Cultured fish: integrative biology and management of domestication and interactions with wild fish

Fish aquaculture for commodity production, fisheries enhancement and conservation is expanding rapidly, with many cultured species undergoing inadvertent or controlled domestication. Cultured fish are frequently released, accidentally and deliberately, into natural environments where they may survive well and impact on wild fish populations through ecological, genetic, and technical interactions. Impacts of fish released accidentally or for fisheries enhancement tend to be negative for the wild populations involved, particularly where wild populations are small, and/or highly adapted to local conditions, and/or declining. Captive breeding and supplementation can play a positive role in restoring threatened populations, but the biology of threatened populations and the potential of culture approaches for conserving them remain poorly understood. Approaches to the management of domestication and cultured‐wild fish interactions are often ad hoc, fragmented and poorly informed by current science. We develop an integrative biological framework for understanding and managing domestication and cultured‐wild fish interactions. The framework sets out how management practices in culture and for cultured fish in natural environments affect domestication processes, interactions between cultured and wild fish, and outcomes in terms of commodity production, fisheries yield, and conservation. We also develop a typology of management systems (specific combinations of management practices in culture and in natural environments) that are likely to provide positive outcomes for particular management objectives and situations. We close by setting out avenues for further research that will simultaneously improve fish domestication and management of cultured‐wild fish interactions and provide key insights into fundamental biology.     

Genetic population structure in flatfishes and potential impact of aquaculture and stock enhancement on wild populations in Europe

Marine fish wild stocks are known to be heavily depleted by overfishing and flatfish species are no exception. Wild catches being soon insufficient for responding to consumer demand, the cultivation of marine species appeared as a logical response to the need of seafood. Nevertheless, fish aquaculture also entails major impacts on wild populations from which genetic ones are now better known. The hybridization between domestic and native strains potentially have a genetic impact on recipient populations as long as 1) domestic populations are distinct from native wild ones (through domestication process, genetic improvement of captive stocks) and/or 2) the native wild populations are structured (metapopulation structure, local adaptation). Some of the flatfish species exhibit population differentiation and even local adaptation and the release of domestic genetically modified fishes (selected, transgenic) could threaten their survival in case of introgression. The impact of aquaculture on flatfishes is probably still low as land-based farms and low production levels guaranty low rates of escapes and therefore limited contacts between wild and farmed strains. However, flatfish aquaculture is regarded by experts as a rapidly growing domain that will greatly develop soon. In our opinion, this perspective, added to the quite good performances of farmed flatfishes when released into the wild, fully justifies a stronger interest from the scientific community to the conservation of their wild stocks.     

Monteiro's Storm‐petrel Oceanodroma monteiroi: a new species from the Azores

The existence of two seasonally distinct breeding populations of Oceanodroma storm‐petrels in the Azores islands was first documented in 1996. The discovery of morphological differences between the populations led to the suggestion that they may represent cryptic sibling species. Recent mtDNA and microsatellite analysis from storm‐petrel populations has considerably advanced our understanding of their taxonomic relationships. Here we present new information on the timing of breeding and moult of the two Azores populations, the extent of exchange of individuals between seasons, and diet from feather isotopes. We conclude that the hot‐season Azores population should be considered a new species for which we propose the name Oceanodroma monteiroi, Monteiro's Storm‐petrel. The species is both genetically distinct and genetically isolated from the sympatric cool‐season population of Madeiran Storm‐petrel Oceanodroma castro, and from all other populations of Oceanodroma castro in the Atlantic and Pacific Oceans examined to date. Differences in the vocalizations permit species recognition, and the extent of primary feather wear and stage of moult aids separation of the two species in the Azores, which is especially valuable during August when both attend the breeding colonies in large numbers. Feather carbon and nitrogen isotopes reveal that the diet of Monteiro's Storm‐petrel differs from that of the sympatric Madeiran Storm‐petrel during both breeding and non‐breeding seasons, and unlike the Madeiran Storm‐petrel, Monteiro's Storm‐petrel appears to maintain the same foraging environment during the summer and winter months, though it shows a dietary shift to higher trophic levels during the non‐breeding season. Monteiro's Storm‐petrel is thought to be confined to the Azores archipelago, where it is currently known to nest on just two small neighbouring islets. The total population size was estimated at 250–300 pairs in 1999.     

