Search bioRxiv⌕ Search

Biology subjects

Jakobsen, K. S.

Publications and source records attributed to Jakobsen, K. S..

At least 37 records · Page 2Linked to original sources

Reference genome bias in light of species-specific chromosomal reorganization and translocations

Whole-genome sequencing efforts has during the past decade unveiled the central role of genomic rearrangements--such as chromosomal inversions--in evolutionary processes, including local adaptation in a wide range of taxa. However, employment of reference genomes from distantly or even closely related species for mapping and the subsequent variant calling, can lead to errors and/or biases in the datasets generated for downstream analyses. Here, we capitalize on the recently generated chromosome-anchored genome assemblies for Arctic cod (Arctogadus glacialis), polar cod (Boreogadus saida), and Atlantic cod (Gadus morhua) to evaluate the extent and consequences of reference bias on population sequencing datasets (approx. 15-20x coverage) for both Arctic cod and polar cod. Our findings demonstrate that the choice of reference genome impacts population genetic statistics, including individual mapping depth, heterozygosity levels, and cross-species comparisons of nucleotide diversity ({pi}) and genetic divergence (DXY). Further, it became evident that using a more distantly related reference genome can lead to inaccurate detection and characterization of chromosomal inversions, i.e., in terms of size (length) and location (position), due to inter-chromosomal reorganizations between species. Additionally, we observe that several of the detected species-specific inversions were split into multiple genomic regions when mapped towards a heterospecific reference. Inaccurate identification of chromosomal rearrangements as well as biased population genetic measures could potentially lead to erroneous interpretation of species-specific genomic diversity, impede the resolution of local adaptation, and thus, impact predictions of their genomic potential to respond to climatic and other environmental perturbations.

genomics↗

Genomic repeat landscape evolution across the teleost fish lineages

Repetitive DNA make up a considerable fraction of most eukaryotic genomes. In fish, transposable element (TE) activity have coincided with rapid species diversification. Here, we annotated the repetitive content in 100 genome assemblies, covering the major branches of the diverse lineage of teleost fish. We investigated if TE content correlates with family level net diversification rates and found support for a weak negative correlation. Further, we found that TE content, the degree of parental care and short tandem repeat (STR) content contributed to genome size variability. In contrast to TEs, STR content showed a negative relationship with genome size. STR content did not correlate with TE content, which implies independent evolutionary paths. Last, marine and freshwater fish have large differences in STR content. The most extreme propagation was found in the genomes of codfish species and Atlantic herring. Such a high density of STRs is likely to increase the mutational load, which we propose could be counterbalanced by high fecundity as seen in codfishes and herring.

evolutionary biology↗

Genomic consequences of range expansion and colonisation in the reed warbler (Acrocephalus scirpaceus)

Range expansion is a common natural phenomenon, which may be intensified by human-induced drivers such as climate change and alterations of habitat. The genetic consequences of range expansion are potentially major, and it is important to study known cases of range expansion to understand how human activities affect contemporary evolution, and to learn more about the genetic adaptive potential of species. The reed warbler (Acrocephalus scirpaceus) is a long-distance migratory bird breeding in Eurasia and wintering south of Sahara. It is currently expanding its range northwards, likely as a consequence of climate change. Interestingly, however, reed warblers have also recently colonised new territory southwards, following habitat restoration at the southern range margin. In this study, we investigate the genetic consequences of these two-directional range expansions with RAD-seq, looking at 10 populations from north to south in Europe. We investigate population structure and genome diversity, and assess the role of selection in divergence between populations across the species range. We do not find evidence of strong genetic structure in the reed warbler populations, and the youngest edge populations do not exhibit any substantial loss in genetic diversity, suggesting ongoing gene flow. On a smaller scale, the edge populations are the most genetically distinct, and we identify environmental disparity, especially in precipitation variability, as the main barrier of gene flow, to a greater extent than geographic distance. We find no evidence that the loci involved in population divergence and adaptation in the core populations are the same that are involved in adaptation at the range edges. Using three genome scan methods to identify selection, we found 49 SNPs putatively under selection, of which 33 were located in introns of 28 unique genes. Most of these are correlated with differences in climatic variables of temperature and precipitation. Some genome scan outliers show signs of being part of nascent selective sweeps, especially one which is distinct for the northern range edge. Our results suggest that in the reed warbler, contemporary range expansion has had little effect on molecular diversity and has been rapidly followed by local adaptation to climatic conditions, which could further corroborate the rapid pace at which colonisation of novel environments has occurred both northwards and southwards.

