A highly infective plant-associated bacterium influences reproductive rates in pea aphids.
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ABSTRACT:
SUBMITTER: Hendry TA
PROVIDER: S-EPMC4785972 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:A key focus of evolutionary developmental biology is on how phenotypic diversity is generated. In particular, both plasticity and developmental instability contribute to phenotypic variation among genetically identical individuals, but the interactions between the two phenomena and their general fitness impacts are unclear. We discovered a striking example of asymmetry in pea aphids: the presence of wings on one side and the complete or partial absence of wings on the opposite side. We used this asymmetric phenotype to study the connection between plasticity, developmental instability and fitness. We found that this asymmetric wing development (i) occurred equally on both sides and thus is a developmental instability; (ii) is present in some genetically unique lines but not others, and thus has a genetic basis; and (iii) has intermediate levels of fecundity, and thus does not necessarily have negative fitness consequences. We conclude that this dramatic asymmetry may arise from incomplete switching between developmental targets, linking plasticity and developmental instability. We suspect that what we have observed may be a more widespread phenomenon, occurring across species that routinely produce distinct, alternative phenotypes.
| S-EPMC7661304 | biostudies-literature
Project description:Environmental stressors can be key drivers of phenotypes, including reproductive strategies and morphological traits. The response to stress may be altered by the presence of microbial associates. For example, in aphids, facultative (secondary) bacterial symbionts can provide protection against natural enemies and stress induced by elevated temperatures. Furthermore, aphids exhibit phenotypic plasticity, producing winged (rather than wingless) progeny that may be better able to escape danger, and the combination of these factors improves the response to stress. How symbionts and phenotypic plasticity, both of which shape aphids' stress response, influence one another, and together influence host fitness, remains unclear. In this study, we investigate how environmental stressors drive shifts in fecundity and winged/wingless offspring production, and how secondary symbionts influence the process. We induced production of winged offspring through distinct environmental stressors, including exposure to aphid alarm pheromone and crowding, and, in one experiment, we assessed whether the aphid response is influenced by host plant. In the winged morph, energy needed for wing maintenance may lead to trade-offs with other traits, such as reproduction or symbiont maintenance. Potential trade-offs between symbiont maintenance and fitness have been proposed but have not been tested. Thus, beyond studying the production of offspring of alternative morphs, we also explore the influence of symbionts across wing/wingless polyphenism as well as symbiont interaction with cross-generational impacts of environmental stress on reproductive output. All environmental stressors resulted in increased production of winged offspring and shifts in fecundity rates. Additionally, in some cases, aphid host-by-symbiont interactions influenced fecundity. Stress on first-generation aphids had cross-generational impacts on second-generation adults, and the impact on fecundity was further influenced by the presence of secondary symbionts and presence/absence of wings. Our study suggests a complex interaction between beneficial symbionts and environmental stressors. Winged aphids have the advantage of being able to migrate out of danger with more ease, but energy needed for wing production and maintenance may come with reproductive costs for their mothers and for themselves, where in certain cases, these costs are altered by secondary symbionts.
| S-EPMC6453707 | biostudies-literature
Project description:The role of kin-selection in the evolution of post-reproductive life is controversial. While anthropological and demographic studies strongly suggest that humans and a few other species experience kin selection for significant post-reproductive survival, these results are necessarily correlational. Understanding could therefore be advanced by the development of a globally available, field and laboratory tractable experimental model of kin-selected post-reproductive survival. In only one invertebrate (Quadrartus yoshinomiyai, a gall-forming aphid endemic to Japan) have individuals too old to reproduce been shown to be both numerous in natural habitats and able to help close relatives survive or reproduce. Pea aphids, (Acyrthosiphon pisum), common, tractable organisms, frequently outlive their reproductive ages in laboratories, live in tight interacting groups that are often clonal, and therefore should be evaluated as potential model organisms for the study of adaptive post-reproductive life. The first major step in this process is to identify an optimal method for assessing if a parthenogenetic adult is post-reproductive. We evaluated three methods, relying respectively on isolation in clip cages, visual examination for embryonic eyespots, and dissection. In every case each method identified the same individuals as reproductive versus post-reproductive. While the clip-cage method requires a multi-day wait to produce data, and dissection is inevitably fatal, the eyespot method is quick (under one minute per individual) easy, and non-invasive. This method makes it possible to accurately assess the post-reproductive status of a large number of parthenogenetic pea aphids. We demonstrate the usefulness of the eyespot method in showing that while reproductively valuable adults tend to place themselves near the centers of clonal colonies, less valuable post-reproductive adults are more often at or beyond the edges of colonies. These encouraging early results provide both impetuous and aid for further investigations into the post-reproductive lives of pea aphids.
