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Evidence of dramatic sterility in F1 male hybrid catfish [male Clarias gariepinus (Burchell, 1822) × female C. macrocephalus (Günther, 1864)] resulting from the failure of homologous chromosome pairing in meiosis I

Author:
Ponjarat, Jatupong, Singchat, Worapong, Monkheang, Pansa, Suntronpong, Aorarat, Tawichasri, Panupong, Sillapaprayoon, Siwapech, Ogawa, Satoshi, Muangmai, Narongrit, Baicharoen, Sudarath, Peyachoknagul, Surin, Parhar, Ishwar, Na-Nakorn, Uthairat, Srikulnath, Kornsorn
Source:
Aquaculture 2019 v.505 pp. 84-91
ISSN:
0044-8486
Subject:
Clarias gariepinus, Clarias macrocephalus, abnormal development, apoptosis, caspase-3, catfish, chromosome pairing, farmed fish, females, gametogenesis, genome, histology, hybrids, males, meiosis, pachytene stage, phenotype, pro-apoptotic proteins, spermatocytes, spermatozoa, testes
Abstract:
Sterile hybrid animals exhibit spermatogenic disruptions with a decreased number and/or malformation of mature sperm. F1 hybrid catfish (2n = 55) is an important cultured fish derived from male North African catfish [Clarias gariepinus (Burchell, 1822); 2n = 56] and female bighead catfish [C. macrocephalus (Günther, 1864); 2n = 54]; they are sterile with gametogenic failure in males. Despite the generality of this phenomenon, the spermatogenic phenotype has not been well described and a comprehensive understanding of the genetic basis of the disruption remains elusive. Our observations in the F1 male hybrid showed abnormal morphology of testes with small size, while meiotic configuration indicated that meiosis succeeded in the early pachytene stage but failed to progress beyond the diplotene-diakinesis stage in primary spermatocytes. This suggests the presence of a number of degenerated spermatocytes. Histological examination recorded no postmeiotic cells and spermatozoa in F1 male hybrid testes. A high frequency of apoptotic testicular cells was also present in the F1 male hybrid, as shown by histochemical results for activated Caspase-3 and TUNEL assays. Low expression levels of Caspase-3, p53 and MCL1 (isoform 2), which activate pro-apoptotic signals in the development process, were also observed in both parental species, but significantly high expression levels were observed in the F1 male hybrid. By contrast, the level of BCL2 expression was very low in the F1 male hybrid, supporting the state of apoptosis as BCL2 inhibits the actions of pro-apoptotic proteins. These results collectively suggest that sterility in male hybrids is caused by spermatogenic disruptions in the pachytene stage, resulting from the failure of homologous chromosome pairing due to chromosomal incompatibility between parental genomes, and subsequent elimination by apoptosis leading to spermatogenic breakdown in the F1 male hybrid.
Agid:
6335453