evolutionary biology↗

Ancient DNA evidence for the ecological globalisation of cod fishing in medieval and post-medieval Europe

Understanding the historical emergence and growth of long-range fisheries can provide fundamental insights into the timing of ecological impacts and the development of coastal communities during the last millennium. Whole genome sequencing approaches can improve such understanding by determining the origin of archaeological fish specimens that may have been obtained from historic trade or distant water. Here, we used genome-wide data to individually infer the biological source of 37 ancient Atlantic cod specimens (ca. 1050 to 1950 CE) from England and Spain. Our findings provide novel genetic evidence that eleventh- to twelfth-century specimens from London were predominantly obtained from nearby populations, while thirteenth- to fourteenth-century specimens derived from distant sources. Our results further suggest that Icelandic cod was exported to London earlier than previously reported. Our observations confirm the chronology and geography of the trans-Atlantic cod trade from Newfoundland to Spain starting by the early sixteenth century. Our findings demonstrate the utility of whole genome sequencing and ancient DNA approaches to describe the globalisation of marine fisheries and increase our understanding regarding the extent of the North-Atlantic fish trade and long-range fisheries in medieval and early modern times.

ecology↗

A Chromosome-level Genome Assembly of the Reed Warbler (Acrocephalus scirpaceus)

The reed warbler (Acrocephalus scirpaceus) is a long-distance migrant passerine with a wide distribution across Eurasia. This species has fascinated researchers for decades, especially its role as host of a brood parasite, and its capacity for rapid phenotypic change in the face of climate change. Currently, it is expanding its range northwards in Europe, and is altering its migratory behaviour in certain areas. Thus, there is great potential to discover signs of recent evolution and its impact on the genomic composition of the reed warbler. Here we present a high-quality reference genome for the reed warbler, based on PacBio, 10X and Hi-C sequencing. The genome has an assembly size of 1,075,083,815 bp with a scaffold N50 of 74,438,198 bp and a contig N50 of 12,742,779 bp. BUSCO analysis using aves_odb10 as a model showed that 95.7% of genes in the assembly were complete. We found unequivocal evidence of two separate macrochromosomal fusions in the reed warbler genome, in addition to the previously identified fusion between chromosome Z and a part of chromosome 4A in the Sylvioidea superfamily. We annotated 14,645 protein-coding genes, of which 97.5% were complete BUSCO orthologs. This reference genome will serve as an important resource, and will provide new insights into the genomic effects of evolutionary drivers such as coevolution, range expansion, and adaptations to climate change, as well as chromosomal rearrangements in birds. Significance statementThe reed warbler (Acrocephalus scirpaceus) has been lacking a genomic resource, despite having been broadly researched in studies of coevolution, ecology and adaptations to climate change. Here, we generated a chromosome-length genome assembly of the reed warbler, and found evidence of macrochromosomal fusions in its genome, which are likely of recent origin. This genome will provide the opportunity for a deeper understanding of the evolution of genomes in birds, as well as the evolutionary path and possible future of the reed warbler.

genomics↗

An accurate assignment test for extremely low-coverage whole-genome sequence data

Genomic assignment tests can provide important diagnostic biological characteristics, such as population of origin or ecotype. In ancient DNA research, such characters can provide further information on population continuity, evolution, climate change, species migration, or trade, depending on archaeological context. Yet, assignment tests often rely on moderate- to high-coverage sequence data, which can be difficult to obtain for many ancient specimens and in ecological studies, which often use sequencing techniques such as ddRAD to bypass the need for costly whole-genome sequencing. We have developed a novel approach that efficiently assigns biologically relevant information (such as population identity or structural variants) in extremely low-coverage sequence data. First, we generate databases from existing reference data using a subset of diagnostic Single Nucleotide Polymorphisms (SNPs) associated with a biological characteristic. Low coverage alignment files from ancient specimens are subsequently compared to these databases to ascertain allelic state yielding a joint probability for each association. To assess the efficacy of this approach, we assigned inversion haplotypes and population identity in several species including Heliconius butterflies, Atlantic herring, and Atlantic cod. We used both modern and ancient specimens, including the first whole-genome sequence data recovered from ancient herring bones. The method accurately assigns biological characteristics, including population membership, using extremely low-coverage (e.g. 0.0001x fold) based on genome-wide SNPs. This approach will therefore increase the number of ancient samples in ecological and bioarchaeological research for which relevant biological information can be obtained.

