Environment-Dependent Heterosis and Transgressive Gene Expression in Reciprocal Hybrids between the Channel Catfish <i>Ictalurus punctatus</i> and the Blue Catfish <i>Ictalurus furcatus</i>
The hybrid between female channel catfish (<i>Ictalurus punctatus</i>) and male blue catfish (<i>Ictalurus furcatus</i>) is superior in feed conversion, disease resistance, carcass yield, and harvestability compared to both parental species. However, heterosis and heterobelti...
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MDPI AG
2022-01-01
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| author | Haolong Wang Timothy J. Bruce Baofeng Su Shangjia Li Rex A. Dunham Xu Wang |
| author_facet | Haolong Wang Timothy J. Bruce Baofeng Su Shangjia Li Rex A. Dunham Xu Wang |
| author_sort | Haolong Wang |
| collection | DOAJ |
| description | The hybrid between female channel catfish (<i>Ictalurus punctatus</i>) and male blue catfish (<i>Ictalurus furcatus</i>) is superior in feed conversion, disease resistance, carcass yield, and harvestability compared to both parental species. However, heterosis and heterobeltiosis only occur in pond culture, and channel catfish grow much faster than the other genetic types in small culture units. This environment-dependent heterosis is intriguing, but the underlying genetic mechanisms are not well understood. In this study, phenotypic characterization and transcriptomic analyses were performed in the channel catfish, blue catfish, and their reciprocal F<sub>1</sub>s reared in tanks. The results showed that the channel catfish is superior in growth-related morphometrics, presumably due to significantly lower innate immune function, as investigated by reduced lysozyme activity and alternative complement activity. RNA-seq analysis revealed that genes involved in fatty acid metabolism/transport are significantly upregulated in channel catfish compared to blue catfish and hybrids, which also contributes to the growth phenotype. Interestingly, hybrids have a 40–80% elevation in blood glucose than the parental species, which can be explained by a phenomenon called transgressive expression (overexpression/underexpression in F<sub>1</sub>s than the parental species). A total of 1140 transgressive genes were identified in F<sub>1</sub> hybrids, indicating that 8.5% of the transcriptome displayed transgressive expression. Transgressive genes upregulated in F<sub>1</sub>s are enriched for glycan degradation function, directly related to the increase in blood glucose level. This study is the first to explore molecular mechanisms of environment-dependent heterosis/heterobeltiosis in a vertebrate species and sheds light on the regulation and evolution of heterosis vs. hybrid incompatibility. |
| first_indexed | 2024-03-10T01:52:36Z |
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| issn | 2079-7737 |
| language | English |
| last_indexed | 2024-03-10T01:52:36Z |
| publishDate | 2022-01-01 |
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| spelling | doaj.art-1006056c3b9a405090c0cf38150a652c2023-11-23T13:01:29ZengMDPI AGBiology2079-77372022-01-0111111710.3390/biology11010117Environment-Dependent Heterosis and Transgressive Gene Expression in Reciprocal Hybrids between the Channel Catfish <i>Ictalurus punctatus</i> and the Blue Catfish <i>Ictalurus furcatus</i>Haolong Wang0Timothy J. Bruce1Baofeng Su2Shangjia Li3Rex A. Dunham4Xu Wang5Department of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL 36849, USAAlabama Agricultural Experiment Station, Auburn, AL 36849, USAAlabama Agricultural Experiment Station, Auburn, AL 36849, USAAlabama Agricultural Experiment Station, Auburn, AL 36849, USAAlabama Agricultural Experiment Station, Auburn, AL 36849, USADepartment of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL 36849, USAThe hybrid between female channel catfish (<i>Ictalurus punctatus</i>) and male blue catfish (<i>Ictalurus furcatus</i>) is superior in feed conversion, disease resistance, carcass yield, and harvestability compared to both parental species. However, heterosis and heterobeltiosis only occur in pond culture, and channel catfish grow much faster than the other genetic types in small culture units. This environment-dependent heterosis is intriguing, but the underlying genetic mechanisms are not well understood. In this study, phenotypic characterization and transcriptomic analyses were performed in the channel catfish, blue catfish, and their reciprocal F<sub>1</sub>s reared in tanks. The results showed that the channel catfish is superior in growth-related morphometrics, presumably due to significantly lower innate immune function, as investigated by reduced lysozyme activity and alternative complement activity. RNA-seq analysis revealed that genes involved in fatty acid metabolism/transport are significantly upregulated in channel catfish compared to blue catfish and hybrids, which also contributes to the growth phenotype. Interestingly, hybrids have a 40–80% elevation in blood glucose than the parental species, which can be explained by a phenomenon called transgressive expression (overexpression/underexpression in F<sub>1</sub>s than the parental species). A total of 1140 transgressive genes were identified in F<sub>1</sub> hybrids, indicating that 8.5% of the transcriptome displayed transgressive expression. Transgressive genes upregulated in F<sub>1</sub>s are enriched for glycan degradation function, directly related to the increase in blood glucose level. This study is the first to explore molecular mechanisms of environment-dependent heterosis/heterobeltiosis in a vertebrate species and sheds light on the regulation and evolution of heterosis vs. hybrid incompatibility.https://www.mdpi.com/2079-7737/11/1/117heterosisheterobeltiosisenvironmentRNA-Seqtranscriptomicstransgressive genes |
| spellingShingle | Haolong Wang Timothy J. Bruce Baofeng Su Shangjia Li Rex A. Dunham Xu Wang Environment-Dependent Heterosis and Transgressive Gene Expression in Reciprocal Hybrids between the Channel Catfish <i>Ictalurus punctatus</i> and the Blue Catfish <i>Ictalurus furcatus</i> Biology heterosis heterobeltiosis environment RNA-Seq transcriptomics transgressive genes |
| title | Environment-Dependent Heterosis and Transgressive Gene Expression in Reciprocal Hybrids between the Channel Catfish <i>Ictalurus punctatus</i> and the Blue Catfish <i>Ictalurus furcatus</i> |
| title_full | Environment-Dependent Heterosis and Transgressive Gene Expression in Reciprocal Hybrids between the Channel Catfish <i>Ictalurus punctatus</i> and the Blue Catfish <i>Ictalurus furcatus</i> |
| title_fullStr | Environment-Dependent Heterosis and Transgressive Gene Expression in Reciprocal Hybrids between the Channel Catfish <i>Ictalurus punctatus</i> and the Blue Catfish <i>Ictalurus furcatus</i> |
| title_full_unstemmed | Environment-Dependent Heterosis and Transgressive Gene Expression in Reciprocal Hybrids between the Channel Catfish <i>Ictalurus punctatus</i> and the Blue Catfish <i>Ictalurus furcatus</i> |
| title_short | Environment-Dependent Heterosis and Transgressive Gene Expression in Reciprocal Hybrids between the Channel Catfish <i>Ictalurus punctatus</i> and the Blue Catfish <i>Ictalurus furcatus</i> |
| title_sort | environment dependent heterosis and transgressive gene expression in reciprocal hybrids between the channel catfish i ictalurus punctatus i and the blue catfish i ictalurus furcatus i |
| topic | heterosis heterobeltiosis environment RNA-Seq transcriptomics transgressive genes |
| url | https://www.mdpi.com/2079-7737/11/1/117 |
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