Lumpfish, Cyclopterus lumpus L. 1758, is widely distributed across a large area on both sides of the North Atlantic Ocean. This species is a determinate batch spawner, with extended ovary development period (at least 8 months) and a relatively long spawning season (over a 4-month period, from March to July).
Lumpfish are increasingly used as a cleaner fish for removal of sea lice from Atlantic salmon, Salmo salar, as a greener and more sustainable alternative to chemical delousing. Interest in use of hatchery-reared lumpfish has therefore increased rapidly; hence, there is a need for year-round production of lumpfish juveniles. A requirement to achieve this objective is a deeper basic understanding of the Brain-Pituitary-Gonad (BPG) axis of the lumpfish. This endocrine cascade consists of a brain-to-pituitary communication through gonadotropin-releasing hormones (GnRHs) and their receptors, relayed by a pituitary-to-gonad signaling through two gonadotropins (LH and FSH) and their respective receptors. In turn, the gonads produce sexual steroid hormones, leading to the final maturation process.
We have now established the lumpfish genomic repertoire for the GnRHs, gonadotropins and their receptors, by performing in silico analyses on the recently released, non-annotated draft genome. The presence of multiple paralogues of our genes of interest was addressed by phylogenetic analyses and synteny verification. We have documented the presence of three GnRHs, four GnRH receptors, one LH- and one FSH-β subunit, and one FSH receptor.
To investigate dynamic changes in transcriptional activity of these BPG genes, we monitored initially immature lumpfish individuals for 10 months (end of September to beginning of August) in a facility in Bergen (Norway), under simulated natural light conditions. We have characterized the molecular, morphological histological and endocrine changes associated with the maturation process. Plasma was analyzed for 11-keto-testosterone (11-KT) and 2-estradiol (E2) of males and females, respectively.
In females, we observed a gradual increase in GSI peaking at the vernal equinox, correlating with a peak in LH-β mRNA in the pituitary and in E2, sharply decreasing thereafter. This LH-β/E2/GSI peak was preceded by a peak of GnRHRn2 expression in the pituitary in the end of February, with an increase detectable already from one month after the winter solstice. The GnRHRn2 peak correlated with a sharp increase in FSH-β mRNA in the pituitary. In males, the GSI increase was more subtle, but a sharp increase in 11-KT was detected around the vernal equinox, with a peak at the beginning of May, a bit later than in females, followed by a clear drop. In contrast to females, this peak was correlated with a peak in LH-β but also FSH-β and GnRHRn2 expression. The mRNA levels of LH-β and FSH-β increased at the end of February, while the increase in GnRHRn2 was more continuous.
These results indicate a different regulation in males and in females, and give insights into the temporal sequence of signaling that regulates maturation. Knowing the identity and temporal expression pattern of GnRHRn2 receptor is key on the way to establishing a protocol to try to artificially stimulate maturation in this species at a very upstream level. This research bears a great potential for improving the efficiency and sustainability of Atlantic salmon aquaculture, in addition to providing basic knowledge on lumpfish biology.