bioinformatics↗

Origin and fate of supergenes in Atlantic cod

Supergenes are sets of genes that are inherited as a single marker and encode complex phenotypes through their joint action. They are identified in an increasing number of organisms, yet their origins and evolution remain enigmatic. In Atlantic cod, four megabase-scale supergenes have been identified and linked to migratory lifestyle and environmental adaptations. Here, we investigate the origin and maintenance of these four supergenes through analysis of whole-genome-sequencing data, including a new long-read-based genome assembly for a non-migratory Atlantic cod individual. We corroborate that chromosomal inversions underlie all four supergenes, and show that they originated at different times between 0.40 and 1.66 million years ago. While we found no evidence for a role of introgression in the origin of the four supergenes, we reveal gene flux between supergene haplotypes with derived and ancestral arrangements, occurring both through gene conversion and double crossover. Our results suggest that supergenes can be maintained over long timescales in the same way as hybridizing species, through the purging of introduced genetic variation.

evolutionary biology↗

Complex population structure of the Atlantic puffin revealed by whole genome analyses

The factors underlying gene flow and genomic population structure in vagile seabirds are notoriously difficult to understand due to their complex ecology with diverse dispersal barriers and extensive periods at sea. Yet, such understanding is vital for conservation management of seabirds that are globally declining at alarming rates. Here, we elucidate the population structure of the Atlantic puffin (Fratercula arctica) by assembling its reference genome and analyzing genome-wide resequencing data of 72 individuals from 12 colonies. We identify four large, genetically distinct clusters, observe isolation-by-distance between colonies within these clusters, and obtain evidence for a secondary contact zone. These observations disagree with the current taxonomy, and show that a complex set of contemporary biotic factors impede gene flow over different spatial scales. Our results highlight the power of whole genome data to reveal unexpected population structure in vagile marine seabirds and its value for seabird taxonomy, evolution and conservation.

genomics↗

Innovation in NLR and TLR sensing drives the MHC-II free Atlantic cod immune system.

The genome sequencing of Atlantic cod revealed an immune system absent of specific cell surface toll-like receptors (TLRs), major histocompatibility complex (MHC) class II, invariant chain (CD74) and the CD4 (cluster of differentiation 4) receptor. Despite the loss of these major components considered as critical to vertebrate innate and adaptive immune systems the cod system is fully functional, however the underlying mechanisms of the immune response in cod remain largely unknown. In this study, ex vivo cod macrophages were challenged with various bacterial and viral microbe-associated molecular patterns (MAMP) to identify major response pathways. Cytosolic MAMP-PRR pathways based upon the NOD-like receptors (NLRs) and RIG-I-like receptors (RLRs) were identified as the critical response pathways. Our analyses suggest that internalization of exogenous ligands through scavenger receptors drives both pathways activating transcription factors like NF-kB (Nuclear factor-kappa B) and interferon regulatory factors (IRFs). Further, ligand-dependent differential expression of a unique TLR25 isoform and multiple NLR paralogues suggests (sub)neofunctionalisation toward specific immune defensive strategies. Our results further demonstrate that the unique immune system of the Atlantic cod provides an unprecedented opportunity to explore the evolutionary history of PRR-based signalling in vertebrate immunity.

immunology↗

Single cell transcriptome profiling of the Atlantic cod immune system

The Atlantic cods unusual immune system, entirely lacking the Major Histocompatibility class II pathway, has prompted intriguing questions about what mechanisms are used to combat bacterial infections and how immunological memory is generated. Here, we examine the diversity of 8,180 spleen cells and peripheral blood leukocytes by single cell RNA sequencing. Unbiased transcriptional clustering revealed eleven distinct immune cell signatures. Resolution at the single cell level enabled characterisation of the major cell subsets including the cytotoxic T cells, B cells, erythrocytes, thrombocytes, neutrophils and macrophages. Further, we describe for the first time rare cell subsets which may represent dendritic cells, natural killer-like cells and a population of cytotoxic cells expressing GATA-3. We propose putative gene markers for each cluster and describe the relative proportions of each cell type in the spleen and peripheral blood leukocytes. By single cell analysis, this study provides the most detailed molecular and cellular characterization of the immune system of the Atlantic cod so far.

