Male Differentiation in the Marine Copepod Oithona nana Reveals the Development of a New Nervous Ganglion and Lin12-Notch-Repeat Protein-Associated Proteolysis

SIMPLE SUMMARY: Copepods are tiny crustaceans and the most abundant animals on Earth; they also play a crucial role in the marine food chain. Among copepods, Oithona is one of most ecologically successful and is known for its differential behavior between males and females. The males adopt the strategy “live fast, die young”: they are constantly in motion to search for females, more vulnerable to predators, feed less, and have a higher mortality rate. In our study, we found the presence of a new male-specific ganglion in Oithona nana probably involved in female cues sensing. We also demonstrate the potential role of new Lin-12 Notch Repeat proteins in the development of this ganglion by interacting with proteins involved in the development of the nervous system. Thanks to our findings, we propose that the “live fast, die young” strategy of the O. nana males is optimized by the explosion of these Lin-12 Notch Repeat proteins in the male proteome involved in the development of the male-specific olfactory ganglion to increase female cue sensing and mating. ABSTRACT: Copepods are among the most numerous animals, and they play an essential role in the marine trophic web and biogeochemical cycles. The genus Oithona is described as having the highest density of copepods. The Oithona male paradox describes the activity states of males, which are obliged to alternate between immobile and mobile phases for ambush feeding and mate searching, respectively, while the female is less mobile and feeds less. To characterize the molecular basis of this sexual dimorphism, we combined immunofluorescence, genomics, transcriptomics, and protein–protein interaction approaches and revealed the presence of a male-specific nervous ganglion. Transcriptomic analysis showed male-specific enrichment for nervous system development-related transcripts. Twenty-seven Lin12-Notch Repeat domain-containing protein coding genes (LDPGs) of the 75 LDPGs identified in the genome were specifically expressed in males. Furthermore, some LDPGs coded for proteins with predicted proteolytic activity, and proteases-associated transcripts showed a male-specific enrichment. Using yeast double–hybrid assays, we constructed a protein–protein interaction network involving two LDPs with proteases, extracellular matrix proteins, and neurogenesis-related proteins. We also hypothesized possible roles of the LDPGs in the development of the lateral ganglia through helping in extracellular matrix lysis, neurites growth guidance, and synapses genesis.