Does transcriptome of freshly hatched fish larvae describe past or predict future developmental trajectory?

Abstract

Background: The larval stage plays a crucial role in the ontogeny of many fish species, leading to profound changes in morphology, physiology and behavior. How larvae face metamorphoses can be associated with their quality, which can vary significantly among the same family or even cohort. This variability depends on the interaction of genetic and nongenetic factors, which are key phenotypic determinants that further affect the overall survival of wild fish and adaptability of cultured stocks. Although researchers and aquaculturists often refer to larvae quality as an important parameter discriminating high- and low-performing stocks, there is currently no universally accepted definition or critically verified set of quality indicators. Therefore, in this study, we generated unique families of Eurasian perch (Perca fluviatilis) larvae to follow their performance during the larval period. Next, we integrated the zootechnical performance data with transcriptomics data from freshly hatched larvae to identify specific molecular quality markers. Results: Zootechnical data revealed statistically significant differences (p < 0.05) in performance between 16 families reared. The RNA-seq data were processed using weighted gene correlation network analysis (WGCNA) and showed particularly significant interactions between gene modules and the length of larvae at the mouth-opening stage, emerging as an important quality-related trait. Next, by comparing the transcriptomic profiles of larvae with high and low lengths at mouth opening, we identified several differentially expressed genes, here chosen as putative larvae quality markers, involved in metabolic processes and antioxidant responses, such as fatty acid desaturase 2 (fads2) and glutathione peroxidase 1b (gpx1b). Conclusions: The findings highlight the length of the larvae at hatching as a valid parameter of larvae quality. Initial length is not just a numerical measurement; it serves as a specific indicator that strongly influences future larval development and survival. 'Longer' larvae appear to benefit from a higher metabolic rate, enhanced antioxidant defenses and a more advanced nervous system. As a result of these insights, we propose genes such as fads2, ctsl1, and gpx1b as potential biomarkers for evaluating larval quality. Our study represents a significant step toward a clear understanding of the factors that determine the quality of fish larvae, with implications for improving aquaculture practices.