Interacción genotipo-ambiente en ganado de la raza Santa Gertrudis en Cuba

Abstract

Background: Shrimp farming is one of the pillars of aquaculture. Among the main shrimp species, Peneaus vannamei stands out, which represents around 70% of the world's shrimp production. The control of genetic diversity is essential to improve a selective breeding program in the shrimp industry. The volume of data on genetic markers in Peneaus vannamei has been growing in the last few years. Aim. To review and analyze the information related to genetic studies in this shrimp species using the most widely known molecular markers. Several different studies on genetic characterization through molecular markers in white-leg shrimp culture were reviewed. Development: This study also tackled the analysis of microsatellite and Single Nucleotide Polymorphism (SNP) markers of this Penaeus shrimp and the genetic characterization of shrimp populations in Cuba using molecular markers. This paper also includes different reviews of research studies of SNP trait-associated markers in Peneaus vannamei shrimp culture. Conclusions: Microsatellite and SNP markers were found to play an important role in the genetic characterization of Penaeus vannamei shrimps, as the most powerful tools for genome analysis. Furthermore, the genetic polymorphism markers associated with phenotypic traits can be used in future selective breeding applications in shrimp farming mainly in developing countries.

Keywords: shrimp, microsatellite, SNP (Source: MESH)

Resumen

Antecedentes: El cultivo intensivo del camarón es una de las principales actividades de la acuicultura. Entre las especies de camarones se destaca el Peneaus vannamei, que representa alrededor del 70% de la producción mundial. El control de la diversidad genética es fundamental para mejorar los programas de crianza selectiva dentro de la camaronicultura. En los últimos años se ha incrementado el volumen de información sobre los marcadores genéticos del Peneaus vannamei. Objetivo. Analizar la información sobre los estudios genéticos en esta especie de camarones a través de los marcadores genéticos de más amplio uso. Se valoraron diferentes estudios sobre la caracterización genética mediante el empleo de marcadores genéticos en cultivos de camarones blancos. Desarrollo: Se analizaron los marcadores microsatélites (SSR) y de polimorfismos de un solo nucleótico (SNP) en esta especie, así como las caracterizaciones genéticas de las poblaciones de camarón en Cuba mediante el empleo de marcadores genéticos. Por otra parte, se realizó una revisión de los SNP marcadores relacionados con rasgos fenotípicos del en cultivos de Peneaus vannamei. Conclusiones: El estudio reveló que los marcadores microsatélites y SNP son las herramientas más útiles para el análisis del genoma y desempeñan un rol significativo en la caracterización genética de Peneaus vannamei. Asimismo, esta revisión demostró las potencialidades de los marcadores genéticos asociados a rasgos fenotípicos para aplicar en la crianza selectiva en el cultivo de camarones, particularmente en los países en desarrollo.

Palabras clave: camarón, microsatélite, SNP (Fuente: MESH)

INTRODUCTION

Aquaculture is the fastest-growing sector of livestock raising, especially in recent years, with an astonishing development, accounting for a 5% annual growth rate. Aquaculture also emerged as one of the most productive industries with a potential for further expansion and development. In 2019, 86,500 tons were produced worldwide, compared to 2,500 tons in 1970 (Anderson et al., 2019; Fao., 2020).

Shrimp is among the most traded products and the second group of aquaculture species exported by its value (FAO, 2018). Shrimp farming is one of the pillars of aquaculture.(FAO, 2020; Sampantamit et al., 2020). Intensive shrimp farming has increased in the last ten years faster than the same specimens in their natural environment. However, high densities of animals in the culture generate stressful conditions, which are ideal for disease outbreaks. Viral and bacterial pandemics cause the highest losses to shrimp farmers (Flegel, 2019). Among the main species, Peneaus vannamei stands out, which represents around 70% of the world's shrimp production (FAO, 2020; Sampantamit et al., 2020). Peneaus vannamei is the most widely farmed species in the world. It is a euryhaline species with better tolerance in high population densities and greater availability of genetically selected viral pathogen-free domesticated broodstock (Chong-Robles et al., 2014).

