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Hedgehog signaling enables nutrition-responsive inhibition of an alternative morph in a polyphenic beetle

Significance Complex, nongradual responses to environmental conditions are commonplace in nature and perhaps most extreme in polyphenic insects where continuous variation in nutrition experienced in early development gives rise to discrete alternative castes or morphs. This research shows that the hedgehog (Hh) pathway has acquired a novel and highly unusual role in the nutrition-dependent regulation of polyphenic development of a beetle. Experimental repression of Hh signaling returns a highly discontinuous response to nutrition to its presumed ancestral, gradual state. Our results suggest that recruitment of the Hh signaling pathway may have been a key step in the evolution of trait thresholds and the corresponding origin of alternative phenotypes and complex allometries. The recruitment of modular developmental genetic components into new developmental contexts has been proposed as a central mechanism enabling the origin of novel traits and trait functions without necessitating the origin of novel pathways. Here, we investigate the function of the hedgehog (Hh) signaling pathway, a highly conserved pathway best understood for its role in patterning anterior/posterior (A/P) polarity of diverse traits, in the developmental evolution of beetle horns, an evolutionary novelty, and horn polyphenisms, a highly derived form of environment-responsive trait induction. We show that interactions among pathway members are conserved during development of Onthophagus horned beetles and have retained the ability to regulate A/P polarity in traditional appendages, such as legs. At the same time, the Hh signaling pathway has acquired a novel and highly unusual role in the nutrition-dependent regulation of horn polyphenisms by actively suppressing horn formation in low-nutrition males. Down-regulation of Hh signaling lifts this inhibition and returns a highly derived sigmoid horn body size allometry to its presumed ancestral, linear state. Our results suggest that recruitment of the Hh signaling pathway may have been a key step in the evolution of trait thresholds, such as those involved in horn polyphenisms and the corresponding origin of alternative phenotypes and complex allometries.