Evolution of chemosensory and detoxification gene families across herbivorous Drosophilidae

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Abstract

Herbivorous insects are exceptionally diverse, accounting for a quarter of all known eukaryotic species, but the genomic basis of adaptations that enabled this dietary transition remains poorly understood. Many studies have suggested that expansions and contractions of chemosensory and detoxification gene families—genes directly mediating interactions with plant chemical defenses—underlie successful plant colonization. However, this hypothesis has been challenging to test because the origins of herbivory in many insect lineages are ancient (>150 million years ago (mya)), obscuring genomic evolutionary patterns. Here, we characterized chemosensory and detoxification gene family evolution across Scaptomyza, a genus nested within Drosophila that includes a recently derived (<15 mya) herbivore lineage of mustard (Brassicales) specialists and carnation (Caryophyllaceae) specialists, and several nonherbivorous species. Comparative genomic analyses revealed that herbivorous Scaptomyza has among the smallest chemosensory and detoxification gene repertoires across 12 drosophilid species surveyed. Rates of gene turnover averaged across the herbivore clade were significantly higher than background rates in over half of the surveyed gene families. However, gene turnover was more limited along the ancestral herbivore branch, with only gustatory receptors and odorant-binding proteins experiencing strong losses. The genes most significantly impacted by gene loss, duplication, or changes in selective constraint were those involved in detecting compounds associated with feeding on living plants (bitter or electrophilic phytotoxins) or their ancestral diet (fermenting plant volatiles). These results provide insight into the molecular and evolutionary mechanisms of plant-feeding adaptations and highlight gene candidates that have also been linked to other dietary transitions in Drosophila.

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  1. history

    Just a small thought - may have been helpful to include this further up in results because i wondered this a few times, which distracted me a bit. Turns out, you have some super relevant analyses for it!

  2. We performed another set of CAFE analyses to compare rates between two clades of similar age: the clade of D. melanogaster and D. erecta (28 million years old) versus the clade of S. flava and S. graminum (23 million years old). This confirmed that the former pair showed no gene families evolving at higher rates

    This was a cool control comparison! Wondering if there's the opportunity for comparison of other insect clades that specialize but not in plants?

  3. gene copy-number evolutionary rates

    Not knowing much about this area.... does increase in gene copy number always mean increase in functional range (i.e. diversifying specificity against intended targets) or can it sometimes mean more types of regulation (i.e. differential expression across tissue types within the insect)?

  4. diversity of herbivorous insects emerged as a result of co-diversification processes with their host plants

    Curious if this is also true for hematophagous arthropods that moved from marine to land hosts?