Jennifer. A. Brisson

The pea aphid ( Acyrthosiphon pisum ) is an important model organism for studying complex biological traits, including wing polyphenism and host-symbiont interactions, yet its regulatory genomic landscape remains largely uncharacterized. Here we present the first genome-wide chromatin accessibility map of the pea aphid, generated using the assay for transposase-accessible chromatin followed by sequencing (ATAC-seq). We profiled open chromatin regions (OCRs) in adult brains and late-stage embryos from winged and wingless morphs maintained under solitary or crowded conditions. We also paired ATAC-seq with RNA-seq in embryonic samples to examine the relationship between chromatin accessibility and gene expression. Libraries showed a high abundance of reads from the aphid endosymbionts Spiroplasma and Buchnera , reflecting preferential Tn5 transposase insertion into nucleosome-free bacterial DNA. After computational removal of these reads, the remaining aphid-mapping libraries displayed hallmarks of high-quality ATAC-seq data. We identified a consensus set of 37,127 OCRs enriched at promoters and distal regulatory elements, with substantial overlap with computationally predicted enhancers and enrichment for transcription factor binding motifs. Tissue identity was the dominant driver of chromatin variation, accounting for 85% of variance along the first principal component, with 19,513 differentially accessible regions distinguishing brain from embryo samples. By contrast, differences associated with wing morph or crowding treatment were modest. Promoter accessibility was significantly and positively correlated with gene expression genome-wide. Together, these data constitute a foundational regulatory genomics resource for the pea aphid and establish a framework for mechanistic studies of gene regulation in this ecologically and economically important insect.

Phenotypic variation within a single genotype under the same environment (intragenetic variation), the biologically meaningful part of V _error , is frequently treated as a statistical nuisance rather than a biological reality, yet it represents an evolutionary driver of fitness that remains poorly integrated into evolutionary theory. The mechanism that translates such stochasticity into deterministic developmental phenotypic outcomes is not well understood. Here, we test a cumulative stochasticity model using wing polyphenism of the pea aphid ( Acyrthosiphon pisum ), where asexual mothers produce winged instead of wingless offspring in response to tactile cues. The model predicts that stochastic variation in maternal locomotor behavior alters the rate of tactile cue accumulation and thereby influences the probability of producing winged offspring. We demonstrate that maternal locomotor activity acts as a "stochastic pacemaker", where an individual’s movement determines the rate at which it actively constructs its environment and accumulates environmental cues. Our results reveal that genotypes differ significantly in both mobility and the temporal pattern of wing induction, with behavioral variation explaining approximately 20% of the total phenotypic variance across genotypes. Crucially, we show that maternal mobility increases progressively during crowding, accompanied by significant temporal heteroscedasticity. This expanding variance and increase in mean suggest that initial, trivial stochasticity is magnified into systematic behavioral divergence through the integration of environmental signals. By demonstrating that total accumulated locomotor activity predicts offspring phenotype, we provide a mechanistic bridge between transient behavioral noise and stable morphological shifts. More broadly, our work reveals that V _error is a dynamic product of behavioral history, suggesting a fundamental role for individual-level niche construction in generating macro-phenotypic diversity.

Stress experienced during embryogenesis can have long‐lasting effects. These effects may be particularly pronounced in hemimetabolous insects given that they do not undergo body reorganization prior to adulthood. Here, we examined the effects of maternal exposure to different temperatures (19, 22, 25, 28 and 31°C) in live‐bearing, asexual female pea aphids ( Acyrthosiphon pisum ). Specifically, we reared pea aphid mothers at these different temperatures, transferred their offspring to a common permissive temperature of 19°C and subsequently measured offspring developmental time, adult morphological traits, and fecundity. We found that pea aphids largely did not survive to adulthood at 31°C, so we were not able to examine their offspring. For the remaining temperatures, offspring whose mothers were raised at 19–25°C had largely similar trait values, while those whose mothers were raised at 28°C developed significantly more slowly, had smaller body parts and had lower fecundity. Our results demonstrate that in this hemimetabolous insect, the effects of embryonic exposure to temperature (either indirectly via the mother or directly from the environment) persist into adulthood.

