Aphids: A Model for Polyphenism and Epigenetics

Environmental conditions can alter the form, function, and behavior of organisms over short and long timescales, and even over generations. Aphid females respond to specific environmental cues by transmitting signals that have the effect of altering the development of their offspring. These epigenetic phenomena have positioned aphids as a model for the study of phenotypic plasticity. The molecular basis for this epigenetic inheritance in aphids and how this type of inheritance system could have evolved are still unanswered questions. With the availability of the pea aphid genome sequence, new genomics technologies, and ongoing genomics projects in aphids, these questions can now be addressed. Here, we review epigenetic phenomena in aphids and recent progress toward elucidating the molecular basis of epigenetics in aphids. The discovery of a functional DNA methylation system, functional small RNA system, and expanded set of chromatin modifying genes provides a platform for analyzing these pathways in the context of aphid plasticity. With these tools and further research, aphids are an emerging model system for studying the molecular epigenetics of polyphenisms

Comparison of the wing polyphenic response of pea aphids (\u3ci\u3eAcyrthosiphon pisum\u3c/i\u3e) to crowding and predator cues

1. Pea aphids (Acyrthosiphon pisum Harris; Hemiptera: Aphididae) exhibit transgenerational wing polyphenism, in which unwinged females produce genetically identical winged offspring in response to environmental cues such as overcrowding and predation risk that indicate poor habitat quality. 2. Laboratory experiments were carried out to explore the intensity of the wing polyphenic response of pea aphids exposed to cues from ladybird predators and crowding, and their response was compared to pea aphids that were not exposed to any cues (control). 3. The study used cues from two different ladybird species: Coccinella septempunctata L. (Coleoptera: Coccinellidae) and Hippodamia convergens Guérin-Méneville (Coleoptera: Coccinellidae) to investigate whether the wing polyphenic response of pea aphids to predator cues can be generalized 4. The intensity of the wing polyphenic response of pea aphids to crowding was found to be much stronger than their response to predator cues. There was no response to H. convergens cues and the response to C. septempunctata cues was mixed

Similar patterns of linkage disequilibrium and nucleotide diversity in native and introduced populations of the pea aphid, Acyrthosiphon pisum

<p>Abstract</p> <p>Background</p> <p>The pea aphid, <it>Acyrthosiphon pisum</it>, is an emerging genomic model system for studies of polyphenisms, bacterial symbioses, host-plant specialization, and the vectoring of plant viruses. Here we provide estimates of nucleotide diversity and linkage disequilibrium (LD) in native (European) and introduced (United States) populations of the pea aphid. Because introductions can cause population bottlenecks, we hypothesized that U.S. populations harbor lower levels of nucleotide diversity and higher levels of LD than native populations.</p> <p>Results</p> <p>We sampled four non-coding loci from 24 unique aphid clones from the U. S. (12 from New York and 12 from California) and 24 clones from Europe (12 alfalfa and 12 clover specialists). For each locus, we sequenced approximately 1 kb from two amplicons spaced ~10 kb apart to estimate both short range and longer range LD. We sequenced over 250 kb in total. Nucleotide diversity averaged 0.6% across all loci and all populations. LD decayed slowly within ~1 kb but reached much lower levels over ~10 kb. Contrary to our expectations, neither LD nor nucleotide diversity were significantly different between native and introduced populations.</p> <p>Conclusion</p> <p>Both introduced and native populations of pea aphids exhibit low levels of nucleotide diversity and moderate levels of LD. The introduction of pea aphids to North America has not led to a detectable reduction of nucleotide diversity or increase in LD relative to native populations.</p

Diurnal and developmental differences in gene expression between adult dispersing and flightless morphs of the wing polymorphic cricket, \u3ci\u3eGryllus firmus\u3c/i\u3e: Implications for life-history evolution

