Cold seawater induces early sexual developmental stages in the BPG axis of European eel males

Abstract

Background The impossibility of closing the life cycle of the European eel ( Anguilla anguilla ) in captivity troubles the future of this critically endangered species. In addition, the European eel is a highly valued and demanded resource, thus the successful closing of its life cycle would have a substantial economic and ecological impact. With the aim of obtaining the highest gamete quality, the study of the effects of environmental factors, such as temperature, on reproductive performance may prove valuable. This is especially true for the exposure to cold water, which has been reported to improve sexual development in multiple other Actinopterygii species. Results European eel males treated with cold seawater (10 °C, T10) for 2 weeks showed an increase in the proliferation and differentiation of spermatogonial cells until the differentiated spermatogonial type A cell stage, and elevated testosterone and 11-ketotestosterone plasma levels. Transcriptomes from the tissues of the brain-pituitary-gonad (BPG) axis of T10 samples revealed a differential gene expression profile compared to the other experimental groups, with clustering in a principal component analysis and in heat maps of all differentially expressed genes. Furthermore, a functional analysis of differentially expressed genes revealed enriched gene ontology terms involved in the regulation of circadian rhythm, histone modification, meiotic nuclear division, and others. Conclusions Cold seawater treatment had a clear effect on the activity of the BPG-axis of European eel males. In particular, our cold seawater treatment induces the synchronization and increased proliferation and differentiation of specific spermatogonial cells. In the transcriptomic results, genes related to thermoception were observed. This thermoception may have caused the observed effects through epigenetic mechanisms, since all analysed tissues further revealed differentially expressed genes involved in histone modification. The presented results support our hypothesis that a low temperature seawater treatment induces an early sexual developmental stage in European eels. This hypothesis is logical given that the average temperature experienced by eels in the early stages of their oceanic reproductive migration is highly similar to that of this cold seawater treatment. Further studies are needed to test whether a cold seawater treatment can improve the response of European eels to artificial hormonal treatment, as the results suggest. Electronic supplementary material The online version of this article (10.1186/s12864-019-5969-6) contains supplementary material, which is available to authorized users.

Unravelling the life‐history patterns and habitat preferences of the Japanese eel (Anguilla japonica) in the Pearl River, China

“…The seawater temperature in China, especially the surface water temperature of the South China Sea, increased by about 1°C over the 40 years from 1980 to 2020, with an average rise of 0.25°C each decade (National Marine Data and Information Service, 2021). Cold sea water is essential to induce early sexual development in catadromous migratory eels, such as for the synchronization and increased proliferation and differentiation of specific spermatogonial cells (Rozenfeld et al ., 2019). Eels require cold sea water to promote the activity of the brain–pituitary–gonad (BPG) axis.…”

Identification and functional analysis of Tex11 and Meig1 in spermatogenesis of Hyriopsis cumingii

“…Proteins containing TPR domains are usually arranged in tandem 3–16 TPRs ( Allan and Ratajczak, 2011 ). TPR structures are important in transcriptional regulation, protein kinase inhibition, peroxisomal protein and mitochondrial transport, cell cycle, immunity and viral replication, protein folding ( Zhang et al, 2004 ; Liu et al, 2012 ; Rozenfeld et al, 2019 ). Hsd-3.8, Klc3, Pp2ac and Ttc21a genes possessing TPR domains were shown to be involved in mammalian spermatogenesis ( Lin et al, 2002 ; Zhang et al, 2012 ; Pan et al, 2015 ; Liu W. J. et al, 2019 ).…”

“…Tex11 genes have been studied more in mammals and less in aquatic animals. Tex11 is an interesting factor in the late developmental stages of male Anguilla ( Rozenfeld et al, 2019 ) . Meiosis expressed gene 1 ( Meig1 ) is a critical gene for the control of spermiogenesis and manchette structure.…”

Epigenetic Responses to Temperature and Climate

“…One study found that exposing European eel males (Anguilla anguilla) to a constant cold temperature during development resulted in increased differentially expressed genes within the brainpituitary-gonad (BPG) axis (Rozenfeld et al 2019). Genes involved in reproduction were differentially expressed in the gonads, while histone H3-K9 methylation and histone H3 deacetylation genes were upregulated in brain and pituitary tissues (Rozenfeld et al 2019). This differential activity in the BPG-axis was correlated with the early induction of sexual development, as indicated with increased spermatogonial cell counts within the testes.…”