An Investigation of ZZ/ZW and XX/XY Sex Determination Systems in North African Catfish (Clarias gariepinus, Burchell, 1822)

Abstract

An investigation of sex-specific loci may provide important insights into fish sex determination strategies. This may be useful for biotechnological purposes, for example, to produce all-male or all-female fish for commercial breeding. The North African catfish species, Clarias gariepinus, has been widely adopted for aquaculture because its superior growth and disease resistance render the species suitable for hybridization with other catfish to improve the productivity and quality of fish meat. This species has either a ZZ/ZW or XX/XY sex determination system. Here, we investigate and characterize these systems using high-throughput genome complexity reduction sequencing as Diversity Arrays Technology. This approach was effective in identifying moderately sex-linked loci with both single-nucleotide polymorphisms (SNPs) and restriction fragment presence/absence (PA) markers in 30 perfectly sexed individuals of C. gariepinus. However, SNPs based markers were not found in this study. In total, 41 loci met the criteria for being moderately male-linked (with male vs. female ratios 80:20 and 70:30), while 25 loci were found to be moderately linked to female sex. No strictly male- or female-linked loci were detected. Seven moderately male-linked loci were partially homologous to some classes of transposable elements and three moderately male-linked loci were partially homologous to functional genes. Our data showed that the male heterogametic XX/XY sex determination system should co-exist with the ZZ/ZW system in C. gariepinus. Our finding of the co-existence of XX/XY and ZZ/ZW systems can be applied to benefit commercial breeding of this species in Thailand. This approach using moderately sex-linked loci provides a solid baseline for revealing sex determination mechanisms and identify potential sex determination regions in catfish, allowing further investigation of genetic improvements in breeding programs.

Genome-Wide SNP Analysis of Hybrid Clariid Fish Reflects the Existence of Polygenic Sex-Determination in the Lineage

“…ZZ/ZW and XX/XY are the common SDSs in the female and male heterogametic systems, and they have evolved repeatedly and independently in the lineage. This results in the presence of rapidly evolving SDSs in closely related species (Gammerdinger and Kocher, 2018;Nguyen et al, 2021a;Nguyen et al, 2021b). Thus, a study of sister taxa retaining divergent sex chromosome systems would be informative when examining SDS evolution.…”

“…Thus, a study of sister taxa retaining divergent sex chromosome systems would be informative when examining SDS evolution. Among the 115 species of clariid fish (Clariidae), some have either male heterogametic or female heterogametic sex determination systems (Pandey and Lakra, 1997;Nguyen et al, 2021a). Both heterogametic systems are present together, including multiple loci and sex chromosomes in the lineage.…”

“…Both heterogametic systems are present together, including multiple loci and sex chromosomes in the lineage. Varying SDSs have been observed in African catfish (Clarias gariepinus, Burchell, 1822) based on their geographical location: a ZZ/ZW system in Africa, a XX/XY system is indicated in some populations from Israel, Hungary, and China, or both systems in the same population in Thailand (Teugels et al, 1992;Eding et al, 1997;Eyo and Effiong, 2005;Nguyen et al, 2021a). The SDS of African catfish might be influenced by a multifactorial, polygenic sexdetermination (PSD) system that occurs in varied species.…”

“…Interspecific hybridization has successfully improved the growth rate, body size, disease resistance, and tolerance to stressors in aquaculture (Suprapto et al, 2017). For instance, male African catfish (C. gariepinus, 2n = 56) have been crossed with female bighead catfish (Clarias macrocephalus, Günther, 1864, 2n = 54 with XX/XY) to produce fast growth and improved disease resistance traits in the resulting hybrids (2n = 55) (Na-Nakorn, 1995;Chaivichoo et al, 2020;Nguyen et al, 2021a;Nguyen et al, 2021b). However, reproductive failure can occur as a result of chromosomal incompatibility with parental genomes.…”

“…In this study, we proposed the following two hypotheses: 1) the hybrid might possess the dominant SDS from male African catfish when Y or W sex chromosomes is present in different individuals, or 2) the hybrid might exhibit new candidate loci or a combination of different alleles due to the influence of PSD found in male African catfish. To determine how sex determination affects the viability of hybrid catfish, genome-wide single-nucleotide polymorphism (SNP) analyses were performed using Diversity Arrays Technology (DArTseq ™ ) of captive-bred individuals scored with phenotypic sex, as described by Nguyen et al (2021a) and Nguyen et al (2021b). Results will provide insights to improve the understanding of SDSs in clariid fish.…”