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Brisson, J. A.

Publications and source records attributed to Brisson, J. A..

7 recordsLinked to original sources

A chromatin accessibility map of pea aphid brain and embryo identifies tissue-specific regulatory elements

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.

genomics↗

The Stochastic Pacemaker: Cumulative Behavioral Noise Drives Morphological Plasticity in Pea Aphids

Phenotypic variation within a single genotype under the same environment (intragenetic variation), the biologically meaningful part of Verror, 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 individuals 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 Verror is a dynamic product of behavioral history, suggesting a fundamental role for individual-level niche construction in generating macro-phenotypic diversity.

evolutionary biology↗

Long-term effects of the early life environment on alternative splicing

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 that 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.

developmental biology↗

New gene annotations for three pea aphid genome assemblies allow comparative analyses of genes and gene family evolution

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.

genomics↗

Analysis of duplication and possible sub-functionalization of wing gene network components in pea aphids

A fundamental focus of evolutionary-developmental biology is uncovering the genetic mechanisms responsible for the gain and loss of characters. One approach to this question is to investigate changes in the coordinated expression of a group of genes important for the development of a character of interest (a gene regulatory network). Here we consider the possibility that modifications to the wing gene regulatory network (wGRN), as defined by work primarily done in Drosophila melanogaster, were involved in the evolution of wing dimorphisms of the pea aphid (Acyrthosiphon pisum). We hypothesize that this may have occurred via changes in expression levels or duplication followed by sub-functionalization of wGRN components. To test this, we annotated members of the wGRN in the pea aphid genome and assessed their expression levels in first and third nymphal instars of winged and wingless morphs of males and asexual females. We find that only two of the 32 assessed genes exhibit morph-biased expression. We also find that three wing genes (apterous (ap), warts (wts), and decapentaplegic (dpp)) have undergone gene duplication. In each case, the resulting paralogs show signs of functional divergence, exhibiting either sex-, morph-, or stage-specific expression. Two gene duplicates, wts2 and dpp3, are of particular interest with respect to wing dimorphism, as they exhibit a wingless male-specific isoform and wingless male-biased expression, respectively. These results supplement our understanding of trends in developmental gene network evolution, such as side-stepping pleiotropic constraint via duplication and sub-functionalization, underlying the emergence of novel phenotypes.

evolutionary biology↗

Intraspecific variation in symbiont density in an insect-microbe symbiosis

AO_SCPLOWBSTRACTC_SCPLOWMany insects host vertically-transmitted microbes, which can confer benefits to their hosts but are costly to maintain and regulate. A key feature of these symbioses is variation: for example, symbiont density can vary among host and symbiont genotypes. However, the evolutionary forces maintaining this variation remain unclear. We studied variation in symbiont density using the pea aphid (Acyrthosiphon pisum) and the bacterium Regiella insecticola, a symbiont that can protect its host against fungal pathogens. We found that relative symbiont density varies both between two Regiella phylogenetic clades and among aphid biotypes. Higher-density symbiont infections are correlated with stronger survival costs, but variation in density has little effect on the protection Regiella provides against fungus. Instead, we found that in some aphid genotypes, a dramatic decline in symbiont density precedes the loss of a symbiont infection. Together, our data suggest that the optimal density of a symbiont infection is likely different from the perspective of aphid and microbial fitness. Regiella might prevent loss by maintaining high within-host densities, but hosts do not appear to benefit from higher symbiont numbers and may be advantaged by losing costly symbionts in certain environments. The standing variation in symbiont density observed in natural populations could therefore be maintained by antagonistic coevolutionary interactions between hosts and their symbiotic microbes.

evolutionary biology↗

Unravelling the genomic basis and evolution of the pea aphid male wing dimorphism

Wing dimorphisms have long served as models for examining the ecological and evolutionary tradeoffs associated with alternative morphologies [1], yet the mechanistic basis of morph determination remains largely unknown. Here we investigate the genetic basis of the pea aphid (Acyrthosiphon pisum) wing dimorphism, wherein males exhibit one of two alternative morphologies that differ dramatically in a set of correlated traits that inclused the presence or absence of wings [2-4]. Unlike the environmentally-induced asexual female aphid wing polyphenism [5], the male wing polymorphism is genetically determined by a single uncharacterized locus on the X chromosome called aphicarus (\"aphid\" plus \"Icarus\", api) [6, 7]. Using recombination and association mapping, we localized api to a 130kb region of the pea aphid genome. No nonsynonymous variation in coding sequences strongly associated with the winged and wingless phenotypes, indicating that api is likely a regulatory change. Gene expression level profiling revealed an aphid-specific gene from the region expressed at higher levels in winged male embryos, coinciding with the expected stage of api action. Comparison of the api region across biotypes (pea aphid populations specialized to different host plants that began diverging ~16,000 years ago [8, 9]) revealed that the two alleles were likely present prior to biotype diversification. Moreover, we find evidence for a recent selective sweep of a wingless allele since the biotypes diversified. In sum, this study provides insight into how adaptive, complex traits evolve within and across natural populations.

evolutionary biology↗