Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet

Abstract

Herbivory is a key innovation in insects, yet has only evolved in onethird of living orders. The evolution of herbivory likely involves major behavioral changes mediated by remodeling of canonical chemosensory modules. Herbivorous flies in the genus Scaptomyza (Drosophilidae) are compelling species in which to study the genomic architecture linked to the transition to herbivory because they recently evolved from microbe-feeding ancestors and are closely related to Drosophila melanogaster. We found that Scaptomyza flava, a leaf-mining specialist on plants in the family (Brassicaceae), was not attracted to yeast volatiles in a four-field olfactometer assay, whereas D. melanogaster was strongly attracted to these volatiles. Yeast-associated volatiles, especially short-chain aliphatic esters, elicited strong antennal responses in D. melanogaster, but weak antennal responses in electroantennographic recordings from S. flava. We sequenced the genome of S. flava and characterized this species' odorant receptor repertoire. Orthologs of odorant receptors, which detect yeast volatiles in D. melanogaster and mediate critical host-choice behavior, were deleted or pseudogenized in the genome of S. flava. These genes were lost step-wise during the evolution of Scaptomyza. Additionally, Scaptomyza has experienced gene duplication and likely positive selection in paralogs of Or67b in D. melanogaster. Olfactory sensory neurons expressing Or67b are sensitive to green-leaf volatiles. Major trophic shifts in insects are associated with chemoreceptor gene loss as recently evolved ecologies shape sensory repertoires.plant-herbivore interactions | gene loss | olfaction | Drosophila melanogaster | Scaptomyza flava U nderstanding the origins and consequences of trophic shifts, especially the transition to herbivory, has been a central problem in evolutionary biology. The paleontological record suggests that evolutionary transitions to herbivory have been rare in insects (1), and the first transitions to herbivory in vertebrates occurred long after the colonization of land (2). However, species radiations result from herbivorous transitions in insects and vertebrates, suggesting that herbivory is a key innovation (3, 4). Identifying functional genomic changes associated with the evolutionary transition to herbivory could yield insight into the mechanisms that have driven their success. However, the origins of the most diverse clades of herbivorous insects are ancient and date to the Jurassic or earlier (5), limiting meaningful genomic comparisons. In contrast, herbivory has evolved more times in Diptera than in any other order (3). The Drosophilidae is an excellent system to study the evolution of herbivory from a functional genomic perspective because it includes several transitions to herbivory, and the genomic model Drosophila melanogaster (6, 7).The transition to herbivory involves adaptations in physiology (8-10), morphology (11), and behavior (12). The evolution of sensory repertoires could reinforce or even precipitate these adapt...

Recurrent specialization on a toxic fruit in an island Drosophila population

“…Second, our most extreme population genetic differentiation signals did not center on obvious attraction-related genes such as olfactory or gustatory receptors, which might be expected if selection acted on standing genetic variation present in the colonizing population (46,47). Indeed, none of the largest peaks contained any member of the chemosensory gene families whose rapid evolution and turnover are associated with ecological specialization in drosophilids and other insects (7,12,16,22,45). Because a minority of mainland flies visited noni in our experiment, it may be worth testing whether standing genetic variation exists for this trait ( Fig.…”

“…Hungate et al (19) hypothesized that olfactory attraction might have evolved first from recessive alleles segregating in the ancestral range, such as loss-of-function mutations at olfaction-related genes (7,12,15,45). Such attraction would yield strong selection for tolerance alleles, which may often be dominant (13,14) and may originate from new mutations or rare variants in the ancestral populations.…”

“…However, ecological differences in preference for the degree of ripeness/decay exist, with species using less decaying material evolving capabilities to resist plant defensive toxins, digest living plant material, and detect the appropriate host and ripening stage (9)(10)(11)(12). Such an "ecological gradient" makes drosophilids ideal for the study of the genetic basis of dietary shifts.…”

Nutrient acquisition across a dietary shift: fruit feeding butterflies crave amino acids, nectivores seek salt

“…Dietary shifts in animals have been associated with changes in chemosensory abilities, life history strategy, cognition, acquisition of microbial symbionts, and even the rate of evolutionary diversification (Gilbert 1972;Mitter et al 1988;Barton et al 1995;Douglas 1998;Price et al 2012;Goldman-Huertas et al 2015). Underlying all these shifts are changes in the relative availabilities of nutrients in the diet.…”

“…The amino acid solution may have tasted more similar to the fruit feeders' natural diet than to the diet of the nectar feeders, and frugivores may therefore have been more willing to accept the amino acid solution. Or, frugivores may have evolved an increased ability to detect amino acids; in the Drosophilidae, trophic shifts have been associated with evolution of the chemosensory system (Goldman-Huertas et al 2015).…”