Differential impacts of carp and salmon pituitary extracts on induced oogenesis, egg quality, molecular ontogeny and embryonic developmental competence in European eel

Abstract

Low egg quality and embryonic survival are critical challenges in aquaculture, where assisted reproduction procedures and other factors may impact egg quality. This includes European eel (Anguilla anguilla), where pituitary extract from carp (CPE) or salmon (SPE) is applied to override a dopaminergic inhibition of the neuroendocrine system, preventing gonadotropin secretion and gonadal development. The present study used either CPE or SPE to induce vitellogenesis in female European eel and compared impacts on egg quality and offspring developmental competence with emphasis on the maternal-to-zygotic transition (MZT). Females treated with SPE produced significantly higher proportions of floating eggs with fewer cleavage abnormalities and higher embryonic survival. These findings related successful embryogenesis to higher abundance of mRNA transcripts of genes involved in cell adhesion, activation of MZT, and immune response (dcbld1, epcam, oct4, igm) throughout embryonic development. The abundance of mRNA transcripts of cldnd, foxr1, cea, ccna1, ccnb1, ccnb2, zar1, oct4, and npm2 was relatively stable during the first eight hours, followed by a drop during MZT and low levels thereafter, indicating transfer and subsequent clearance of maternal mRNA. mRNA abundance of zar1, epcam, and dicer1 was associated with cleavage abnormalities, while mRNA abundance of zar1, sox2, foxr1, cldnd, phb2, neurod4, and neurog1 (before MZT) was associated with subsequent embryonic survival. In a second pattern, low initial mRNA abundance with an increase during MZT and higher levels persisting thereafter indicating the activation of zygotic transcription. mRNA abundance of ccna1, npm2, oct4, neurod4, and neurog1 during later embryonic development was associated with hatch success. A deviating pattern was observed for dcbld1, which mRNA levels followed the maternal-effect gene pattern but only for embryos from SPE treated females. Together, the differences in offspring production and performance reported in this study show that PE composition impacts egg quality and embryogenesis and in particular, the transition from initial maternal transcripts to zygotic transcription.

Using Osmotic Pumps to Induce the Production of Gametes in Male and Female European Eels

“…The female European eels need several weeks of standard hormonal treatment to reach the sexual maturation, between 16 to 25 weeks using SPE as hormonal treatment [37,38] and 12 to 25 weeks using CPE [11,39]. In the present study, sexual maturation was achieved between 13 to 17 weeks using CPE injections (the control group), which coincides with the aforementioned studies.…”

Type of hormonal treatment administered to induce vitellogenesis in European eel influences biochemical composition of eggs and yolk-sac larvae

“…On the one side, CPE females produced eggs containing a higher amount of total lipids and free amino acids, while on the other, SPE females produced eggs showing a higher percentage of buoyant eggs and fertilization rate. The latter indicates that other maternally derived components than nutrients, such as mRNAs and steroid hormones, present in the egg cytoplasm, might govern the essential processes during early embryogenesis, as also recently suggested for European eel (Kottmann et al 2020a;.…”

“…Females were randomly divided into two groups. After two weeks of acclimatization, one group received weekly injections of salmon pituitary extract (SPE, 18.75 mg kg −1 initial body weight, Argent Chemical Laboratories, Washington, USA), while the second group received weekly injections of carp pituitary extract (CPE, same dose, and same supplier) to induce vitellogenesis (Kottmann et al 2020a ). For completion of final maturation and ovulation, an additional injection of PE was given in combination with administration of 17α,20ß-dihydroxy-4-pregnen-3-one (DHP, Sigma-Aldrich, St. Louis, MO, USA) at 2.0 mg kg −1 present body weight, with stripping of eggs 12–14 h after injection (Palstra et al 2005 ; Kottmann et al 2021 ).…”

“…Female reproduction protocols involve repeated administration of pituitary extracts of carp (CPE) or salmon (SPE) to induce and sustain vitellogenesis, while administration of a maturation-inducing steroid is needed to complete oocyte maturation and ovulation (Palstra et al 2005 ; Da Silva et al 2018 ; Kottmann et al 2021 ). Recently, Kottmann et al ( 2020a ), studying the differential impact of CPE and SPE administration on egg quality and embryonic developmental competence, reported higher proportions of buoyant eggs and embryonic survival in offspring from SPE-treated females compared to CPE females. Thus, different content and composition of hormones in the pituitary glands and/or a species-specific affinity of eel receptors to carp and/or salmon hormones may influence egg quality (Schmitz et al 2005 ).…”

Sperm production and quality in European eel (Anguilla anguilla) in relation to hormonal treatment

“…However, these differences between stripping at 6 hr or 24 hr after treatment were not statistically significant. Other studies focussing on offspring production have applied an intermediate procedure, where males are stripped 12-hr post-hormonal treatment (Benini et al, 2018;Butts et al, 2014;Politis et al, 2014) in order to synchronize the timing of priming with female final maturation treatment (Kottmann et al, 2020;da Silva et al, 2018). The comparison of sperm quality of males stripped at 12 vs. 24 hr after hormonal induction in the present study did not show any differences between treatments in terms of milt weight or sperm density.…”