Novel insights into the selective breeding for disease resistance to vibriosis by using natural outbreak survival data in Chinese tongue sole (Cynoglossus semilaevis)

doi:10.1016/j.aquaculture.2020.735670

Aquaculture

Volume 529, 15 December 2020, 735670

https://doi.org/10.1016/j.aquaculture.2020.735670 Get rights and content

Highlights

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Significant variation of vibriosis natural outbreak survival was observed among families of Chinese tongue sole.
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Low to moderate heritabilities for vibriosis resistance traits were estimated.
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The results provided novel insights for genetic improvement of vibriosis resistance by selective breeding in tongue sole.

Abstract

As an important farmed flatfish species, Chinese tongue sole (Cynoglossus semilaevis) is heavily threatened by vibriosis in recent years. Genetic selection for disease resistance is a sustainable and effective approach to reduce frequent outbreaks. To verify whether the resistance of vibriosis (caused by co-infections of different Vibrio spp. in natural outbreak) can be included in breeding programs, in this study, genetic analysis of resistance to vibriosis based on natural outbreak survival data was carried out by using four statistical models (three cross-sectional models and one longitudinal model). The magnitude of the genetic variation in the resistance of vibriosis was estimated through a 56-day natural outbreak test of 15,912 individuals from 78 full-sib families (the offspring of 77 sires and 78 dams). Variance components and heritabilities were estimated at two cut-off points respectively, i.e. day 35 with 49.2% cumulative mortality and day 56 with 71.6% finial cumulative mortality. Heritabilities of resistance to vibriosis were low to moderate, where values at day 56 (0.04–0.21) were significantly different from zero, while values at day 35 (0.03–0.10) were not significantly different from zero in each corresponding model. The Spearman rank correlations between family EBVs for different models were high (> 0.98), indicating a nearly identical ranking of families. Compare to three simpler cross-section models, the longitudinal model taken the time until death into account demonstrated the highest accuracy of family selection. These results confirmed the existence of genetic variation for resistance to vibriosis and provided novel insights into the selective breeding for disease resistance to vibriosis by using natural outbreak survival data in tongue sole.

Introduction

Chinese tongue sole (Cynoglossus semilaevis) is an indigenous marine flatfish species which is widely distributed in China's north coastal areas (Guan et al., 2018). Tongue sole has been overfished since the 1990s, and indoor farming began in 2003 then with a rapid development of aquaculture industry (Guan et al., 2018). Now, tongue sole contributes to a large part of flatfish species production and is one of the most expensive farmed fish species on the market in China (Song et al., 2020; Guan et al., 2018). With the development of production scale and intension of aquaculture industry of tongue sole, high-stress rearing environmental conditions such as high stocking density, inadequate nutrition and problems related to water quality should be responsible for frequent disease outbreaks with significant production losses.

Vibrio spp. as important global fish pathogenic bacteria with a wide range of aquatic hosts (Mohamad et al., 2019), have emerged as the most important disease in tongue sole in China, an epidemic with a high mortality rate (50%–70%) recently observed mainly in juvenile fish (body length between 10 cm and 20 cm) at relatively high summer temperatures (Li et al., 2019; Zhang et al., 2015; Tang et al., 2008). Symptoms of vibriosis of tongue sole included surface ulcers, ascites, tail rot, eye infection and septicemia. Indeed, Vibrio spp., such as V. anguillarum, V. harveyi, V. vulnificus, V. salmonicida, V. alginolyticus, V. parahaemolyticus, V. rotiferianus, V. ponticus that are known to cause devastating impacts on cultured marine fishes worldwide due to their strong pathogenicity and ubiquitous presence in marine environment (Mohamad et al., 2019). Some Vibrio species are opportunistic pathogens to cultured fishes and can co-infect within the same host (Liu et al., 2016a; Kim et al., 2014; Gauger et al., 2006).

The common methods to control, prevent and treat vibriosis in aquaculture are by using disinfectors, vaccines and antibiotics. However, the Vibrio spp. pathogens have proven difficult to eradicate and prolonged misusage use of antibiotics in farms has resulted in limited success and antibiotic resistant strains (Nguyen et al., 2017; Rao and Lalitha, 2015; Song et al., 2014; Cabello et al., 2013; Magnadottir, 2010). In aquaculture, for obtaining a continuous and permanent genetic gain, the selective breeding has been proved a more effective approach to enhance disease resistance (Ødegård et al., 2011; Yáñez et al., 2014). Selective breeding for resistance to vibriosis have been well studied in several aquaculture species such as Atlantic cod (Gadus morhua L.) (Bangera et al., 2011, Bangera et al., 2013; Kettunen et al., 2007; Kettunen and Fjalestad, 2006), clam (Meretrix petechialis) (Liang et al., 2017), turbot (Scophthalmus maximus) (Wang and Ma, 2019), Pacific oyster (Crassostrea gigas) (Azéma et al., 2017).

