Identifying genomic hotspots of differentiation and candidate genes involved in the adaptive divergence of pea aphid host races

Abstract

Identifying the genomic bases of adaptation to novel environments is a long-term objective in evolutionary biology. Because genetic differentiation is expected to increase between locally adapted populations at the genes targeted by selection, scanning the genome for elevated levels of differentiation is a first step towards deciphering the genomic architecture underlying adaptive divergence. The pea aphid Acyrthosiphon pisum is a model of choice to address this question, as it forms a large complex of plant-specialized races and cryptic species, resulting from recent adaptive radiation. Here, we characterized genomewide polymorphisms in three pea aphid races specialized on alfalfa, clover and pea crops, respectively, which we sequenced in pools (poolseq). Using a model-based approach that explicitly accounts for selection, we identified 392 genomic hotspots of differentiation spanning 47.3 Mb and 2,484 genes (respectively, 9.12% of the genome size and 8.10% of its genes). Most of these highly differentiated regions were located on the autosomes, and overall differentiation was weaker on the X chromosome. Within these hotspots, high levels of absolute divergence between races suggest that these regions experienced less gene flow than the rest of the genome, most likely by contributing to reproductive isolation. Moreover, population-specific analyses showed evidence of selection in every host race, depending on the hotspot considered. These hotspots were significantly enriched for candidate gene categories that control host-plant selection and use. These genes encode 48 salivary proteins, 14 gustatory receptors, 10 odorant receptors, five P450 cytochromes and one chemosensory protein, which represent promising candidates for the genetic basis of host-plant specialization and ecological isolation in the pea aphid complex. Altogether, our findings open new research directions towards functional studies, for validating the role of these genes on adaptive phenotypes.

Chromosome-scale genome assemblies of aphids reveal extensively rearranged autosomes and long-term conservation of the X chromosome

“…To assess how aphid chromosome architecture compares to that of Diptera and Lepidoptera, we studied chromosome rearrangements of three aphid species spanning approximately 30 million years of aphid evolution. To this end, we generated high-quality chromosome-scale genome assemblies of two extensively studied aphid species: the green peach aphid Myzus persicae, a model generalist aphid and major crop pest (Mathers et al 2017); and the pea aphid Acyrthosiphon pisum, a model for speciation genomics and basic aphid biology (Hawthorne and Via 2001;Brisson and Stern 2006;Peccoud et al 2009;Pecoud and Simon 2010;Nouhaud et al 2018). Then, we compared these aphid assemblies to a previously published chromosome-scale assembly of the corn-leaf aphid Rhopalosiphum maidis .…”

Transcriptome Profiling Revealed Potentially Critical Roles for Digestion and Defense-Related Genes in Insects’ Use of Resistant Host Plants: A Case Study with Sitobion Avenae

“…A study has found at least 17 aphid species with multiple biotypes evolved [11]. This is probably because differential levels of resistance in variable plants present a huge pressure of natural selection that favors host-associated ecological divergence of various aphid populations [12,13]. Increasing evidence has shown that the differential levels of plant resistance to aphids can be attributed to plant secondary chemistry.…”

Genomic evidence of genetic variation with pleiotropic effects on caterpillar fitness and plant traits in a model legume

“…Interactions between plants and herbivorous insects have received considerable scientific attention due to their ubiquity (Forister et al, ), agricultural relevance (Schoonhoven, Loon, & Dicke, ; Via, ), and hypothesized contribution to the extreme biodiversity of these taxonomic groups (via coevolutionary diversification; Braga, Guimaraes, Wheat, Soren, & Janz, ; Edger et al, ; Ehrlich & Raven, ; Fordyce, ; Mitter, Farrell, & Wiegmann, ). These interactions are often affected by genetic variation within species, including variation in plant resistance to insects, and for insect acceptance of, and performance on, potential host plants (e.g., Berenbaum & Zangerl, ; Dambroski et al, ; Gompert et al, ; Mitchell, Brennan, Graham, & Karley, ; Nouhaud et al, ; Ordas et al, ; Rausher & Simms, ; Schoonhoven et al, ; Spencer, ; Stowe, ; Via, ). Progress in explaining this variation has been made by identifying specific phytochemicals responsible for resistance to insects (e.g., furanocoumarins and glucosinolates), as well as the insect genes and pathways that detoxify these compounds (e.g., cytochrome P450 enzymes, nitrile specifier protein, etc.…”