| S-EPMC5088610 | biostudies-literature
Project description:BACKGROUND: Recent genomic analyses of arthropod defense mechanisms suggest conservation of key elements underlying responses to pathogens, parasites and stresses. At the center of pathogen-induced immune responses are signaling pathways triggered by the recognition of fungal, bacterial and viral signatures. These pathways result in the production of response molecules, such as antimicrobial peptides and lysozymes, which degrade or destroy invaders. Using the recently sequenced genome of the pea aphid (Acyrthosiphon pisum), we conducted the first extensive annotation of the immune and stress gene repertoire of a hemipterous insect, which is phylogenetically distantly related to previously characterized insects models. RESULTS: Strikingly, pea aphids appear to be missing genes present in insect genomes characterized to date and thought critical for recognition, signaling and killing of microbes. In line with results of gene annotation, experimental analyses designed to characterize immune response through the isolation of RNA transcripts and proteins from immune-challenged pea aphids uncovered few immune-related products. Gene expression studies, however, indicated some expression of immune and stress-related genes. CONCLUSIONS: The absence of genes suspected to be essential for the insect immune response suggests that the traditional view of insect immunity may not be as broadly applicable as once thought. The limitations of the aphid immune system may be representative of a broad range of insects, or may be aphid specific. We suggest that several aspects of the aphid life style, such as their association with microbial symbionts, could facilitate survival without strong immune protection.
| S-EPMC2872881 | biostudies-literature
Project description:Phenotypic plasticity, the production of alternative phenotypes (or morphs) from the same genotype due to environmental factors, results in some genes being expressed in a morph-biased manner. Theoretically, these morph-biased genes experience relaxed selection, the consequence of which is the buildup of slightly deleterious mutations at these genes. Over time, this is expected to result in increased protein divergence at these genes between species and a signature of relaxed purifying selection within species. Here we test these theoretical expectations using morph-biased genes in the pea aphid, a species that produces multiple morphs via polyphenism. We find that morph-biased genes exhibit faster rates of evolution (in terms of dN/dS) relative to unbiased genes and that divergence generally increases with increasing morph bias. Further, genes with expression biased toward rarer morphs (sexual females and males) show faster rates of evolution than genes expressed in the more common morph (asexual females), demonstrating that the amount of time a gene spends being expressed in a morph is associated with its rate of evolution. And finally, we show that genes expressed in the rarer morphs experience decreased purifying selection relative to unbiased genes, suggesting that it is a relaxation of purifying selection that contributes to their faster rates of evolution. Our results provide an important empirical look at the impact of phenotypic plasticity on gene evolution.
| S-EPMC4104313 | biostudies-literature
Project description:We analysed 12 years of species-specific emergence dates of plants at a Low-Arctic site near Kangerlussuaq, Greenland to investigate associations with sea ice dynamics, a potential contributor to local temperature variation in near-coastal tundra. Species displayed highly variable rates of phenological advance, from a maximum of -2.55 ± 0.17 and -2.93 ± 0.51 d yr-1 among a graminoid and forb, respectively, to a minimum of -0.55 ± 0.19 d yr-1 or no advance at all in the two deciduous shrub species. Monthly Arctic-wide sea ice extent was a significant predictor of emergence timing in 10 of 14 species. Despite variation in rates of advance among species, these rates were generally greatest in the earliest emerging species, for which monthly sea ice extent was also the primary predictor of emergence. Variation among species in rates of phenological advance reshuffled the phenological community, with deciduous shrubs leafing out progressively later relative to forbs and graminoids. Because early species advanced more rapidly than late species, and because rates of advance were greatest in species for which emergence phenology was associated with sea ice dynamics, accelerating sea ice decline may contribute to further divergence between early- and late-emerging species in this community.
| S-EPMC5206582 | biostudies-literature
Project description:Wing dimorphism, that is, wingless and winged forms, can be induced by maternal stress signals and is an adaptive response of aphids to environmental changes. Here, we investigated the ecological and molecular effects of three kinds of stress, namely crowding, predation, and aphid alarm pheromone, on wing dimorphism. These three stressors induced high proportion of up to 60% of winged morphs in offspring. Transcriptome analysis of stress-treated female aphids revealed different changes in maternal gene expression induced by the three stressors. Crowding elicited widespread changes in the expression of genes involved in nutrient accumulation and energy mobilization. Distinct from crowding, predation caused dramatic expression changes in cuticle protein (CP) genes. Twenty-three CP genes that belong to CP RR2 subfamily and are highly expressed in legs and embryos were greatly repressed by the presence of ladybird. By contrast, application of alarm pheromone, E-β-farnesene, caused slight changes in gene expression. The three factors shared a responsive gene, cuticle protein 43. This study reveals the adaptive response of aphids to environmental stresses and provides a rich resource on genome-wide expression genes for exploring molecular mechanisms of ecological adaptation in aphids.Open research badgesThis article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.55b2b15.