The functional basis of life history adaptation is a key topic of research in life history evolution. Studies of wing polymorphism in the cricket Gryllus firmus have played a prominent role in this field. However, prior in-depth investigations of morph specialization have primarily focused on a single hormone, juvenile hormone, and a single aspect of intermediary metabolism, the fatty-acid biosynthetic component of lipid metabolism. Moreover, the role of diurnal variation in life history adaptation in G. firmus has been understudied, as is the case for organisms in general. Here, we identify genes whose expression differs consistently between the morphs independent of time-of-day during early adulthood, as well as genes that exhibit a strong pattern of morph-specific diurnal expression. We find strong, consistent, morph-specific differences in the expression of genes involved in endocrine regulation, carbohydrate and lipid metabolism, and immunity – in particular, in the expression of an insulin-like-peptide precursor gene and genes involved in triglyceride production. We also find that the flight-capable morph exhibited a substantially greater number of genes exhibiting diurnal change in gene expression compared with the flightless morph, correlated with the greater circadian change in the hemolymph juvenile titer in the dispersing morph. In fact, diurnal differences in expression within the dispersing morph at different times of the day were significantly greater in magnitude than differences between dispersing and flightless morphs at the same time-of-day. These results provide important baseline information regarding the potential role of variable gene expression on life history specialization in morphs of G. firmus, and the first information on genetically-variable, diurnal change in gene expression, associated with a key life history polymorphism. These results also suggest the existence of prominent morph-specific circadian differences in gene expression in G. firmus, possibly caused by the morph-specific circadian rhythm in the juvenile hormone titer. Nine supplemental files attached below

Widespread Selection Across Coding and Noncoding DNA in the Pea Aphid Genome

Genome-wide patterns of diversity and selection are critical measures for understanding how evolution has shaped the genome. Yet, these population genomic estimates are available for only a limited number of model organisms. Here we focus on the population genomics of the pea aphid (Acyrthosiphon pisum). The pea aphid is an emerging model system that exhibits a range of intriguing biological traits not present in classic model systems. We performed low-coverage genome resequencing of 21 clonal pea aphid lines collected from alfalfa host plants in North America to characterize genome-wide patterns of diversity and selection. We observed an excess of low-frequency polymorphisms throughout coding and noncoding DNA, which we suggest is the result of a founding event and subsequent population expansion in North America. Most gene regions showed lower levels of Tajima’s D than synonymous sites, suggesting that the majority of the genome is not evolving neutrally but rather exhibits significant constraint. Furthermore, we used the pea aphid’s unique manner of X-chromosome inheritance to assign genomic scaffolds to either autosomes or the X chromosome. Comparing autosomal vs. X-linked sequence variation, we discovered that autosomal genes show an excess of low frequency variants indicating that purifying selection acts more efficiently on the X chromosome. Overall, our results provide a critical first step in characterizing the genetic diversity and evolutionary pressures on an aphid genome

The Epigenetics of Emerging and Nonmodel Organisms

Genetic model organisms have gifted researchers with a breathtakingly detailed understanding of the most intimate aspects of their genomes, cells, and development. And yet there is a problem—model organisms have been selected because they have simple life histories and happily inhabit laboratories. In short, they make a virtue of being boring. But the diversity of the natural world is not fully captured by yeast, flies, or mice. To truly appreciate the variety of biological mechanisms underlying this remarkable diversity, one must study the often inconvenient but fascinating non model organism. Experimental and descriptive approaches in non model organisms have become more tractable with reduced genome-sequencing costs and the transferability of techniques and tools developed in model organisms, elevating some of them from non-model to emerging model organism status

Pea aphid winged and wingless males exhibit reproductive, gene expression, and lipid metabolism differences

