Cytochrome P450 diversification and hostplant utilization patterns in specialist and generalist moths: Birth, death and adaptation

Abstract

Across insect genomes, the size of the cytochrome P450 monooxygenase (CYP) gene superfamily varies widely. CYPome size variation has been attributed to reciprocal adaptive radiations in insect detoxification genes in response to plant biosynthetic gene radiations driven by co-evolution between herbivores and their chemically defended hostplants. Alternatively, variation in CYPome size may be due to random "birth-and-death" processes, whereby exponential increase via gene duplications is limited by random decay via gene death or transition via divergence. We examined CYPome diversification in the genomes of seven Lepidoptera species varying in host breadth from monophagous (Bombyx mori) to highly polyphagous (Amyelois transitella). CYPome size largely reflects the size of Clan 3, the clan associated with xenobiotic detoxification, and to some extent phylogenetic age. Consistently across genomes, families CYP6, CYP9 and CYP321 are most diverse and CYP6AB, CYP6AE, CYP6B, CYP9A and CYP9G are most diverse among subfamilies. Higher gene number in subfamilies is due to duplications occurring primarily after speciation and specialization ("P450 blooms"), and the genes are arranged in clusters, indicative of active duplicating loci. In the parsnip webworm, Depressaria pastinacella, gene expression levels in large subfamilies are high relative to smaller subfamilies. Functional and phylogenetic data suggest a correlation between highly dynamic loci (reflective of extensive gene duplication, functionalization and in some cases loss) and the ability of enzymes encoded by these genes to metabolize hostplant defences, consistent with an adaptive, nonrandom process driven by ecological interactions.

Evolution of herbivory remodels aDrosophilagenome

“…Genomic comparisons among anciently evolved herbivores and distantly related non-herbivores, or across herbivorous lineages, have uncovered striking expansions and losses of genes involved in chemosensation and detoxification in arthropods (e.g., (19,32,65,69,70) . Yet the lack of dense sampling among closely related taxa has, in many cases, precluded pinpointing the timing of these changes relative to the evolution of herbivory.…”

“…However, new studies suggest that this finding obscures potentially adaptive "blooms" that are more nuanced, localized phylogenetically and driven by the particular niches of the insects involved. Specifically, studies on insects with well-defined interactions with plants, including shifts from carnivory to folivory in bees and variation in diet breadth across Drosophila and Lepidoptera species, largely refute a purely stochastic birth-death hypothesis (19,58,(63)(64)(65) . We found a similar pattern of fewer CYP450 gene numbers in S. flava , likely due to a narrowing of their dietary niche, coupled with high turnover rates (high gain + loss rate) and a modest, but biologically significant bloom in the canonical xenobiotic resistance gene Cyp6g1 .…”

Substrate‐specificity of cytochrome P450‐mediated detoxification as an evolutionary strategy for specialization on furanocoumarin‐containing hostplants: CYP6AE89 in parsnip webworms

“…Webworm larvae express constitutively high levels of CYP6AE1 and CYP6AE89 transcripts irrespective of larval consumption of hostplant flowers or artificial diets amended with xanthotoxin or sphondin (Calla et al, 2017). For this study, gene expression levels of CYP6AE1 and CYP6AE89 were evaluated in midguts of caterpillars consuming the linear furanocoumarin xanthotoxin or the angular furanocoumarin sphondin.…”

“…A genome‐wide analysis of cytochrome P450s in the parsnip webworm identified, amongst others, transcripts of eight previously undescribed CYP6AE enzymes in the genome (CYP6AE89, CYP6AE90, CYP6AE91, CYP6AE92, CYP6AE93, CYP6AE95, CYP6AE96 and CYP6AE127) and confirmed the presence of CYP6AE1 reported earlier (Li et al ., ). Of these, CYP6AE1, CYP6AE89, CYP6AE91, CYP6AE93 and CYP6AE95 were found in the whole‐larva transcriptome, with two transcripts – CYP6AE1 and CYP6AE89 – expressed constitutively at very high levels (Calla et al ., ).…”

Role of cytochrome P450 2B sequence variation and gene copy number in facilitating dietary specialization in mammalian herbivores

“…Seminal work on insects revealed that a generalist insect has more detoxification enzymes with lower catalytic activity towards a wider variety of substrates than a specialist (Li, Baudry, Berenbaum, & Schuler, ; Li, Berenbaum, & Schuler, ; Li, Zangerl, Schuler, & Berenbaum, ). Moreover, the diversification of detoxification enzymes in relation to host plants appears adaptive and nonrandom (Calla et al., ). The regulation of cytochrome P450 genes is also consistent with host‐plant specialization in herbivorous Drosophila (Bono, Matzkin, Castrezana, & Markow, ).…”