Currently, for most aquaculture species, disease resistance is generally assessed based on challenge test data (Ødegård et al., 2011). Evidence showed that challenge test and natural infection may share a similar molecular mechanism which could be inferred from the high genetic correlation between experimental challenge and field outbreak data (Gjøen et al., 1997; Wetten et al., 2007). Hence, it is expected that the improvement of disease resistance either by challenge test or natural infection will be transferred to the commercial populations. For genetic analysis of survival traits in aquaculture species, standard statistical approaches and methodologies have been developed, including survival trait definitions and corresponding statistical models, for example case studies by Bangera et al. (2014), Yáñez et al. (2013), Ødegård et al., 2010a, Ødegård et al., 2011, Ødegård et al. (2006), Gitterle et al. (2006).

Selective breeding programs for disease resistance have been already established in tongue sole, mainly targeted at vibriosis (V. harveyi and V. anguillarum) (Li et al., 2019; Liu et al., 2016b) and edwardsiellosis (Edwardsiella tarda) (Li et al., 2020b; Liu et al., 2016b) based on challenge test data. However, genetic parameters and selection response about natural outbreak survival are still not available. To address this knowledge gap and include natural outbreak disease resistance into the breeding objective, the estimation of heritability is needed to understand whether genetic variation occurs for this desirable trait. So, in this study we aimed at estimating genetic parameters for resistance to vibriosis by using valuable natural outbreak survival data.

Section snippets

Fish material

Methods of family production and maintenance were as described by Li et al. (2019). Finally, 78 families (78 dams and 77 sires) were used in this study. In the early month of August 2014, approximately 200 individuals (total length 8–10 cm) from each family were random sampled, anesthetized and tagged (by family) with a visible implant elastomer (VIE) (Qingdao Starfish Instruments Co., Ltd). Before tagging, each family was reared in a separate tank. Tagging work completed on 8th August. All the

Descriptive statistics of survival

Cumulative mortality, mean family survival and minimum and maximum of family survival in two batches at day 35 and day 56 for natural vibriosis outbreak are given in Table 2. Kaplan-Meier survival curves of the best and the worst family and all the families and two replicated batches during the outbreak period were shown in Fig. 1. At day 35 and 56, the cumulative mortalities across all the families were 49.2% and 71.6% respectively. Survival rates varied considerably among families, which

Discussion

In aquaculture, frequent disease outbreaks have caused tremendous economic losses, reportedly by up to tens of billion dollars in the last two decades (FAO, 2015; FAO, 2016). Therefore, disease resistance as an economically important trait should be included in the breeding goal. Conventionally, for aquaculture fishes, selective breeding for improved disease resistance is mainly based on challenge test by injection with specific pathogens isolated from diseased fish with typical symptoms in

Conclusion

This is the first genetic analysis of vibriosis natural outbreak data in tongue sole. The estimated heritabilities for resistance to vibriosis using four different statistical models were low or not significantly different from zero at 35 days and were significant at day 56, indicating potential prospects for genetic improvement by using such data. Spearman rank correlations between family EBVs for the different models were all close to unity. Compare to simpler cross-section models (i.e., CLM,

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This work was supported by the China Agriculture Research System (CARS-47-G03).

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Chinese tongue sole (Cynoglossus semilaevis) is an economically important marine flatfish which is now severely threatened by various bacterial pathogens (especially at juvenile stage) in China. As we all known, it is of great importance to increase the natural disease resistance of farmed fish. So, the aim of this study was to verify the exitance of genetic variance of natural disease resistance and to detect the selection response by using juvenile natural survival data (involving four year-classes and three generations with 221 full-sib families, 195,589 individuals). Survival was defined as binary trait (dead/alive) fitted in two cross-sectional models (i.e. cross-sectional linear sire-dam model (CLM) and cross-sectional threshold (logit) sire-dam model (CTM)). Heritabilities of survival were estimated with each generation dataset and with complete dataset. Heritability estimates varied among generations regardless of model used, i.e., 0.01–0.17 and 0.03–0.25 for CLM and CTM respectively. On the observed (CLM) and underlying (CTM) scale with complete dataset, the heritabilities were 0.09 ± 0.04 and 0.13 ± 0.06 respectively. Both models performed nearly identical and very high selection accuracy (> 0.99), the accuracy of selection obtained from CLM (0.993) was slightly higher than CTM (0.991). By cross-validation, the prediction accuracy of CLM is 21% higher than CTM, which was 0.885 and 0.730 for CLM and CTM respectively. The average of predicted genetic gain for each generation was 14.89%, and the average of realized genetic gain was 8.10% per generation for juvenile survival. These results confirmed the existence of genetic variation for juvenile natural survival and highlighted the enormous potential for improving natural survival by selective breeding in tongue sole.

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