Uncovering QTL for resistance and survival time to Philasterides dicentrarchi in turbot (Scophthalmus maximus)

Disease resistance‐related traits have received increasing importance in aquaculture breeding programs worldwide. Currently, genomic information offers new possibilities in breeding to address the improvement of this kind of traits. The turbot is one of the most promising European aquaculture species, and Philasterides dicentrarchi is a scuticociliate parasite causing fatal disease in farmed turbot. An appealing approach to fight against disease is to achieve a more robust broodstock, which could prevent or diminish the devastating effects of scuticociliatosis on farmed individuals. In the present study, a genome scan for quantitative trait loci (QTL) affecting resistance and survival time to P. dicentrarchi in four turbot families was carried out. The objectives were to identify QTL using different statistical approaches [linear regression (LR) and maximum likelihood (ML)] and to locate significantly associated markers for their application in genetic breeding strategies. Several genomic regions controlling resistance and survival time to P. dicentrarchi were detected. When analyzing each family separately, significant QTL for resistance were identified by the LR method in two linkage groups (LG1 and LG9) and for survival time in LG1, while the ML methodology identified QTL for resistance in LG9 and LG23 and for survival time in LG6 and LG23. The analysis of the total data set identified an additional significant QTL for resistance and survival time in LG3 with the LR method. Significant association between disease resistance‐related traits and genotypes was detected for several markers, a single one explaining up to 22% of the phenotypic variance. Obtained results will be essential to identify candidate genes for resistance and to apply them in marker‐assisted selection programs to improve turbot production.     

SNP panel development for genetic management of wild and domesticated white bass (Morone chrysops)

White bass (Morone chrysops), striped bass and their interspecific hybrid are important game fishes, whereas the hybrid striped bass is an important aquaculture species in the US. Numerous state, federal and private hatcheries, therefore, rear these species for stocking purposes as well as for food fish. Although striped bass populations (both wild and domesticated) have been extensively evaluated, relatively little effort has been directed toward the study and improvement of white bass. In this study, we developed SNP resources to examine the genetic relationships among a long‐term domesticated white bass line and five potential founder stocks for selective breeding collected from drainages in Arkansas, Texas and Alabama. Using genotyping‐by‐sequencing, we generated 13 872 genome‐wide SNP loci across the six populations. Stringent filtering of SNP‐calling parameters identified 426 informative SNP loci. Population genetic and structure analyses using these loci revealed only moderate genetic differentiation between populations (global F_st = 0.083) and indicated two major genetic clusters. A final 57‐SNP assay was successfully designed and validated using the MassARRAY system. The developed SNP panel assigned 96 additional genotyped individuals to their population of origin with 100% accuracy. The SNP resources developed in this study should facilitate ongoing efforts in selective breeding and conservation of white bass.     

Microsatellite DNA markers for parental assignment in hybrid striped bass (Morone saxatilis × Morone chrysops)

Development of nine polymorphic microsatellites from a genomic library of hybrid striped bass (female Morone chrysops × male Morone saxatilus) DNA is described. Breeding of hybrid striped bass for aquaculture is based largely on breeding wild fish. Molecular markers such as microsatellites will be useful tools for developing broodstock, estimating heritability for production traits, and selective breeding via marker‐assisted selection. The nine polymorphic microsatellites include six dinucleotide and three complex repeat motifs. The number of alleles detected among a sample of 10 individuals of each species was relatively low. All polymerase chain reaction primer pairs also amplified products in the sea bass Dicentrarchus labrax.     

Comparison of population genetic estimates amongst wild,F1 and F2 cultured abalone (Haliotis midae)

Haliotis midae is South Africa's most important aquaculture species. The reproduction cycle is currently not closed as many farms rely on wild‐caught broodstock for seed production. However, there is an increasing interest in genetic improvement in commercial stocks, with a growing number of producers implementing selective breeding strategies. High throughput commercial production and mass spawning make it difficult to maintain breeding records; therefore, mostly mass selection is practised. The high fecundity and unequal parental contributions also often lead to increased levels of inbreeding. This study therefore aimed to assess the genetic effects of such breeding practices on commercial populations of H. midae. Using microsatellite loci, the genetic properties of a wild, an F1 and an F2 population were estimated and compared. Although there was no significant loss of genetic diversity amongst the cultured populations in comparison with the wild progenitor population, there was low‐to‐moderate genetic differentiation between populations. Relatedness amongst the F2 population was significant, and the rate of inbreeding was high. The effective population size for the F2 (±50) was also comparatively small with respect to the wild (∞) and F1 (±470) populations. These results suggest that farms need to give caution to breeding practices beyond the first (F1) generation and aim to increase effective population sizes and minimise inbreeding to ensure long‐term genetic gain and productivity. This study also confirms the usefulness of population genetic analyses for commercial breeding and stock management in the absence of extensive pedigree records.     