Alternative, intraspecific phenotypes offer an opportunity to identify the mechanistic basis of differences asso- ciated with distinctive life history strategies. Wing dimorphic insects, in which both flight-capable and flight- incapable individuals occur in the same population, are particularly well-studied in terms of why and how the morphs trade offflight for reproduction. Yet despite a wealth of studies examining the differences between fe- male morphs, little is known about male differences, which could arise from different causes than those acting on females. Here we examined reproductive, gene expression, and biochemical differences between pea aphid ( Acyrthosiphon pisum ) winged and wingless males. We find that winged males are competitively superior in one- on-one mating circumstances, but wingless males reach reproductive maturity faster and have larger testes. We suggest that males tradeoffincreased local matings with concurrent possible inbreeding for outbreeding and in- creased ability to find mates. At the mechanistic level, differential gene expression between the morphs revealed a possible role for activin and insulin signaling in morph differences; it also highlighted genes not previously identified as being functionally important in wing polymorphism, such as genes likely involved in sperm produc- tion. Further, we find that winged males have higher lipid levels, consistent with their use as flight fuel, but we find no consistent patterns of different levels of activity among five enzymes associated with lipid biosynthesis. Overall, our analyses provide evidence that winged versus wingless males exhibit differences at the reproductive, gene expression, and biochemical levels, expanding the field’s understanding of the functional aspects of morph differences

Natural genetic variation in transcriptome reflects network structure inferred with major effect mutations: insulin/TOR and associated phenotypes in Drosophila melanogaster

<p>Abstract</p> <p>Background</p> <p>A molecular process based genotype-to-phenotype map will ultimately enable us to predict how genetic variation among individuals results in phenotypic alterations. Building such a map is, however, far from straightforward. It requires understanding how molecular variation re-shapes developmental and metabolic networks, and how the functional state of these networks modifies phenotypes in genotype specific way. We focus on the latter problem by describing genetic variation in transcript levels of genes in the InR/TOR pathway among 72 <it>Drosophila melanogaster </it>genotypes.</p> <p>Results</p> <p>We observe tight co-variance in transcript levels of genes not known to influence each other through direct transcriptional control. We summarize transcriptome variation with factor analyses, and observe strong co-variance of gene expression within the dFOXO-branch and within the TOR-branch of the pathway. Finally, we investigate whether major axes of transcriptome variation shape phenotypes expected to be influenced through the InR/TOR pathway. We find limited evidence that transcript levels of individual upstream genes in the InR/TOR pathway predict fly phenotypes in expected ways. However, there is no evidence that these effects are mediated through the major axes of downstream transcriptome variation.</p> <p>Conclusion</p> <p>In summary, our results question the assertion of the 'sparse' nature of genetic networks, while validating and extending candidate gene approaches in the analyses of complex traits.</p

Abiotic and Biotic Stressors Causing Equivalent Mortality Induce Highly Variable Transcriptional Responses in the Soybean Aphid

Environmental stress affects basic organismal functioning and can cause physiological, developmental, and reproductive impairment. However, in many nonmodel organisms, the core molecular stress response remains poorly characterized and the extent to which stress-induced transcriptional changes differ across qualitatively different stress types is largely unexplored. The current study examines the molecular stress response of the soybean aphid (Aphis glycines) using RNA sequencing and compares transcriptional responses to multiple stressors (heat, starvation, and plant defenses) at a standardized stress level (27% adult mortality). Stress-induced transcriptional changes showed remarkable variation, with starvation, heat, and plant defensive stress altering the expression of 3985, 510, and 12 genes, respectively. Molecular responses showed little overlap across all three stressors. However, a common transcriptional stress response was identified under heat and starvation, involved with up-regulation of glycogen biosynthesis and molecular chaperones and down-regulation of bacterial endosymbiont cellular and insect cuticular components. Stressor-specific responses indicated heat affected expression of heat shock proteins and cuticular components, whereas starvation altered a diverse set of genes involved in primary metabolism, oxidative reductive processes, nucleosome and histone assembly, and the regulation of DNA repair and replication. Exposure to host plant defenses elicited the weakest response, of which half of the genes were of unknown function. This study highlights the need for standardizing stress levels when comparing across stress types and provides a basis for understanding the role of general vs. stressor specific molecular responses in aphids