Neuromodulatory receptors, such as serotonin receptors (5HTRs), change neuronal and synaptic properties, thereby altering behavioral outputs of neural circuits. In the sea slug Tritonia diomedea (Mollusca, Gastropoda, Nudibranchia), 5HT plays a role in activating rhythmic dorsal-ventral (DV) swimming by enhancing the strength of synapses made by the C2 neuron, which is part of the swim neural circuit. The identity of 5HTRs expressed by C2 homologues was previously unknown. Hermissenda crassicornis, another nudibranch, has C2 and serotonergic neuron homologues, but does not produce a DV swim. Furthermore, 5HT does not modulate Hermissenda C2 synaptic strength. In contrast, Pleurobranchaea californica, from the sister clade Pleurobranchomorpha swims with DV flexions in an analogous manner to Tritonia and 5HT enhances synaptic strength of the Pleurobranchaea C2 homolog. Phylogenetic analyses indicate that Tritonia and Pleurobranchaea evolved swimming independently. We hypothesized that 5HTR gene expression underlies species-typical behaviors. We predicted that 5HTR subtype expression would be similar in DV swimming species and different from non-DV swimming species. We used two approaches to examine 5HTR expression in C2 homologues: single-cell transcriptomics and single-cell quantitative PCR (qPCR). We found that receptor subtype 5HT7 was expressed only in C2 homologues of DV swimmers. Thus, differential expression of 5HTRs in C2 homologues correlates with swimming ability and modulation, while shared 5HT7 expression in DV swimmers indicates that swimming evolved independently using parallel gene expression. Identification of differentially expressed neuromodulator receptor genes in single neurons helps explain how species-typical behaviors evolved.