Genetic structure and divergence of tench Tinca tinca European populations

The tench Tinca tinca is a freshwater species with human-mediated translocations, aquaculture interest and limited information on its genetic structure. mtDNA sequencing analysis of control region and two genes in 50 individuals from five European populations identified two phylogroups, with greater variability than that reported until now, and a hybridization zone in the Danube River region. Restriction analyses of additional samples reveal the complicated genetic structure characteristics of tench's wild and translocated populations, supporting future breeding practices.     

Moulded by humans: The domestication of blue‐veined cheese fungi

It is hard to imagine a world without food‐associated microbes. The production of bread, wine, beer, salami, coffee, chocolate, cheese and many other foods and beverages all rely on specific microbes. In cheese, myriad microbial species collaborate to yield the complex organoleptic properties that are appreciated by millions of people worldwide. In the early days of cheese making, these complex communities emerged spontaneously from the natural flora associated with the raw materials, the equipment, the production environment or craftsmen involved in the production process. However, in some cases, the microbes shifted their natural habitat to the new cheese‐associated environment. The most obvious cause of this is backslopping, where part of a fermented product is used to inoculate the next batch. In addition, some microbes may simply adhere to the tools used in the production process. These microbial communities gradually adapted to the novel man‐made niches, a process referred to as “domestication.” Domestication is associated with specific genomic and phenotypic changes and ultimately leads to lineages that are genetically and phenotypically distinct from their wild ancestors. In this issue of Molecular Ecology, Dumas et al. have investigated a prime example of cheese‐associated microbes, the fungus Penicillium roqueforti. The authors identified several hallmarks of domestication in the genome and phenome of this species, allowing them to hypothesize about the origin of blue‐veined cheese fungi domestication, and the specific evolutionary processes involved in adaptation to the cheese matrix.     

PCR primers for trinucleotide and tetranucleotide microsatellites in greater amberjack,Seriola dumerili

Eighteen nuclear‐encoded microsatellites from a genomic DNA library of greater amberjack, Seriola dumerili, were isolated and characterized. The microsatellites include 13 perfect (five tetranucleotide and eight trinucleotide) and five imperfect (three tetranucleotide, one trinucleotide and one combination dinucleotide/trinucleotide) repeat motifs. The number of alleles at the 18 microsatellites among a sample of 29 fish ranged from two to 20; gene diversity (expected heterozygosity) ranged from 0.068 to 0.950, whereas observed heterozygosity ranged from 0.069 to 0.966. Following Bonferroni correction, genotypes at all 18 microsatellites fit expectations of Hardy–Weinberg equilibrium, and all pairwise comparisons of microsatellites did not deviate significantly from genotypic equilibrium. Greater amberjack support commercial and recreational fisheries along both the Atlantic and the Gulf coasts of the USA and represent a species with potential for worldwide aquaculture. The microsatellites developed will be useful for population genetic studies of ‘wild’ populations and breeding studies of domesticated populations.     

A new strain group of common carp: The genetic differences and admixture events between Cyprinus carpio breeds

Common carp (Cyprinus carpio) has an outstanding economic importance in freshwater aquaculture due to its high adaptive capacity to both food and environment. In fact, it is the third most farmed fish species worldwide according to the Food and Agriculture Organization. More than four million tons of common carp are produced annually in aquaculture, and more than a hundred thousand tons are caught from the wild. Historically, the common carp was also the first fish species to be domesticated in ancient China, and now, there is a huge variety of domestic carp strains worldwide. In the present study, we used double digestion restriction site‐associated DNA sequencing to genotype several European common carp strains and showed that they are divided into two distinct groups. One of them includes central European common carp strains as well as Ponto–Caspian wild common carp populations, whereas the other group contains several common carp strains that originated in the Soviet Union, mostly as cold‐resistant strains. We believe that breeding with wild Amur carp and subsequent selection of the hybrids for resistance to adverse environmental conditions was the attribute of the second group. We assessed the contribution of wild Amur carp inheritance to the common carp strains and discovered discriminating genes, which differed in allele frequencies between groups. Taken together, our results improve our current understanding of the genetic variability of common carp, namely the structure of natural and artificial carp populations, and the contribution of wild carp traits to domestic strains.     

