UC Santa Barbara

We now know that co-option, or reuse of ancestral components, plays a prominent role in the evolution of emergent systems, like the reuse of gene regulatory networks in the evolution of developmental programs for morphology. Do the evolutionary origins of animal behaviors show evidence of modular reuse that we find at other levels of biological organization? I found that the skin of Octopus bimaculoides is intrinsically light sensitive, and that bright light causes colored chromatophore organs in octopus skin to expand, even without input from the central brain or eyes. Because this Light-Activated Chromatophore Expansion (or LACE) behavior relies on evolutionary novel chromatophore organs, LACE is also an evolutionary novelty. As such, I can pinpoint its origin in evolutionary time and ask whether the ability of mollusc skin to sense light existed prior to the evolution of cephalopod chromatophores and LACE. I found expression of the same r-opsin based phototransduction genes in both O. bimaculoides eyes and skin, and the spectral sensitivity of LACE closely matches that of the r-opsin in octopus eyes, consistent with the hypothesis that r-opsin phototransduction underlies LACE. The r-opsin phototransduction cascade can be traced back to at least the last common ancestor of bilaterians, so did the reuse of the cascade in octopus skin arise before, in time with, or after the evolution of cephalopod chromatophores? After surveying 28 mollusc mantle transcriptomes for opsins, I found that r-opsin cascade genes are expressed across the molluscs, from multiple species in each of the major mollusc classes, and an ancestral state reconstruction suggests that the last common ancestor of molluscs expressed r-opsin in its mantle. Taken together, these results suggest that the evolution of LACE required co-option of an ancient phototransduction module, and that like the evolution of development and other emergent systems, reuse may play a fundamental role in the macroevolution of animal behaviors.