The increased demand for shrimp in the international market led to the development of more efficient production systems through efficient management of larval development, controlled nutrition, advances in disease diagnosis, maintenance of water quality, and genetic improvements of productive indicators (Andriantahina et al., 2013). The control of genetic diversity is essential to improve a selective breeding program in the shrimp industry. A population with low genetic variability compared to others of the same species has a lower capacity to adapt to the environment (Tiknaik et al., 2020). There are several documented examples of inbreeding depression in closed cycle breeding among cultured species, Penaeus vannamei (Perez-Enriquez, Medina-Espinoza, et al., 2018). The development and use of best practices for the domestication and management of broodstock banks should be done through genetic techniques (Cobo and Pérez, 2018).

Considering the growing volume of data on genetic markers in Peneaus vannamei and because of the growing relevance of this topic in recent years, this paper aimed to review and analyze the information of genetic studies in Peneaus vannamei shrimp cultures using the most popular molecular markers for future studies and assess the utilization of single nucleotide polymorphisms (SNP) markers in future genetic breeding programs for this shrimp species in Cuba.

DEVELOPMENT

Genetic studies on farmed shrimp began more than forty years ago. The first cultivators, who completed the life cycles of species such as Penaeus monodon, considered the variations in gene frequency and the alteration of the development of these animals as they were cultivated (Andriantahina et al., 2013; Cobo and Pérez, 2018).

In Penaeus vannamei, the classification of microsatellite and polymorphism markers and their standardization in specific databases is still insufficient (Mangabeira-Silva et al., 2020). Over the last ten years, sequencing the P. vannamei genome meant a tremendous breakthrough, with the characterization of multiple markers, such as single nucleotide polymorphisms and microsatellites, the construction of linkage maps, and the generation of transcriptomes and partial genomes. Moreover, in the last 30 years of breeding, P. vannamei has been subjected to high selection pressures that have profoundly affected its genome (Zhang et al., 2019).

In aquaculture, these genetic markers monitor and select organisms in a culture that will be part of genetic crossbreeding programs. Through them, variability and genetic structure may determine the best crosses, minimize inbreeding and increase the selection response (Cobo and Pérez, 2018; Machado Tamayo, 2006).

Among molecular genetic markers, SSR and SNP are the most commonly recommended for analyzing genetic variability and association due to their properties (A. R. Cobo, 2016). A review of several studies on genetic diversity and population structure analysis using genetic markers SSR and SNP in P. vannamei shrimp to characterize populations (Table 1) revealed that the use of SNPs in recent years has been associated with advances in new-generation sequencing (NGS), SNP genotyping techniques, high levels of polymorphisms, genomic frequencies, and codominant inheritance of SNP markers. Garcia et al., 2021; Medrano-Mendoza et al. (2023) used the largest number of SNPs as genetic markers in genetic diversity studies, 50K (50 SNPs). This marker number greatly exceeded the 35 SSR used by Garcia and Alcivar-Warren (2007). In both markers, the total size of samples used in the last five years has increased, as did the number of populations of P. vannamei studied. The broodstocks are the stages studied most because they are relevant in obtaining satisfactory results in the shrimp production chain. Garcia and Alcivar-Warren (2007) obtained between 21 and 31 alleles per locus using 35 microsatellite markers, while Lu et al. (2018) obtained between 1.17 and 2.0 alleles per locus after genotyping 318919 SNP markers (Table 1).

Table 1. Genetic diversity and population structure analysis with Microsatellite or SSR markers and Single Nucleotide Polymorphism (SNPs) markers in P. vannamei shrimps to characterize populations. PL (Post-Larvas).