基因组选择在猪杂交育种中的应用

基因组选择是指在全基因组范围内通过基因组中大量的标记信息估计出个体全基因组范围的育种值,可进一步提升育种效率和准确性,目前在猪纯繁育种中得到广泛应用。但有研究表明,现有的基因组选择方法在猪杂交育种上的应用效果并不理想,在跨群体条件下预测准确性极低。杂交作为养猪业中最为广泛的育种手段之一,通过结合基因组选择理论进一步提升猪的生产性能,具有重要的经济和研究价值。本文综述了基因组选择的发展及其在猪育种中的应用现状,并结合国内外猪杂交育种的方式,分析了目前基因组选择方法在猪杂交育种应用方面的不足,旨在为未来基因组选择在猪杂交育种中的合理应用提供参考。     

Applying the latest advances in genomics and phenomics for trait discovery in polyploid wheat

Improving traits in wheat has historically been challenging due to its large and polyploid genome, limited genetic diversity and in‐field phenotyping constraints. However, within recent years many of these barriers have been lowered. The availability of a chromosome‐level assembly of the wheat genome now facilitates a step‐change in wheat genetics and provides a common platform for resources, including variation data, gene expression data and genetic markers. The development of sequenced mutant populations and gene‐editing techniques now enables the rapid assessment of gene function in wheat directly. The ability to alter gene function in a targeted manner will unmask the effects of homoeolog redundancy and allow the hidden potential of this polyploid genome to be discovered. New techniques to identify and exploit the genetic diversity within wheat wild relatives now enable wheat breeders to take advantage of these additional sources of variation to address challenges facing food production. Finally, advances in phenomics have unlocked rapid screening of populations for many traits of interest both in greenhouses and in the field. Looking forwards, integrating diverse data types, including genomic, epigenetic and phenomics data, will take advantage of big data approaches including machine learning to understand trait biology in wheat in unprecedented detail.     

Molecular Population Genetics of Rice Domestication

Domestication is a selection process that genetically modifies species to meet human needs. A most intriguing feature of domestication is the extreme phenotypic diversification among breeds. What could be the ultimate source of such genetic variations? Another notable outcome of artificial selection is the reduction in the fitness of domesticated species when they live in the wild without human assistance. The complete sequences of the two subspecies of rice cultivars provide an opportunity to address these questions. Between the two subspecies, we found much higher rates of non‐synonymous (N) than synonymous (S) substitutions and the N/S ratios are higher between cultivars than between wild species. Most interestingly, substitutions of highly dissimilar amino acids that are deleterious and uncommon between natural species are disproportionately common between the two subspecies of rice. We suggest strong selection in the absence of effective recombination may be the driving force, which we called the domestication‐associated Hill‐Robertson effect. These hitchhiking mutations may contribute to some fitness reduction in cultivars. Comparisons of the two genomes also reveal the existence of highly divergent regions in the genomes. Haplotypes in these regions often form highly polymorphic linkage blocks that are much older than speciation between wild species. Genes from such regions could contribute to the differences between indica and japonica and are likely to be involved in the diversifying selection under domestication. Their existence suggests that the amount of genetic variation within the single progenitor species Oryza rufipogon may be insufficient to account for the variation among rice cultivars, which may come from a more inclusive gene pool comprising most of the A‐genome wild species. Genes from the highly polymorphic regions also provide strong support for the independent domestication of the two subspecies. The genomic variation in rice has revealing implications for studying the genetic basis of indica‐japonica differentiation under rice domestication and subsequent improvement.     

Genetic interactions between marine finfish species in European aquaculture and wild conspecifics

The principal species of marine aquaculture in Europe are Atlantic salmon (Salmo salar), sea bass (Dicentrarchus labrax) and sea bream (Sparus auratus). For Atlantic salmon and sea bass, a substantial part of total genetic variation is partitioned at the geographical population level. In the case of sea bream, gene flow across the Azores/Mediterranean scale appears to be extensive and population structuring is not detected. For Atlantic salmon and sea bass, natural population structure is at risk from genetic interaction with escaped aquaculture conspecifics. The locally adaptive features of populations are at risk from interbreeding with non‐local aquaculture fish. Wild populations, generally, are at risk from interactions with aquaculture fish that have been subject to artificial selection or domestication. Atlantic salmon is the main European aquaculture species and its population genetics and ecology have been well‐studied. A general case regarding genetic interactions can be based on the information available for salmon and extended to cover other species, in the appropriate context. A generalized flow chart for interactions is presented. Salmon escape from aquaculture at all life stages, and some survive to breed among wild salmon. Reproductive fitness in the escaped fish is lower than in native, wild fish because of behavioural deficiencies at spawning. However, as the number of salmon in aquaculture greatly exceeds the number of wild fish, even small fractional rates of escape may result in the local presence of large numbers, and high frequencies, of escaped fish. At present, policy and legislation in relation to minimizing genetic interactions between wild and aquaculture fish is best developed for Atlantic salmon, through the recommendations of the Oslo Agreement developed by the North Atlantic Salmon Conservation Organization and subsequent agreements on their implementation. In future, the potential use of genetically modified fish in aquaculture will make additional policy development necessary. Improved containment is recommended as the key to minimizing the numbers and therefore the effects of escaped fish. Emergency recovery procedures are recommended as a back‐up measure in the case of containment failure. Reproductive sterility is recommended as a future key to eliminating the genetic potential of escaped fish. The maintenance of robust populations of wild fish is recommended as a key to minimizing the effects of escaped fish on wild populations.     

