Jennifer A. Brisson

Wing Dimorphism in Aphids

Many species of insects display dispersing and nondispersing morphs. Among these, aphids are one of the best examples of taxa that have evolved specialized morphs for dispersal versus reproduction. The dispersing morphs typically possess a full set of wings as well as a sensory and reproductive physiology that is adapted to flight and reproducing in a new location. In contrast, the nondispersing morphs are wingless and show adaptations to maximize fecundity. In this review, we provide an overview of the major features of the aphid wing dimorphism. We first provide a description of the dimorphism and an overview of its phylogenetic distribution. We then review what is known about the mechanisms underlying the dimorphism and end by discussing its evolutionary aspects.

Disrupting evolutionary processes: The effect of habitat fragmentation on collared lizards in the Missouri Ozarks

Humans affect biodiversity at the genetic, species, community, and ecosystem levels. This impact on genetic diversity is critical, because genetic diversity is the raw material of evolutionary change, including adaptation and speciation. Two forces affecting genetic variation are genetic drift (which decreases genetic variation within but increases genetic differentiation among local populations) and gene flow (which increases variation within but decreases differentiation among local populations). Humans activities often augment drift and diminish gene flow for many species, which reduces genetic variation in local populations and prevents the spread of adaptive complexes outside their population of origin, thereby disrupting adaptive processes both locally and globally within a species. These impacts are illustrated with collared lizards (Crotaphytus collaris) in the Missouri Ozarks. Forest fire suppression has reduced habitat and disrupted gene flow in this lizard, thereby altering the balance toward drift and away from gene flow. This balance can be restored by managed landscape burns. Some have argued that, although human-induced fragmentation disrupts adaptation, it will also ultimately produce new species through founder effects. However, population genetic theory and experiments predict that most fragmentation events caused by human activities will facilitate not speciation, but local extinction. Founder events have played an important role in the macroevolution of certain groups, but only when ecological opportunities are expanding rather than contracting. The general impact of human activities on genetic diversity disrupts or diminishes the capacity for adaptation, speciation, and macroevolutionary change. This impact will ultimately diminish biodiversity at all levels.

A functional DNA methylation system in the pea aphid, Acyrthosiphon pisum.

Methylation of cytosine is one of the main epigenetic mechanisms involved in controlling gene expression. Here we show that the pea aphid (Acyrthosiphon pisum) genome possesses homologues to all the DNA methyltransferases found in vertebrates, and that 0.69% (±0.25%) of all cytosines are methylated. Identified methylation sites are predominantly restricted to the coding sequence of genes at CpG sites. We identify twelve methylated genes, including genes that interact with juvenile hormone, a key endocrine signal in insects. Bioinformatic prediction using CpG ratios for all predicted genes suggest that a large proportion of genes are methylated within the pea aphid.

Aphid wing dimorphisms: linking environmental and genetic control of trait variation

Both genetic and environmental factors underlie phenotypic variation. While research at the interface of evolutionary and developmental biology has made excellent advances in understanding the contribution of genes to morphology, less well understood is the manner in which environmental cues are incorporated during development to influence the phenotype. Also virtually unexplored is how evolutionary transitions between environmental and genetic control of trait variation are achieved. Here, I review investigations into molecular mechanisms underlying phenotypic plasticity in the aphid wing dimorphism system. Among aphids, some species alternate between environmentally sensitive (polyphenic) and genetic (polymorphic) control of wing morph determination in their life cycle. Therefore, a traditional molecular genetic approach into understanding the genetically controlled polymorphism may provide a unique avenue into not only understanding the molecular basis of polyphenic variation in this group, but also the opportunity to compare and contrast the mechanistic basis of environmental and genetic control of similar dimorphisms.

Functional conservation of DNA methylation in the pea aphid and the honeybee.

DNA methylation is a fundamental epigenetic mark known to have wide-ranging effects on gene regulation in a variety of animal taxa. Comparative genomic analyses can help elucidate the function of DNA methylation by identifying conserved features of methylated genes and other genomic regions. In this study, we used computational approaches to distinguish genes marked by heavy methylation from those marked by little or no methylation in the pea aphid, Acyrthosiphon pisum. We investigated if these two classes had distinct evolutionary histories and functional roles by conducting comparative analysis with the honeybee, Apis (Ap.) mellifera. We found that highly methylated orthologs in A. pisum and Ap. mellifera exhibited greater conservation of methylation status, suggesting that highly methylated genes in ancestral species may remain highly methylated over time. We also found that methylated genes tended to show different rates of evolution than unmethylated genes. In addition, genes targeted by methylation were enriched for particular biological processes that differed from those in relatively unmethylated genes. Finally, methylated genes were preferentially ubiquitously expressed among alternate phenotypes in both species, whereas genes lacking signatures of methylation were preferentially associated with condition-specific gene expression. Overall, our analyses support a conserved role for DNA methylation in insects with comparable methylation systems.

