Shared neural transcriptomic patterns underlie the repeated evolution of mutualistic cleaning behaviour in Labridae wrasses

Abstract Despite the astonishing diversity of life, evolutionary biologists have documented numerous instances where species converge in how they behave, look and function. Given the importance of happenstance in evolution, it is often assumed that mechanisms driving independent evolution of similar phenotypes (convergence) are distinct; yet recent discoveries suggest that conserved genomic mechanisms can underlie convergent traits. Here, we generate forebrain transcriptomes from six sympatric Labridae wrasses that vary in mutualistic cleaning behaviour and apply differential gene expression, co-expression and phylogenetic comparative analyses to address three questions. First, do neurotranscriptomes vary among species with distinct cleaning behaviour? Second, do species that have independently evolved facultative cleaning share neurotranscriptomic patterns? Third, are transcriptomic signatures linked to facultative cleaning also expressed in obligate cleaners? We identify shared neurotranscriptomic patterns in the repeated evolution of facultative cleaning, including 25 novel candidate genes. We then find that transcriptomic patterns associated with facultative cleaning are shared in our focal obligate cleaner species, with more genes than expected by chance with concordant expression patterns in obligate and facultative cleaners. Our results illuminate the neuromolecular basis of cooperative behaviour and demonstrate the predictive potential of comparative transcriptomics to unravel mechanistic underpinnings of the repeated evolution of complex phenotypes.