Marker Type	Marker number	Total sample size	Population studied	Live Stages	Quantity of alleles per locus	Reference
SSR	2	601	1	Broodstocks	7.5 - 10	(Cruz et al., 2004)
SSR	5	207	5	Adults/ Juveniles/PL	7.4 - 8.6	(Valles-Jimenez et al., 2004)
SSR	11	35	1	Adults	18	(Zhi‐Ying et al., 2006)
SSR	4	310	4	Broodstocks Juveniles/PL	4.5 - 6.8	(Tamayo, 2006)
SSR	35	48	4	Adults/ juveniles	21 - 31	(Garcia and Alcivar-Warren, 2007)
SSR	6	658	13	Broodstocks	8.9	(Perez-Enriquez et al., 2009)
SSR	4	200	5	Broodstocks	1.0 - 12	(Adriana Artiles et al., 2011)
SSR	4	130	6	Broodstocks	3.5 - 6	(Pérez-Beloborodova et al., 2012)
SSR	7	192	7	Adults	4.0 - 21	(Zhang et al., 2014)
SSR	4	123	4	Broodstocks	5.0 - 9.0	(Artiles et al., 2015)
SSR	10	90	1	Juveniles	7.8	(Andriantahina et al., 2015)
SSR	4	45	3	PL	5.0 - 10	(Rezaee et al., 2016)
SSR	7	216	3	Adults/ PL	4.0 - 8.0	(Suárez, 2016)
SSR	4	360	9	Broodstocks	3.5 - 9.0	(Cobo, 2016)
SSR	5	192	81	Broodstocks	6.6	(Perez-Enriquez and Max-Aguilar, 2016)
SNP	76	192	81	Broodstocks	1.97	(Perez-Enriquez and Max-Aguilar, 2016)
SSR	6	195	7	Broodstocks	14	(Guadalupe, 2017)
SNP	192	162	7	Broodstocks	1.9 -1.91	(Guadalupe, 2017)
SNP	6	119	3	Juveniles		(Ferreira Jr et al., 2017)
SSR	7	1162	30	Broodstocks	5.8 - 12.4	(Ren et al., 2018)
SSR	14	359	5	Broodstocks	3 - 13.2	(Perez-Enriquez, Medina-Espinoza, et al., 2018)
SSR	6	500	10	Broodstocks	15.6	(Perez-Enriquez, Millán-Márquez, et al., 2018)
SNP	318919	1849	7	Juveniles	1.17 - 2.0	(Lu et al., 2018)
SNP	2619	95	21	Broodstocks	1.3 -1.5	(Perez-Enriquez, Robledo, et al., 2018)
SSR	6	952/20000	8	Broodstocks	3.0 - 12.5	(Knibb et al., 2020)
SNP	19157	952/20000	7	Broodstocks		(Knibb et al., 2020)
SSR	16	1110	36	Adults	10 - 10.6	(Jiang et al., 2021)
SNP	50 K	96	140	Adults		(Garcia et al., 2021)
SSR	12	369	37	Adults	4.4 - 17	(Ren et al., 2022)
SNP	96	615	19	Broodstocks		(Silva et al., 2022)
SNP	192	311	6	Broodstocks	1.7 - 1.8	(Casado et al., 2022)
SNP	50 K	6160	176	Juveniles		(Medrano-Mendoza et al., 2023)

The review of studies on different applications of Microsatellite and Single Nucleotide Polymorphism genetic markers used in P. vannamei shrimp studies to characterize populations (Table 2) showed that 80.5% of the papers published targetted SNPs as genetic markers mainly for genetic linkage maps and association studies through quantitative trait loci (QTL). Medina Gonzaléz (2006) used the largest quantity of microsatellite markers (120 SSR) to design a genetic linkage map for the white shrimp Penaeus vannameiusing codominant markers. Moreover, (Jones, Jerry, Khatkar, Raadsma, Van Der Steen, et al. (2017) designed a comprehensive comparative gene-based linkage and linkage disequilibrium map for the Pacific white shrimp using a high-density marker with 234452 SNPs. Lu et al. (2018) used 318919 SNP high-density markers as MAS to identify SNP markers associated with tolerance to ammonia toxicity by selective genotyping from de novo assembled transcriptome in Penaeus vannamei. The high-density linkage maps are necessary to conduct genetic studies and identify the desired QTL Shekhar et al. (2021) and Sui et al. (2022) used the highest density marker (629748 SNP) as GWAS for genomic signatures of artificial selection in the fecundity of the Pacific white shrimp (Table 2). The assembled shrimp genome and a large amount of SNP markers provide a useful resource for the application of genome-wide association studies and genomic selection. That way, genetic breeding will take place at a faster rate in shrimp culture (Zhang et al., 2019).

Table 2. Different applications of Single Nucleotide Polymorphisms (SNPs) and microsatellite genetic markers in P. vannamei shrimp studies to characterize populations in the loci with quantity traits (QTL), genetic selection (GS), marker-assisted selection (MAS), and genome-wide association study (GWAS).