ABDOMINAL PIGMENTATION VARIATION IN DROSOPHILA POLYMORPHA: GEOGRAPHIC VARIATION IN THE TRAIT, AND UNDERLYING PHYLOGEOGRAPHY

Abstract Drosophila polymorpha is a widespread species that exhibits abdominal pigmentation variation throughout its range. To gain insight into this variation we combined phenotypic and genotypic data to test a series of nested hypotheses. First, we tested the null hypothesis that geographic variation in pigmentation is due to neutral factors. We used nested clade analysis to examine the distribution of haplotypes from a nuclear and a mitochrondrial locus. Restricted gene flow via isolation by distance, the primary inference of this phylogeographic analysis, was then used to generate and test the hypothesis of increasing average abdominal pigmentation difference with increasing geographic distance. We found no correlation between geographic distance and phenotypic distance. We then tested the hypothesis that pigmentation is affected by environmental differences among localities. We found a significant effect of habitat type on the average abdominal pigmentation phenotype of different localities. Finally, we tested the hypothesis that pigmentation in D. polymorpha is associated with desiccation resistance. We found that dark individuals of both sexes survived significantly longer in a desiccating environment than light individuals. These patterns combined lead us to hypothesize that abdominal pigmentation variation in D. polymorpha is important in mediating the organisms interactions with local ecological factors.

Comprehensive survey of developmental genes in the pea aphid, Acyrthosiphon pisum: frequent lineage‐specific duplications and losses of developmental genes

Aphids exhibit unique attributes, such as polyphenisms and specialized cells to house endosymbionts, that make them an interesting system for studies at the interface of ecology, evolution and development. Here we present a comprehensive characterization of the developmental genes in the pea aphid, Acyrthosiphon pisum, and compare our results to other sequenced insects. We investigated genes involved in fundamental developmental processes such as establishment of the body plan and organogenesis, focusing on transcription factors and components of signalling pathways. We found that most developmental genes were well conserved in the pea aphid, although many lineage‐specific gene duplications and gene losses have occurred in several gene families. In particular, genetic components of transforming growth factor beta (TGFβ) Wnt, JAK/STAT (Janus kinase/signal transducer and activator of transcription) and EGF (Epidermal Growth Factor) pathways appear to have been significantly modified in the pea aphid.

Common genome‐wide patterns of transcript accumulation underlying the wing polyphenism and polymorphism in the pea aphid (Acyrthosiphon pisum)

SUMMARY The pea aphid, Acyrthosiphon pisum, exhibits several environmentally cued polyphenisms, in which discrete, alternative phenotypes are produced. At low‐density, parthenogenetic females produce unwinged female progeny, but at high‐density females produce progeny that develop with wings. These alternative phenotypes represent a solution to the competing demands of dispersal and reproduction. Males also develop as either winged or unwinged, but these alternatives are determined by a genetic polymorphism. Winged and unwinged males are morphologically less distinct from each other than winged and unwinged females, possibly because males experience fewer trade‐offs between dispersal and reproduction. To assess whether shared physiological differences mirror the shared morphological differences that characterize the wing polyphenism and polymorphism, we used a cDNA microarray representing an estimated 10% of the coding genome (1734 genes) to examine differential transcript accumulation between winged and unwinged females and males. We identified several transcripts that differentially accumulate between winged and unwinged morphs in both sexes, the majority of which are involved in energy production. Unexpectedly, the extent of differential transcript accumulation between winged and unwinged morphs was greater for adult males than for adult females. Together, these results suggest not only that similar physiological differences underlie the polyphenism and polymorphism, but that male morphs, like females, are subject to trade‐offs between reproduction and dispersal that are reflected in levels of transcript accumulation and possibly genome‐wide patterns of gene regulation. These data also provide a baseline for future studies of the molecular and physiological basis of life‐history trade‐offs.

Wing development genes of the pea aphid and differential gene expression between winged and unwinged morphs.

Little is known about when, how or even if the wing development gene network elucidated in Drosophila is deployed in direct‐developing insects. Here we identify the wing development genes (as determined in Drosophila) of the pea aphid (Acyrthosiphon pisum), which produces winged or unwinged adults in response to environmental cues. We find that the principal wing development genes studied in Drosophila are present in the aphid genome and that apterous and decapentaplegic exhibit duplications. We followed expression levels of 11 of these developmental genes at embryogenesis and across the nymphal instars. Six showed significant stage‐specific expression level effects and apterous1 exhibited significantly different expression levels between winged and unwinged morphs, suggesting this gene acts proximately to realize polyphenic development.

Juvenile hormone titre and related gene expression during the change of reproductive modes in the pea aphid

Most aphids show reproductive polyphenism, i.e. they alternate their reproductive modes from parthenogenesis to sexual reproduction in response to short photoperiods. Although juvenile hormone (JH) has been considered a likely candidate for regulating the transition from asexual to sexual reproduction after photoperiod sensing, there are few studies investigating the direct relationship between JH titres and the reproductive‐mode change. In addition, the sequencing of the pea aphid genome has allowed identification of the genes involved in the JH pathway, which in turn allows us to examine their expression levels in relation to the reproductive‐mode change. Using liquid chromatography‐mass spectrometry in the pea aphid, JHIII titre was shown to be lower in aphids producing sexual morphs under short‐day conditions than in aphids producing parthenogenetic morphs under long‐day conditions. The expression levels of genes upstream and downstream of JH action were quantified by real‐time quantitative reverse‐transcription‐PCR across the reproductive‐mode change. The expression level of JH esterase, which is responsible for JH degradation, was significantly higher in aphids reared under short‐day conditions. This suggests that the upregulation of the JH degradation pathway may be responsible for the lower JHIII titre in aphids exposed to short‐days, leading to the production of sexual morphs.