The Pacific white shrimp, Litopenaeus vannamei, is naturally distributed in tropical waters off the Pacific Ocean from Peru to Mexico, from the Gulf of Mexico to central Peru, especially close to Ecuador (Zhang et al., 1990). It benefits from small head and chest armor, high meat content, strong stress resistance, fast growth, a long breeding period, high density and low salinity tolerance for aquaculture, and simple transportation of live shrimp. Along with Fenneropenaeus chinensis and Penaeus monodon, it is listed as one of the world’s three most widely cultivated shrimp species and is crucial to both shrimp fisheries and aquaculture (Wang et al., 2004; Zhang et al., 2009).

One of the most important methods for genetic improvement in aquatic animals is cross-breeding (Zhang et al., 2019). Their offspring can outperform their parents in terms of production performance, environmental tolerance, and meat quality by crossing individuals of different strains or genotypes (Piferrer et al., 2009). Because they can quantify the level of heterosis obtained after crossing different lines and reflect the matching effect of target traits, heterosis and combining ability are very important references in breeding. Zhou (Zhou et al., 2021) studied the heterosis and combining ability of body mass traits of three populations of Penaeus monodon through a complete diallel cross design. Sun (Sun et al., 2011) discovered significant differences in high ammonia-N tolerance among various families of Penaeus monodon, and He (He et al., 2008) found that there were significant differences in the resistance of juvenile shrimp seedlings among Chinese shrimp families. Different families have significant differences in tolerance to ammonia-N and pH, indicating significant selection potential. Fang (Fang et al., 2000) discovered that as pH increased, fewer juvenile Chinese shrimp survived. Acute salinity stress has been shown to affect the growth and survival rate of L. vannamei larvae in previous studies. Pan (Pan et al., 2007) reported these findings; Lin (Lin et al., 2010) compared the tolerance of different families of L. vannamei to freshwater and obtained the basic population of excellent freshwater tolerant families; and Wang (Wang et al., 2022) discovered that both growth and comprehensive stress tolerance traits can be genetically improved through breeding, and growth traits can also be manipulated. This study aims to evaluate the stress tolerance of the breeding population, access the mortality rates of two introduced self-bred and hybrid families of L. vannamei under 96 h of high ammonia-N, high pH, and low salt stress, provide candidate materials for further family selection, and provide reference data for stress resistance breeding of L. vannamei.

The genetic basis, disease resistance and pathogenicity of pathogenic microorganisms of mariculture animals are significantly impacted by adverse water quality factors in the aquaculture environment, such as abnormal temperature, salinity, ammonia-N content, pH, nitrite, and other stress factors (He et al., 2008). The main pollutant in the environment for shrimp farming is Ammonia-N, which is primarily found in the water body as non ionized ammonia (NH₃) and ionic ammonia (NH₄ ⁺), both of which are in a dynamic equilibrium. Because NH₃ is not charged and has high fat solubility, it can penetrate cell membranes and negatively affect shrimp growth, molting, oxygen consumption, immunity, ammonia-N excretion, osmotic pressure regulation and disease resistance (Lei and Chen, 2003; Huang et al., 2012; Cui et al., 2017). pH is an important ecological factor that affects the survival status of aquaculture organisms and can reflect the quality of the water. Due to their extreme sensitivity to acidification and alkalization, shrimp and crab species can be somewhat impacted by high or low pH levels in terms of growth, immunity, ion balance, etc. The osmotic regulation of crustaceans is closely related to environmental salinity. Acute salinity stress will have an impact on the osmotic pressure of the internal environment, the level of respiratory metabolism, and immune function (Camacho-Jiménez et al., 2018; Joseph and Philip, 2020). Breeding work based on family lines, such as Pinctada martensii, Argopectenirradians, Patinopectenyessoensis, Paralichthys olivaceus, etc., has gradually become more popular in recent years (He et al., 2007; Qin et al., 2007; Chen et al., 2008; Zhang et al., 2008). When compared to population selection, family selection has the advantages of fast speed, obvious effects, high work efficiency, flexible operation, and outstanding excellent traits. The family’s genetic composition is relatively uniform, making it simple to determine the genotypes of the parents and offspring. As a result, family selection has begun to be widely applied in the breeding of superior aquatic animal varieties. Another important advantage of family selection is the ability to estimate the breeding values of some difficult to measure traits of the parents by observing the phenotypic traits of whole or half sib families. This enables the selection of quantitative traits through family selection, such as growth rate and disease resistance (Wu et al., 2011).