immunology↗

Metagenomic shotgun analyses reveal complex patterns of intra- and interspecific variation in the intestinal microbiomes of codfishes

The relative importance of host-specific selection or environmental factors in determining the composition of the intestinal microbiome in wild vertebrates remains poorly understood. Here, we use metagenomic shotgun sequencing of individual specimens to compare the intra- and interspecific variation of intestinal microbiome communities in two ecotypes (NEAC and NCC) of Atlantic cod (Gadus morhua) - that have distinct behavior and habitats- and three Gadidae species that occupy a range of ecological niches. Interestingly, we find significantly diverged microbiomes amongst the two Atlantic cod ecotypes. Interspecific patterns of variation are more variable, with significantly diverged communities for most species comparisons, apart from the comparison between coastal cod (NCC) and Norway pout (Trisopterus esmarkii), whose community compositions are not significantly diverged. The absence of consistent species-specific microbiomes suggests that external environmental factors, such as temperature, diet or a combination there-off comprise major drivers of the intestinal community composition of codfishes. ImportanceThe composition of the intestinal microbial community associated with teleost fish is influenced by a diversity of factors, ranging from internal factors (such as host-specific selection) to external factors (such as niche occupation). These factors are often difficult to separate, as differences in niche occupation (e.g. diet, temperature or salinity) may correlate with distinct evolutionary trajectories. Here, we investigate four gadoid species with contrasting levels of evolutionary separation and niche occupation. Using metagenomic shotgun sequencing, we observe distinct microbiomes amongst two Atlantic cod (Gadus morhua) ecotypes (NEAC and NCC) with distinct behavior and habitats. In contrast, interspecific patterns of variation are more variable. For instance, we do not observe interspecific differentiation between the microbiomes of coastal cod (NCC) and Norway pout (Trisopterus esmarkii) whose lineages have evolutionary separated over 20 million years ago. The observed pattern of microbiome variation in these gadoid species is therefore most parsimoniously explained by differences in niche occupation.

microbiology↗

Genome sequencing of the nine-spined stickleback (Pungitius pungitius) provides insights into chromosome evolution.

The Gasterostidae fish family hosts several species that are important models for eco-evolutionary, genetic and genomic research. In particular, a wealth of genetic and genomic data have been generated for the three-spined stickleback (Gasterosteus aculeatus), the ecologys supermodel, while the genomic resources for the nine-spined stickleback (Pungitius pungitius) have remained relatively scarce. Here, we report a high-quality chromosome-level genome assembly of P. pungitius consisting of 5,303 contigs (N50 = 1.2 Mbp) with a total size of 521 Mbp. These contigs were mapped to 21 linkage groups using a high-density linkage map, yielding a final assembly with 98.5% BUSCO completeness. A total of 25,062 protein-coding genes were annotated, and ca. 23% of the assembly was found to consist of repetitive elements. A comprehensive analysis of repetitive elements uncovered centromeric-specific tandem repeats and provided insights into the evolution of retrotransposons. A multigene phylogenetic analysis inferred a divergence time of about 26 million years (MYA) between nine- and three-spined sticklebacks, which is far older than the commonly assumed estimate of 13 MYA. Compared to the three-spined stickleback, we identified an additional duplication of several genes in the hemoglobin cluster. Sequencing data from populations adapted to different environments indicated potential copy number variations in hemoglobin genes. Furthermore, genome-wide synteny comparisons between three- and nine-spined sticklebacks identified chromosomal rearrangements underlying the karyotypic differences between the two species. The high-quality chromosome-scale assembly of the nine-spined stickleback genome obtained with long-read sequencing technology provides a crucial resource for comparative and population genomic investigations of stickleback fishes and teleosts.

genomics↗

Switching on the light: using metagenomic shotgun sequencing to characterize the intestinal microbiome of Atlantic cod

