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Summary Animals must flexibly respond to environmental stimuli to survive, and optimal responses critically depend on the organism’s current needs. Many organisms have evolved both cell-intrinsic and intertissue signaling pathways that integrate metabolic status. However, how this information is encoded in molecular signals is currently not well understood. Here we show that the nematodeC. elegansemploys lipidated neurohormones that combine the neurotransmitter octopamine and fat metabolism-derived building blocks to relay information about lipid metabolic status and drive inhibition of aversive olfactory responses during food removal. Using targeted metabolomics, we show that lipidated neurohormone synthesis requires the carboxylesterase CEST-2.1, which links octopamine-glucosides with endogenous methyl-branched or diet-derived cyclopropane fatty acids that act as agonists of the nuclear receptor and master regulator of fat metabolism, NHR-49/PPARα. Loss ofcest-2.1,loss of bacterial cyclopropane fatty acid production, or loss of endogenous biosynthesis of the methyl-branched fatty acid substrates of CEST-2.1 mimics the behavioral responses of animals lacking octopamine, indicating that regulation of neurotransmitter-dependent behavior is linked to the coordination of fat metabolism via NHR-49/PPARα. Biosynthesis and subsequent neuromodulation via lipidated neurohormone relies on an intertissue trafficking pathway in which octopamine is shuttled first into the intestine where it is chemically modified, which is likely followed by neuronal import and intracellular hydrolysis to finally release free octopamine. We propose that esterase-dependent synthesis and subsequent hydrolysis of lipidated neurohormones represents a chemical encoding mechanism by which animals integrate information from neurotransmitter signaling and lipid homeostasis to direct appropriate behaviors. 

Abstract AimHumans are unintentionally affecting the evolution of fishery species directly through exploitation and indirectly by altering climate. We aim to test for a relationship between biogeographic patterns in the shell phenotypes of an over‐exploited shellfish and the presence of humans to identify human‐mediated adaptive trade‐offs. The implications of these trade‐offs are discussed with respect to the sustainability of the fishery. TaxonThe endemic Hawaiian intertidal limpet, ‘opihi makaiauli (Patellagastropoda, Nacellidae, Cellana exarata) MethodsWe surveyed phenotypic characters associated with temperature and predation avoidance across the entire species range and tested for differences in the relationship between these characters and latitude, on islands with and without humans. ResultsAmong all limpets surveyed, there was a bimodal distribution in shell colour (light, dark) and a parapatric pattern of shell coloration across the archipelago with lighter shells being prevalent on the uninhabited islands and darker, more camouflaged shells being prevalent on the inhabited islands. On the cooler, uninhabited islands, all morphometric characters associated with thermal avoidance (surface area, height and doming) increased with decreasing latitude. On the hotter, inhabited islands, however, shells were flatter, less variable and less adapted for avoiding thermal stress than predation. Main ConclusionsThe biogeographic patterns in shell phenotype and previous genetic studies suggest that the population is beginning to bifurcate in response to disruptive and directional selection as well as geographic isolation between the islands with and without humans. Decreased phenotypic and genetic diversity on the inhabited islands despite much larger populations of ‘opihi suggests a prominent historical bottleneck. The prevalence of maladaptive dark, flat phenotypes for thermal avoidance on the inhabited islands suggests that predation is a stronger selective force, driving adaptive trade‐offs in shape and colour. We propose that this is likely a case of fisheries‐induced evolution and a millennium of harvesting is the most likely selective pressure driving the observed biogeographic patterns in shell morphology. The flatter, darker shells will allow body temperatures to rise higher in direct sunlight, therefore we hypothesize that the thermal niche of ‘opihi is narrower on inhabited islands and will continue to narrow as Earth warms.