Evolution of chemosensory and detoxification gene families across herbivorous Drosophilidae

Herbivorous insects are exceptionally diverse, accounting for a quarter of
all known eukaryotic species, but the genetic 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 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 non-herbivorous
species. Comparative genomic analyses revealed that herbivorous Scaptomyza
have 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 plants (bitter or electrophilic phytotoxins) or their
ancestral diet (yeast and fruit volatiles). These results provide insight
into the molecular and evolutionary mechanisms of plant-feeding
adaptations and highlight strong gene candidates that have also been
linked to other dietary transitions in Drosophila.