Understanding how the embryonic environment affects adult phenotype is critical in the context of both human health and the increasing variance of environmental conditions due to climate change. Here we consider this topic within the framework of phenotypic integration, i.e., the pattern of correlations among elements of functionally robust trait suites. We investigated the life-long consequences of alternative embryonic environments on phenotypic integration in the pea aphid ( Acyrthosiphon pisum ). We exposed live-bearing pea aphid mothers to an adverse, high-density environment or a benign, low-density environment and measured morphological traits, fecundity, and transcriptional profiles in the resulting winged and wingless adult offspring. We observe that morphological integration decreases in both morphs in response to the adverse maternal environment. Transcriptional integration, on the other hand, shows a morph-specific response: integration increases in wingless offspring but decreases in winged offspring in response to the adverse maternal environment. Our results show the remarkable phenotypic diversity that a single genotype can express in response to environmental variation; that maternal environmental conditions can have strong effects on offspring trait variation and trait integration; and that these effects differ at the morphological and transcriptional levels.

All organisms respond to their environments, and early life environments may be especially impactful. Alternative splicing has been implicated as one mechanism that may underlie the response of organisms to their environments. However, most studies of this type examine immediate effects of an environmental perturbation on patterns of alternative splicing; little is known about the long-term consequences of early life environments. Here, we show the early life environment exerts a lasting influence on patterns of alternative splicing in the pea aphid ( Acyrthosiphon pisum ). This species is sensitive to conspecific density (crowding), with a transgenerational (mother-to-daughter) wing polyphenism cued by this environmental signal. We demonstrate that the maternal environment during embryonic development alters daughters’ alternative splicing profiles independently of morph identity, and that these effects persist into adulthood. By comparing the magnitude of maternal-environment effects to morph-specific differences, we reveal that the influence of early environmental conditions on splicing is unexpectedly large. These findings suggest that environmental history can leave a persistent molecular imprint beyond its role in morph determination. More broadly, this work highlights the need to disentangle environmental and morph-specific transcriptomic variation in studies of developmental polyphenism and connects to broader efforts, across biology and medicine, to understand how early life experiences shape long-term molecular and physiological outcomes.

Satellite DNAs (satDNAs), ubiquitous sequences in eukaryotic genomes, play a crucial role in genome organization, function, and evolution. The pea aphid Acyrthosiphon pisum is a major crop pest, and an emerging model for ecological, developmental, and evolutionary studies. This study characterizes the satellitome of the A. pisum to better understand its genomic organization and the evolutionary dynamics of satDNAs at the intraspecies level. The analysis of satDNAs across various host-plant adapted biotypes reveals a general sharing of the satellitome, with significative quantitative differences. We observe the amplification or contraction of specific satDNA families, even in the same biotype, consistent with the fast-evolutionary changes characteristic of these sequences. Rapid differential accumulation of repetitive elements among biotypes together with other factors may contribute to the origin of genetic incompatibilities. At the interspecific level, fluctuations in satDNA abundances, including the loss of certain families, are consistent with the library hypothesis, long-term conservation, and differential amplification of an ancestral satellitome. SatDNAs are considerably enriched in the heterochromatin of the chromosome X (Chr-X) and to a less extent, dispersed across the euchromatic region of all chromosomes. The enrichment of these sequences on Chr-X also features the elements that are most recently amplified and homogenized. This suggests that Chr-X could serve as a fountain of youth for satDNAs, contributing to the “fast-X” effect. Our findings provide valuable insights into genome structure, assembly, and the potential impact of satDNAs on species diversification, as well as the evolution of autosomes and Chr-X.

Reliable genome annotation is crucial for analyses of gene function, conservation, duplication, and evolution. Factors such as the sequencing technology used to create the assembly, as well as duplication and rearrangements within the genome of interest, can have a large impact on the quality of gene annotations. In particular, short-read-based assemblies tend to mis-assemble duplicated genes as single loci, a problem that requires additional long-read sequencing to resolve. Pea aphids exhibit a high level of gene duplication from frequent genomic rearrangements, which has led to the mis-assembly and mis-annotation of genes. Here, we re-annotate the pea aphid reference genome, along with two long-read pea aphid genomes, to facilitate future analyses of gene duplication and function in pea aphids. We use an integrated approach, consolidating both ab initio and RNA-Seq-based annotations into unified gene models. The new annotations contain genes that were missing, mis-annotated, or mis-assembled in the reference genome, and are generally consistent across assemblies, showing very good agreement between the long-read assemblies. Our annotation method is sensitive enough to refine existing gene models, uncovering alternatively used promoters and isoforms, and aids in finding gene duplications. These data provide a useful supplement to the existing reference annotations and a new comparative framework for discovery and analysis of gene function and duplication in this important emerging model insect.