Marker Types	Markers Application	Marker number	Reference
SNP	Genetic linkage map and QTL	5	(Glenn et al., 2005)
SNP	Association Studies (QTL)	6	(Yu et al., 2006)
SSR	Genetic linkage map	120	(Medina González, 2006)
SSR	Genetic linkage map and GS	35	(Garcia and Alcivar-Warren, 2007)
SSR	Genetic linkage map	30	(Zhang et al., 2007)
SNP	Association Studies (QTL)	5	(Zeng et al., 2008)
SNP	Association Studies (QTL)	211	(Ciobanu et al., 2010)
SNP	Genetic linkage map	1344	(Du et al., 2010)
SNP	Association Studies (QTL)	18	(Liu et al., 2014b)
SNP	Association Studies (QTL)	38	(Liu et al., 2014a)
SNP	Genetic linkage map	25140	(Yu et al., 2015)
SSR	Genetic Selection (GS)	10	(Andriantahina et al., 2015)
SSR	Parentage assignment	5	(Perez-Enriquez and Max-Aguilar, 2016)
SNP	Parentage assignment	76	(Perez-Enriquez and Max-Aguilar, 2016)
SNP	Genetic linkage map	234452	(Jones, Jerry, Khatkar, Raadsma, Van Der Steen, et al., 2017)
SNP	Association Studies (QTL)	6	(Ferreira Jr et al., 2017)
SNP	Genetic Selection (GS)	3.2K	(Wang et al., 2017)
SNP	Association Studies (QTL)	2619	(Perez-Enriquez, Robledo, et al., 2018)
SNP	Marker Assisted Selection (MAS)	318919	(Lu et al., 2018)
SNP	Association Studies (QTL)	7000	(Santos et al., 2018)
SNP	Parentage assignment and QTL	76	(Nolasco-Alzaga et al., 2018)
SNP	Association Studies (QTL)	30	(X. Zhang et al., 2019)
SNP	Genetic Selection (GS)	6	(Lien et al., 2019)
SNP	Genetic linkage map and QTL	17242	(Peng et al., 2020)
SNP	Genetic linkage map and QTL	17338	(Zeng et al., 2020)
SNP	Genetic Selection (GS)	3	(Perez-Enriquez et al., 2020)
SNP	Genetic linkage map	3567	(Huang et al., 2021)
SNP	Association Studies (QTL)	582	(Mangabeira-Silva et al., 2020)
SNP	Association Studies (QTL)	1	(Kaewduang et al., 2021)
SNP	Association Studies (QTL)	9	(Kongchum et al., 2022)
SNP	Genome-wide association study (GWAS)	94113	(Lyu et al., 2021)
SSR	Parentage assignment	16	(Jiang et al., 2021)
SSR	Genetic Selection (GS)	12	(Ren et al., 2022)
SNP	Genome-wide association study (GWAS)	629748	(Sui et al., 2022)
SNP	Parentage assignment	96	(Silva et al., 2022)
SNP	Genome-wide association study (GWAS)	50K	(Medrano-Mendoza et al., 2023)

DNA microsatellites have quickly become popular molecular markers for advanced biotechnology applications. The availability and use of microsatellites facilitate the collection of information on important functional traits such as survival and growth traits at the family level. High polymorphism and easiness of labeling are two of its main characteristics that apply to numerous genetic studies in shrimp (Machado Tamayo, 2006). SNP panels, on the other hand, are widely used to analyze genetic diversity in specific phenotypic elements from certain populations(Ciobanu et al., 2010).

D. K. Garcia and Alcivar-Warren, 2007 characterized 35 new microsatellite genetic markers in the Pacific white-leg shrimp to know their usefulness in the study of the genetic diversity of wild and cultured stocks, tracing pedigree in breeding programs, and linkage mapping. Genotypes and productive traits have been associated with several shrimp species, including the description of an SSR region linked to genetic diversity and growth breeding selection in Penaeus vannamei (Andriantahina et al., 2015). Another example is the description of SNPs associated with survival and disease resistance in Penaeus vannamei (Martin Marti et al., 2010). Furthermore, Medrano-Mendoza et al. (2023) evaluated the genetic diversity, population structure, and linkage disequilibrium and performed a genome-wide association study (GWAS) to search for single nucleotide polymorphisms (SNPs) that might be associated with the Pacific white shrimp (Penaeus vannamei) resistance to the White Spot Syndrome Virus (WSSV).