The biological roles of the intestinal microbiome and how it is impacted by environmental factors are yet to be determined in wild marine fish species. Atlantic cod (Gadus morhua) is an ecologically important species with a wide-spread distribution in the North Atlantic Ocean. 16S rRNA-based amplicon analyses found no geographical differentiation between the intestinal microbiome of Atlantic cod from different locations. Nevertheless, it is unclear if this lack of differentiation results from an insufficient resolution of this method to resolve fine-scaled biological complexity. Here, we take advantage of the increased resolution provided by metagenomic shotgun sequencing to investigate the intestinal microbiome of 19 adult Atlantic cod individuals from two coastal populations in Norway - located 470 km apart. Our results show that the intestinal microbiome is dominated by the Vibrionales order, consisting of varying abundances of Photobacterium, Aliivibrio and Vibrio species. Moreover, resolving the species community to unprecedented resolution, we identify two abundant species, P. iliopiscarium and P. kishitanii, which comprise over 50% of the classified reads. Interestingly, genomic data shows that the intestinal P. kishitanii strains have functionally intact lux genes, and its high abundance suggests that fish intestines form an important part of its ecological niche. These observations support a hypothesis that bioluminescence plays an ecological role in the marine food web. Despite our improved taxonomical resolution, we identify no geographical differences in bacterial community structure, indicating that the intestinal microbiome of these coastal cod is colonized by a limited number of closely related bacterial species with a broad geographical distribution that are well suited to thrive in this host-associated environment.

microbiology↗

The genome of the plague-resistant great gerbil reveals species-specific duplication of an MHCII gene

The great gerbil (Rhombomys opimus) is a social rodent living in permanent, complex burrow systems distributed throughout Central Asia, where it serves as the main host of several important vector-borne infectious diseases and is defined as a key reservoir species for plague (Yersinia pestis). Studies from the wild have shown that the great gerbil is largely resistant to plague but the genetic basis for resistance is yet to be determined. Here, we present a highly contiguous annotated genome assembly of great gerbil, covering over 96 % of the estimated 2.47 Gb genome. Comparative genomic analyses focusing on the immune gene repertoire, reveal shared gene losses within TLR gene families (i.e. TLR8, TLR10 and all members of TLR11-subfamily) for the Gerbillinae lineage, accompanied with signs of diversifying selection of TLR7 and TLR9. Most notably, we find a great gerbil-specific duplication of the MHCII DRB locus. In silico analyses suggest that the duplicated gene provides high peptide binding affinity for Yersiniae epitopes. The great gerbil genome provides new insights into the genomic landscape that confers immunological resistance towards plague. The high affinity for Yersinia epitopes could be key in our understanding of the high resistance in great gerbils, putatively conferring a faster initiation of the adaptive immune response leading to survival of the infection. Our study demonstrates the power of studying zoonosis in natural hosts through the generation of a genome resource for further comparative and experimental work on plague survival and evolution of host-pathogen interactions.

genomics↗

Evolutionary adaptability linked to length variation in short genic tandem repeats

Intrinsically disordered protein regions are of high importance for temperature sensing and immune responses in plants. Tracts of identical amino acids accumulate in these regions and can vary in length over generations due to expansions and retractions of short tandem repeats at the genomic level. However, little attention has been paid to what extent length variation is shaped by natural selection. By environmental association analysis on 2,514 length variable tracts in 770 whole-genome sequenced wild Arabidopsis thaliana we show that length variation in glutamine and asparagine amino acid homopolymers, as well as in interaction hotspots, correlate with local bio-climatic habitat. We determined experimentally that the promoter activity of a light-stress gene depended on polyglutamine length variants in a disordered transcription factor. Our results show that length variations impact protein function and are substantially shaped by natural selection. Length variants modulating protein function at a global genomic scale has implications for understanding protein evolution and eco-evolutionary biology.

evolutionary biology↗

Long-read sequence capture elucidates the evolution of the hemoglobin gene clusters in codfishes

