Origin of a complex key innovation in an obligate insect–plant mutualism

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Abstract
Evolutionary key innovations give organisms access to new ecological resources and cause rapid, sometimes spectacular adaptive radiation. The well known obligate pollination mutualism between yuccas and yucca moths is a major model system for studies of coevolution, and it relies on the key innovation in the moths of complex tentacles used for pollen collecting and active pollination. These structures lack apparent homology in other insects, making them a rare example of a novel limb. We performed anatomical and behavioral studies to determine their origin and found evidence of a remarkably simple mechanism. Morphological analyses of the tentacles and adjacent mouthparts in pollinators and closely related taxa showed that the tentacle appears abruptly in female pollinating yucca moths. Several morphological synapomorphies between the galeae, which constitute the characteristic lepidopteran proboscis, and the tentacle suggest that the tentacle evolved quickly through expression of the genetic template for the galea at an apical growth bud on the first segment of the maxillary palp. Behavioral data indicate that tentacle and proboscis movements are controlled by a shared hydraulic extension mechanism, thus no new mechanism was needed for tentacle function. Known developmental paths from other insects can explain the origin of this sex-specific key innovation in a few steps.