Geography and end use drive the diversification of worldwide winter rye populations

To meet the current challenges in human food production, improved understanding of the genetic diversity of crop species that maximizes the selection efficacy in breeding programs is needed. The present study offers new insights into the diversity, genetic structure and demographic history of cultivated rye (Secale cereale L.). We genotyped 620 individuals from 14 global rye populations with a different end use (grain or forage) at 32 genome‐wide simple sequence repeat markers. We reveal the relationships among these populations, their sizes and the timing of domestication events using population genetics and model‐based inference with approximate Bayesian computation. Our main results demonstrate (i) a high within‐population variation and genetic diversity, (ii) an unexpected absence of reduction in diversity with an increasing improvement level and (iii) patterns suggestive of multiple domestication events. We suggest that the main drivers of diversification of winter rye are the end use of rye in two early regions of cultivation: rye forage in the Mediterranean area and grain in northeast Europe. The lower diversity and stronger differentiation of eastern European populations were most likely due to more intensive cultivation and breeding of rye in this region, in contrast to the Mediterranean region where it was considered a secondary crop or even a weed. We discuss the relevance of our results for the management of gene bank resources and the pitfalls of inference methods applied to crop domestication due to violation of model assumptions and model complexity.     

Impacts of domestication on population genetics of a traditional Chinese medicinal herb,Atractylodes macrocephala (Asteraceae)

As a medicinal herb, Atractylodes macrocephala Koidz. experienced centuries of cultivation in China, and germplasm resources of all cultivated populations have degraded over time as a consequence of domestication processes. This study used chloroplast DNA and microsatellites to clarify not only the effects of domestication on population genetics, but also determine the geographic origins of landraces. The results revealed that cultivated populations (except the “Pingzhu” landrace) showed higher genetic diversity than their wild counterparts and low levels of genetic differentiation occurred between cultivated and wild groups. Furthermore, STRUCTURE and UPGMA analyses grouped all wild populations into three genotypic clusters, two of which (in Shaanxi and Hunan Province) shared the same gene pool with cultivated A. macrocephala, suggesting that wild populations in Central China have been involved in the origin of cultivated A. macrocephala. Moreover, the wild population from Qimen, Anhui Province and the cultivated “Pingzhu” landrace harbor unique gene pools and rare alleles that could be useful in future breeding efforts. This large‐scale analysis of population genetics on a medicinal herb that has a centuries‐long history of human‐mediated selection will facilitate utilization and conservation of the valuable genetic resources of medicinal species.     

Identification of polymorphic microsatellite loci in the mud crab Scylla serrata (Brachyura: Portunidae)

Five microsatellite loci are identified and characterized from the genome of Scylla serrata, a widespread and commercially important species of coastal marine crab. The loci were detected by randomly screening for di‐ and tri‐nucleotide repeat units within a partial genomic library developed for the species. The five loci consist of dinucleotide repeats and are both co‐dominant and polymorphic within the species. A sample (N = 36) of S. serrata from one Australian population has an average observed heterozygosity of 0.875 and provides no evidence of either linkage among loci or significant deviation from random mating expectations across loci. PCR products for each of the five loci were also observed from a small sample of three other species within the Scylla genus. These markers may provide genetic information that will be useful for both aquaculture and studies of natural populations of the genus.     

‘Big data’ from shrinking pathogen populations

Falling costs for genome sequencing and genotyping mean that population genomic data sets are becoming commonplace for a wide variety of species. Once these data are used for the initial tasks of investigating population structure and demographic history, however, is there reason to go back for more? In this issue of Molecular Ecology, Nkhoma et al. (2013) explore the applications of longitudinal genomic diversity data for detecting changes in the prevalence and transmission of the Plasmodium falciparum malaria parasite in South‐East Asia. While this study finds several genetic signatures indicative of reduced disease transmission, other measures, such as short‐term effective population size, geographical population structure and heterozygosity, were not informative. These results indicate the potential contribution of genomic data to the surveillance of small, dynamic populations, whether they are at risk of extinction or targeted for elimination. The interpretation of such data will require close consideration of biological context, however, at both the species and the population level.