What Goes Wrong during Early Development of Artificially Reproduced European Eel Anguilla anguilla? Clues from the Larval Transcriptome and Gene Expression Patterns

SIMPLE SUMMARY: Closing the life cycle of the European eel in captivity is urgently needed to gain perspective for the commercial production of juvenile glass eels. Larvae are produced weekly at our facilities, but large variations in larval mortality are observed during the first week after hatching. Although much effort has been devoted to investigating ways to prevent early larval mortality, it remains unclear what the causes are. The aim of this study was to perform a transcriptomic study on European eel larvae in order to identify genes and physiological pathways that are differentially regulated in the comparison of larvae from batches that did not survive for longer than three days vs. larvae from batches that survived for at least a week up to 22 days after hatching (non-viable vs. viable larvae). In contrast to earlier published studies on European eel, we conclude that larvae exhibit immune competency. Non-viable larvae initiated an inflammatory and host protection immune response and tried to maintain osmoregulatory homeostasis. As a perspective, microbial control and salinity reduction might benefit eel larvae in terms of lower mortality and improved development by lowering the costs of immune functioning and osmoregulation. ABSTRACT: In eels, large variations in larval mortality exist, which would impede the viable production of juvenile glass eels in captivity. The transcriptome of European eel larvae was investigated to identify physiological pathways and genes that show differential regulation between non-viable vs. viable larvae. Expression of genes involved in inflammation and host protection was higher, suggesting that non-viable larvae suffered from microbial infection. Expression of genes involved in osmoregulation was also higher, implying that non-viable larvae tried to maintain homeostasis by strong osmoregulatory adaptation. Expression of genes involved in myogenesis, neural, and sensory development was reduced in the non-viable larvae. Expression of the major histocompatibility complex class-I (mhc1) gene, M-protein (myom2), the dopamine 2B receptor (d2br), the melatonin receptor (mtr1), and heat-shock protein beta-1 (hspb1) showed strong differential regulation and was therefore studied in 1, 8, and 15 days post-hatch (dph) larvae by RT-PCR to comprehend the roles of these genes during ontogeny. Expression patterning of these genes indicated the start of active swimming (8 dph) and feed searching behavior (15 dph) and confirmed immunocompetence immediately after hatching. This study revealed useful insights for improving larval survival by microbial control and salinity reduction.