The identification of SNP markers in white shrimp was possible thanks to previously-reported coding regions in Genbank, using information analysis software (Du et al., 2010). Zhang et al. (2019) identified 31,993,474 single nucleotide polymorphisms (SNPs) in the genome of P. vannamei. These were the first data published about the alignment of the genome of these species, and the largest set of high-quality SNPs obtained from P. vannamei, in addition to the fact that it is a valuable resource for genetic research and selection. A limited number of research studies use genome-wide association studies (GWAS) in shrimp, which could be a potential resource for obtaining large numbers of SNP markers useful for the genomic selection of various traits in aquaculture species, but future development of low-cost, high-density markers in shrimp may be required to maximize the GWAS potential (Yu et al., 2014).

In Cuba, Artiles et al. (2011) estimated the genetic variability and the relatedness index between the five founding stocks of this same species, introduced and cultivated in Cuba in different years. In the fifth and last introduction, the authors detected the lowest heterozygosity values concerning the previous broodstock importations. The authors suggested the need to cross them with broodstock from different origins to improve the gene pool and production yields. Likewise, Pérez-Beloborodova et al. (2012) characterized the first descendants of four founder stocks and two crosses of P. vannamei introduced in Cuba for aquaculture, using four microsatellite loci. The authors observed the beginning of a drop in their genetic variables. Besides, Artiles et al. (2015) evaluated the genetic variation and productive markers of four progenies from the first cultured shrimp stock introduced in Cuba (Penaeus vannamei), and four microsatellite regions were explored to characterize the four populations cultured. Casado et al. (2022) made the first report on SNP use for the genetic characterization of an exotic shrimp species cultured in Cuba.

Recent advances in analytical methods and high throughput genotyping might contribute to simpler breeding schemes and increase genetic gain, particularly for complex traits or characteristics that are difficult to measure. Specifically, quantitative trait loci (QTL) mapping, or genes with a higher effect, may have an immediate application in marker-assisted selection (MAS) (Khatkar et al., 2017).

As a result of the rapid development of high-throughput sequencing and genotyping techniques, it is possible to identify multiple causative genes of phenotypic variants of P. vannamei (Lukwambe et al., 2019; Lyu et al., 2021; Wang, Yu, Zhang, Zhang, Yuan, et al., 2019).

At present, genomic data are used for shrimp farming; advances in genetics are expected to speed up over time. SNP use will contribute to genome selection and other relevant studies of the entire genome, depending on the amount of linkage disequilibrium (LD) determined (Garcia et al., 2021). So far, little genome-wide research has been done on this species.

CONCLUSION

This paper examined and analyzed information about genetic studies in Peneaus vannamei shrimp cultures based on the most widely used molecular markers. Microsatellite and Single Nucleotide Polymorphism markers play a critical role in the genetic characterization of Penaeus vannamei shrimp. These two molecular genetic markers represent the most powerful tools for genome analysis, and they permit the association of genetic traits with an underlying gene variation.

The inclusion of novel molecular biology techniques, and their optimization helped decrease the costs of SNP-assisted genetic determination, thus making the use of this technique in the genetic characterization of shrimp farming populations in Cuba possible. Nevertheless, this genetic study fails to meet the needs of Cuban shrimp culture. The knowledge about the presence of trait-associated single nucleotide polymorphism (SNP) markers in Peneaus vannamei shrimp culture could favor the implementation of a genetic management program for this shrimp species in Cuba.

Further studies on genetic marker-based penaeid shrimp genome could increase shrimp production substantially worldwide. The advantages of the knowledge acquired on diversity and the genetic structure of Peneaus vannamei populations permit the monitoring and decision-making concerning these populations to maximize diversity and manage genetic improvements and assess the genetic traits of new stocks. Single nucleotide polymorphism markers associated with phenotypic traits could be used in future selective breeding applications in shrimp farming, mainly in developing countries.

ACKNOWLEDGMENTS

The authors wish to thank Professor Peter Bossier, Ph.D., at the ARC-UGent for his collaboration and advisory. We also would like to thank the Belgium Fund for Cooperation and Development, through the VLIR-UOS, an organization that fosters associations between universities and colleges in Flanders (Belgium).

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AUTHOR CONTRIBUTION STATEMENT

Research conception and design: ECS, HCA, AAC; redaction of the manuscript: ECS, AAC.

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.