Swimming suppresses hepatic vitellogenesis in European female silver eels as shown by expression of the estrogen receptor 1, vitellogenin1 and vitellogenin2 in the liver

Abstract

BackgroundWhen European silver eels (Anguilla anguilla) venture into the Atlantic Ocean for their 6,000 km semelparous spawning run to the Sargasso Sea, they are still in a prepubertal stage. Further sexual development appears to be blocked by dopaminergic inhibition of hypothalamus and pituitary activity. Recently, we found that swimming for several weeks in freshwater stimulated the incorporation of fat droplets in the oocytes. So, it was hypothesized that long term swimming in seawater would release the inhibition further and would also stimulate the production of vitellogenin by the liver.MethodsFor this study a swim-flume was constructed to allow simulated migration of migratory female silver eels for 3 months (1,420 km) in natural seawater at 20 degrees C. Primers were designed for polymerase chain reactions to measure the mRNA expression of estrogen receptor 1 (esr1), vitellogenin1 (vtg1) and vitellogenin2 (vtg2) genes in the liver of European female silver eels.ResultsIn comparison to resting eels, swimming eels showed a diminished expression of esr1, vtg1 and vtg2 in the liver. They also had lower plasma calcium (Ca; indicative of vitellogenin) levels in their blood. This showed that vitellogenesis is more strongly suppressed in swimming than in resting eels. However, when eels were subsequently stimulated by 3 weekly carp pituitary extract injections, the expression of the same genes and plasma levels of Ca strongly increased in both groups to similar levels, thus equalizing the initial differences between resting and swimming.ConclusionsIt is concluded that vitellogenesis remains suppressed during resting and even more during swimming. The fact that swimming stimulates fat deposition in the oocytes but suppresses vitellogenesis indicates that these events are separated in nature and occur sequentially. Swimming-suppressed vitellogenesis may imply that in nature eels undergo vitellogenesis and final maturation near or at the spawning grounds.

Saving energy to fuel exercise: swimming suppresses oocyte development and downregulates ovarian transcriptomic response of rainbow troutOncorhynchus mykiss

“…Additionally, during long-distance migrations there is a need to be able to suppress sexual maturation until a next clue signals to continue sexual maturation when being close to the spawning grounds. What we have shown in this study on rainbow trout, and in previous studies on European eels (45,48,50), is that the onset of ovarian vitellogenesis is a clear suppression point and an example of phenotypic plasticity during long distance, and often semelparous, reproductive migrations (Fig. 7).…”

“…Swimming trials in fresh water induced lipid deposition in the oocytes and oocyte growth, which are the first steps of sexual maturation (46,72). Experiments to investigate the effects on sexual maturation during the subsequent trajectory of swimming in sea water revealed suppressed gonadotropin expression (47) and vitellogenesis in females (48,49,50), while, in contrast, continued sexual maturation was observed in males (47). However, the genomic resources and necessary tools for European eel that would help unravel the mechanisms behind the effects of exercise on sexual maturation in migrant fish are not currently available for this species.…”

Deep RNA Sequencing of the Skeletal Muscle Transcriptome in Swimming Fish

“…In this study, we have mimicked the conditions experienced by trout during reproductive migration with the specific aim to provide insight into the relationship between migration and sexual maturation, two seemingly competing processes representing a state of muscle building versus a state of muscle wasting, respectively [4]–[6], [48]. In this regard, we hypothesize that sex steroids, and particularly androgens, may play a key role in exercise-enhanced muscle building.…”

Temporal progression in migratory status and sexual maturation in European silver eels during downstream migration

“…Silver eels have been reported to have a higher activity than yellow eels (van Ginneken et al 2005) as well as higher cortisol levels (van Ginneken et al 2007b). Cortisol may be responsible for lipid mobilisation to fuel swimming exercise but may also play a role in lifting the dopaminergic inhibition of sexual maturation in female eels (Dufour et al 2003; Palstra et al 2008, 2010c), perhaps by binding to glucocorticoid receptor—expressing neurons (Teitsma et al 1999). The shipment from Germany to The Netherlands of the eels in this study caused too much handling, which prevented to measure cortisol as trustable parameter.…”