| S-EPMC6822051 | biostudies-literature
Project description:Associations between microbes and animals are ubiquitous and hosts may benefit from harbouring microbial communities through improved resource exploitation or resistance to environmental stress. The pea aphid, Acyrthosiphon pisum, is the host of heritable bacterial symbionts, including the obligate endosymbiont Buchnera aphidicola and several facultative symbionts. While obligate symbionts supply aphids with key nutrients, facultative symbionts influence their hosts in many ways such as protection against natural enemies, heat tolerance, color change and reproduction alteration. The pea aphid also encompasses multiple plant-specialized biotypes, each adapted to one or a few legume species. Facultative symbiont communities differ strongly between biotypes, although bacterial involvement in plant specialization is uncertain. Here, we analyse the diversity of bacterial communities associated with nine biotypes of the pea aphid complex using amplicon pyrosequencing of 16S rRNA genes. Combined clustering and phylogenetic analyses of 16S sequences allowed identifying 21 bacterial OTUs (Operational Taxonomic Unit). More than 98% of the sequencing reads were assigned to known pea aphid symbionts. The presence of Wolbachia was confirmed in A. pisum while Erwinia and Pantoea, two gut associates, were detected in multiple samples. The diversity of bacterial communities harboured by pea aphid biotypes was very low, ranging from 3 to 11 OTUs across samples. Bacterial communities differed more between than within biotypes but this difference did not correlate with the genetic divergence between biotypes. Altogether, these results confirm that the aphid microbiota is dominated by a few heritable symbionts and that plant specialization is an important structuring factor of bacterial communities associated with the pea aphid complex. However, since we examined the microbiota of aphid samples kept a few generations in controlled conditions, it may be that bacterial diversity was underestimated due to the possible loss of environmental or transient taxa.
| S-EPMC4373712 | biostudies-literature
Project description:Knowledge of the relationship between the number of offspring produced (recruitment) and adult abundance is fundamental to forecasting the dynamics of an exploited population. Although small-scale experiments have documented the importance of maternal quality to offspring survival in plants and animals, the effects of this association on the recruitment dynamics of exploited populations are largely unknown. Here, we present results from both a simple population model and a meta-analysis of time-series data from 25 species of exploited marine fishes that suggest that a population of older, larger individuals has a higher maximum reproductive rate than an equivalent population of younger, smaller individuals, and that this difference increases with the reproductive lifespan of the population. These findings (i) establish an empirical link between population age structure and reproductive rate that is consistent with strong effects of maternal quality on population dynamics and (ii) provide further evidence that extended age structure is essential to the sustainability of many exploited fish stocks.
| S-EPMC2664375 | biostudies-literature
Project description:Aphids are economically important pest insects that damage plants by phloem feeding and the transmission of plant viruses. Their ability to feed exclusively on nutritionally poor phloem sap is dependent on the obligatory symbiotic bacterium Buchnera aphidicola, but additional facultative symbionts may also be present, a common example of which is Serratia symbiotica. Many Serratia species secrete extracellular enzymes, so we hypothesised that S. symbiotica may produce proteases that help aphids to feed on plants. Molecular analysis, including fluorescence in situ hybridization (FISH), revealed that S. symbiotica colonises the gut, salivary glands and mouthparts (including the stylet) of the pea aphid Acyrthosiphon pisum, providing a mechanism to transfer the symbiont into host plants. S. symbiotica was also detected in plant tissues wounded by the penetrating stylet and was transferred to naïve aphids feeding on plants containing this symbiont. The maintenance of S. symbiotica by repeated transmission via plants may explain the high frequency of this symbiont in aphid populations. Proteomic analysis of the supernatant from a related but cultivable S. symbiotica strain cultured in liquid medium revealed the presence of known and novel proteases including metalloproteases. The corresponding transcripts encoding these S. symbiotica enzymes were detected in A. pisum and in plants carrying the symbiont, although the mRNA was much more abundant in the aphids. Our data suggest that enzymes from S. symbiotica may facilitate the digestion of plant proteins, thereby helping to suppress plant defense, and that the symbionts are important mediators of aphid-plant interactions.
| S-EPMC6479166 | biostudies-literature