Twenty families from 4 populations of 2 introduced populations of L. vannamei were used as experimental subjects in this study through a combination of self-breeding and hybridization. Seven families with strong tolerance were initially selected using ammonia-N, pH, and salinity tolerance as indicators. The optimal families under ammonia-N and pH stress overlapped (TT2), and some families overlapped under low salt and pH stress. Chinese shrimp larvae from different families were subjected to acute toxicity tests, and He (He et al., 2008) discovered that there were significant differences in ammonia-N tolerance and high pH traits, indicating significant selection potential. Chen (Chen et al., 2017) tested the low salt tolerance of 11 families of Penaeus monodon and found significant differences in each family’s survival rate at half-lethal time. In order to select strains of shrimp with stress resistance and resolve the paradox between environmental degradation and high yield in the later stages of shrimp breeding from the perspective of genetic improvement of breeding varieties, comparative analysis of physical differences between different populations, further analysis of heterosis of stress resistance, and comparison of genetic differences between different mating combinations are necessary (Camacho-Jiménez et al., 2018). In this experiment, a study on the mortality rate of families constructed from the same source of maternal and paternal parents found that although the mortality rates of families were different, there was no significant difference (P > 0.05). The progeny populations whose male parent were from the Thai and American populations had higher survival rates than those whose female parent were from the Thai and American populations under ammonia nitrogen and pH stresses, but the opposite results were observed under low salt stresses. The overall tolerance of different groups of families to ammonia-N, pH, and low salt is generally higher than that of Thai sources. The American strain (MM) and a few hybrid strains (MT) performed better under ammonia-N, pH, and low salt stress, whereas the Thai strain (TT) and a few Thai American hybrid families performed worse, indicating the American strain’s advantages in stress resistance. It can be assumed that this advantage was brought about by the American strain’s strong capacity for stress resistance. The Thai strain is relatively weak, and another possibility is that the advantage of stress resistance is determined jointly by both hybrid strains rather than by the advantage of a single strain. The possibility needs to be further investigated in future generations. The analysis showed that the hybrid families of Thailand and the United States had heterosis for ammonia-N and pH tolerance, and that, with the exception of low salt stress, the average heterosis value of growth traits of hybrid combinations was positive (14.89% to 81.67%). L. vannamei’s growth traits have been the subject of many studies both domestically and abroad, and it has been discovered that hybrid combinations generally show heterosis in growth performance (Sui et al., 2016; Lu et al., 2017). For ammonia-N and pH traits, TM and MT populations showed different levels of heterosis, but overall, the heterosis of TM was better than that of MT, and the average heterosis rate of the TM population for ammonia-N was the highest, 81.67%. In low salt tolerance, the hybrid combinations showed a certain degree of hybridization disadvantage (−10.13% to −7.80%), which was weaker than the median of both parents. Ji (Ji et al., 2018) compared the stress resistance and growth traits of the first generation of shrimp in different populations of L. vannamei, and found that the results were consistent. The survival rates of the four populations under acute stress showed that the stress resistance of the MM and MT populations was slightly higher than that of the TT and TM populations, and that the inheritance of the maternal parent was dominant. The hybrid MT population demonstrated significantly greater stress resistance than that of the TM population. Different cross combinations show different heterosis, and heterosis of different characters also varies. Heterosis is a complex biological phenomenon. According to some studies, the stronger the complementarity and the more obvious the heterosis, the greater the genetic difference between hybrid parents (Pillai et al., 2011). In this experiment, the hybrid population showed poor performance in low salt stress resistance, which may be due to the enrichment of harmful recessive genes at different loci in parents with different genetic backgrounds. The probability of growth or stress resistance decline in the hybrid offspring will increase if the harmful recessive genes in the chromosomes provided by the parents of the hybrid offspring happen to be alleles (Ma et al., 2005). Selection of parents is crucial in the hybrid breeding process because improper parent selection could result in the regression of certain important economic traits in hybrid offspring.

Stress resistance is a threshold trait that multiple genes control and refers to an organism’s ability to adapt to harsh environments. It is generally believed that heritability is relatively low and that it is relatively difficult to improve traits through breeding (Bulmer, 1980). The research on the stress resistance of Penaeus monodon (Huang et al., 2012), Macrobrachium rosenbergii (Thanh et al., 2010) and Penaeus chinensis (Li et al., 2005) shows that the stress resistance of some aquatic animals has high heritability and can be improved through breeding. This study screened out superior populations (MM and MT), as well as high ammonia-N and high pH families (TT2) and low salt families (MM10) using the average mortality rate and hybrid advantage of families under high ammonia-N, high pH, and low salt stress for 96 h. The results of this study provide two candidate dominant families for the breeding of L. vannamei families. The next step is to preserve the selected families with strong stress resistance and improve the stress resistance of the families through continuous breeding and purification. In addition, the genetic structure of different populations and families will be analyzed at the molecular level, and molecular marker-assisted breeding will be carried out for further verification and selection in future breeding work. To provide reference data for breeding a new strain of L. vannamei that is fast-growing and stress-resistant and has significantly improved target economic traits. to.

The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding author.

The animal study was reviewed and approved by the Animal Care and Use Committee of the South China Sea Fisheries Research Institute.

MS, SJ, YL, and FZ: conceptualization. MS, SJ, SGJ, YL, and QY: methodology. MS and SJ: data curation. MS: writing—original draft preparation. FZ: writing—review and editing. All authors contributed to the article and approved the submitted version.