligate asexual lineages, thereby sustaining asexual reproduction.

Climatic changes, such as heatwaves, pose unprecedented challenges for insects, as escalated temperatures above the thermal optimum alter insect reproductive strategies and energy metabolism. While thermal stress responses have been reported in different insect species, thermo-induced developmental abnormalities in phloem-feeding pests are largely unknown. In this laboratory study, we raised two groups of first instar nymphs belonging to two clones of the pea aphid Acyrthosiphon pisum, on fava beans Vicia faba. The instars developed and then asexually reproduced under constant exposure to a sub-lethal heatwave (27°C) for 14 days. Most mothers survived but their progenies showed abnormalities, as stillbirths and appendageless or weak nymphs with folded appendages were delivered. Clone N116 produced more deceased and appendageless embryos, contrary to N127, which produced fewer dead and more malformed premature embryos. Interestingly, the expression of the HSP70 and HSP83 genes differed in mothers between the clones. Moreover, noticeable changes in metabolism, e.g., lipids, were also detected and that differed in response to stress. Deformed offspring production after heat exposure may be due to heat injury and differential HSP gene expression, but may also be indicative of a conflict between maternal and offspring fitness. Reproductive altruism might have occurred to ensure some of the genetically identical daughters survive. This is because maintaining homeostasis and complete embryogenesis could not be simultaneously fulfilled due to the high costs of stress. Our findings shine new light on pea aphid responses to heatwaves and merit further examination across different lineages and species.

The wing polyphenism of pea aphids is a compelling laboratory model with which to study the molecular mechanisms underlying phenotypic plasticity. In this polyphenism, environmental stressors such as high aphid density cause asexual, viviparous adult female aphids to alter the developmental fate of their embryos from wingless to winged morphs. This polyphenism is transgenerational, in that the pea aphid mother experiences the environmental signals, but it is her offspring that are affected. Previous research suggested that the steroid hormone ecdysone may play a role in this polyphenism. Here, we analyzed ecdysone-related gene expression patterns and found that they were consistent with a down-regulation of the ecdysone pathway being involved in the production of winged offspring. We therefore predicted that reduced ecdysone signaling would result in more winged offspring. Experimental injections of ecdysone or its analog resulted in a decreased production of winged offspring. Conversely, interfering with ecdysone signaling using an ecdysone receptor antagonist or knocking down the ecdysone receptor gene with RNAi resulted in an increased production of winged offspring. Our results are therefore consistent with the idea that ecdysone plays a causative role in the regulation of the proportion of winged offspring produced in response to crowding in this polyphenism. Our results also show that an environmentally regulated maternal hormone can mediate phenotype production in the next generation, as well as provide significant insight into the molecular mechanisms underlying the functioning of transgenerational phenotypic plasticity.