Abstract
Understanding how organisms adapt to environmental changes is a major question in evolution and ecology. In particular, the role of ancestral variation in rapid adaptation remains unclear because its trace on genetic variation, known as soft selective sweep, is often hardly recognizable from genome-wide selection scans. Here, we investigate the evolution of chemosensory genes in Drosophila yakuba mayottensis, a specialist subspecies on toxic noni (Morinda citrifolia) fruits on the island of Mayotte. We combine population genomics analyses and behavioral assays to evaluate the level of divergence in chemosensory genes and perception of noni chemicals between specialist and generalist subspecies of D. yakuba. We identify a signal of soft selective sweep on a handful of genes, with the most diverging ones involving a cluster of gustatory receptors expressed in bitter-sensing neurons. Our results highlight the potential role of ancestral genetic variation in promoting host plant specialization in herbivorous insects and identify a number of candidate genes underlying behavioral adaptation.
Highlights
Host plant specialization by herbivorous insects is a complex phenomenon requiring the simultaneous evolution of multiple adaptive phenotypes on the same genome
We have identified multiple regions, surprisingly, none contained any member of the four chemosensory gene families, despite a significant difference in olfactory preference between generalist and specialist populations
We found that only sites at Gr22b, Gr22d, Gr59a and Gr93b had a differentiation between D. y. mayottensis and D. y. yakuba from Cameroon ≥ 0.50, i.e., the differentiating alleles at those genes have increased in frequency only in D. y. mayottensis
Summary
Host plant specialization by herbivorous insects is a complex phenomenon requiring the simultaneous evolution of multiple adaptive phenotypes on the same genome. These phenotypes are classified under two broad categories: preference phenotypes inducing the choice of the particular host by the insect, and performance phenotypes improving the survival of the insect on the host [1]. Preference phenotypes could rely on visual, chemical, anatomical or phenological attributes of the host plant. The family Drosophilidae contains a wide spectrum of fly-plant associations going from generalist detritivorous species such as D. melanogaster to strict herbivorous such as species of the genus Scaptomyza [5]
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