Combining high-throughput sequencing with targeted sequence capture has become an attractive tool to study specific genomic regions of interest. Most studies have so far focused on the exome using short-read technology. These approaches are not designed to capture intergenic regions needed to reconstruct genomic organization, including regulatory regions and gene synteny. Here, we demonstrate the power of combining targeted sequence capture with long-read sequencing technology for comparative genomic analyses of the hemoglobin (Hb) gene clusters across eight species separated by up to 70 million years. Guided by the reference genome assembly of the Atlantic cod (Gadus morhua) together with genome information from draft assemblies of selected codfishes, we designed probes covering the two Hb gene clusters. Use of custom-made barcodes combined with PacBio RSII sequencing led to highly continuous assemblies of the LA (~100kb) and MN (~200kb) clusters, which include syntenic regions of coding and intergenic sequences. Our results revealed an overall conserved genetic organization and synteny of the Hb genes within this lineage, yet with several, lineage-specific gene duplications. Moreover, for some of the species examined, we identified amino acid substitutions at two sites in the Hbb1 gene as well as length polymorphisms in its regulatory region, which has previously been linked to temperature adaptation in Atlantic cod populations. This study highlights the use of targeted long-read capture as a versatile approach for comparative genomic studies by generation of a cross-species genomic resource elucidating the evolutionary history of the Hb gene family across the highly divergent group of codfishes.

genomics↗

A single Vibrionales 16S rRNA oligotype dominates the intestinal microbiome in two geographically separated Atlantic cod populations

BackgroundHost-microbe interactions are particularly intriguing in Atlantic cod (Gadus morhua), as it lacks the MHC II complex involved in presentation of extracellular pathogens. Nonetheless, little is known about the diversity of its microbiome in natural populations. Here, we use 16S rRNA high-throughput sequencing to investigate the microbial community composition in gut content and mucosa of 22 adult individuals from two coastal populations in Norway, located 470 km apart.\n\nResultsWe identify a core microbiome of 23 OTUs (97% sequence similarity) in all individuals that comprises 93% of the total number of reads. The most abundant orders are classified as Vibrionales, Fusobacteriales, Clostridiales and Bacteroidales. While mucosal samples show significantly lower diversity than gut content samples, no differences in OTU community composition are observed between the two populations. The differential abundance of oligotypes within two common OTUs does reveal limited spatial segregation. Remarkably, the most abundant OTU consists of a single oligotype (order Vibrionales, genus Photobacterium) that represents nearly 50% of the reads in both locations.\n\nConclusionsOur results show that the intestinal bacterial community of two geographically separated coastal populations of Atlantic cod is dominated by a limited number of highly abundant 16S rRNA oligotypes shared by all specimens examined. The ubiquity of these oligotypes suggests that the northern coastal Atlantic cod gut microbiome is colonized by a limited number of species with excellent dispersal capabilities that are well suited to thrive in their host environment.

microbiology↗

Genomic architecture of codfishes featured by expansions of innate immune genes and short tandem repeats

BackgroundIncreased availability of genome assemblies for non-model organisms has resulted in invaluable biological and genomic insight into numerous vertebrates including teleosts. The sequencing and assembly of the Atlantic cod (Gadus morhua) genome and the genomes of many of its relatives (Gadiformes) demonstrated a shared loss 100 million years ago of the major histocompatibility complex (MHC) II genes. The recent publication of an improved version of the Atlantic cod genome assembly reported an extreme density of tandem repeats compared to other vertebrate genome assemblies. Highly contiguous genome assemblies are needed to further investigate the unusual immune system of the Gadiformes, and the high density of tandem repeats in this group.\n\nResultsHere, we have sequenced and assembled the genome of haddock (Melanogrammus aeglefinus) - a relative of Atlantic cod - using a combination of PacBio and Illumina reads. Comparative analyses uncover that the haddock genome contains an even higher density of tandem repeats outside and within protein coding sequences than Atlantic cod. Further, both species show an elevated number of tandem repeats in genes mainly involved in signal transduction compared to other teleosts. An in-depth characterization of the immune gene repertoire demonstrates a substantial expansion of MCHI in Atlantic cod compared to haddock. In contrast, the Toll-like receptors show a similar pattern of gene losses and expansions. For another gene family associated with the innate immune system, the NOD-like receptors (NLRs), we find a large expansion common to all teleosts, with possible lineage-specific expansions in zebrafish, stickleback and the codfishes.\n\nConclusionsThe generation of a highly contiguous genome assembly of haddock revealed that the high density of short tandem repeats as well as expanded immune gene families is not unique to Atlantic cod - but most likely a feature common to all codfishes. A shared expansion of NLR genes in teleosts suggests that the NLRs have a more substantial role in the innate immunity of teleosts than other vertebrates. Moreover, we find that high copy number genes combined with variable genome assembly qualities may impede complete characterization, i.e. the number of NLRs might be underestimates in the different teleost species.

genomics↗