0000000001301362
AUTHOR
Kjetill S. Jakobsen
Evolutionary redesign of the Atlantic cod (Gadus morhua L.) Toll-like receptor repertoire by gene losses and expansions
AbstractGenome sequencing of the teleost Atlantic cod demonstrated loss of the Major Histocompatibility Complex (MHC) class II, an extreme gene expansion of MHC class I and gene expansions and losses in the innate pattern recognition receptor (PRR) family of Toll-like receptors (TLR). In a comparative genomic setting, using an improved version of the genome, we characterize PRRs in Atlantic cod with emphasis on TLRs demonstrating the loss of TLR1/6, TLR2 and TLR5 and expansion of TLR7, TLR8, TLR9, TLR22 and TLR25. We find that Atlantic cod TLR expansions are strongly influenced by diversifying selection likely to increase the detectable ligand repertoire through neo- and subfunctionalizatio…
Genomics of speciation and introgression in Princess cichlid fishes from Lake Tanganyika.
How variation in the genome translates into biological diversity and new species originate has endured as the mystery of mysteries in evolutionary biology. African cichlid fishes are prime model systems to address speciation-related questions for their remarkable taxonomic and phenotypic diversity, and the possible role of gene flow in this process. Here, we capitalize on genome sequencing and phylogenomic analyses to address the relative impacts of incomplete lineage sorting, introgression and hybrid speciation in the Neolamprologus savoryi-complex (the 'Princess cichlids') from Lake Tanganyika. We present a time-calibrated species tree based on whole-genome sequences and provide strong ev…
Tandem repeats lead to sequence assembly errors and impose multi-level challenges for genome and protein databases
AbstractThe widespread occurrence of repetitive stretches of DNA in genomes of organisms across the tree of life imposes fundamental challenges for sequencing, genome assembly, and automated annotation of genes and proteins. This multi-level problem can lead to errors in genome and protein databases that are often not recognized or acknowledged. As a consequence, end users working with sequences with repetitive regions are faced with ‘ready-to-use’ deposited data whose trustworthiness is difficult to determine, let alone to quantify. Here, we provide a review of the problems associated with tandem repeat sequences that originate from different stages during the sequencing-assembly-annotatio…
Three chromosomal rearrangements promote genomic divergence between migratory and stationary ecotypes of Atlantic cod
AbstractIdentification of genome-wide patterns of divergence provides insight on how genomes are influenced by selection and can reveal the potential for local adaptation in spatially structured populations. In Atlantic cod – historically a major marine resource – Northeast-Arctic- and Norwegian coastal cod are recognized by fundamental differences in migratory and non-migratory behavior, respectively. However, the genomic architecture underlying such behavioral ecotypes is unclear. Here, we have analyzed more than 8.000 polymorphic SNPs distributed throughout all 23 linkage groups and show that loci putatively under selection are localized within three distinct genomic regions, each of sev…
Disentangling structural genomic and behavioural barriers in a sea of connectivity
18 pages, 4 tables, 3 figures.-- This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited
An improved version of the Atlantic cod genome and advancements in functional genomics: implications for the future of cod farming
Abstract Recent advancements within state-of-the-art genomic tools and the generation of the first version of the Atlantic cod genome (Star et al., 2011) have proven to be valuable resources, improving our understanding of this species’ biology. In this chapter we describe some aspects and implications of using these resources to identify genes and molecular pathways involved in Atlantic cod growth and development, as well as responses to nutritional changes, pathogens and other immune stimuli, and environmental stressors (e.g., temperature, stress, or pollutants). Additionally, we highlight the immunological puzzle of the Atlantic cod that lacks components of the adaptive immune system pre…
The era of reference genomes in conservation genomics
Progress in genome sequencing now enables the large-scale generation of reference genomes. Various international initiatives aim to generate reference genomes representing global biodiversity. These genomes provide unique insights into genomic diversity and architecture, thereby enabling comprehensive analyses of population and functional genomics, and are expected to revolutionize conservation genomics.
The new era of genome sequencing using high-throughput sequencing technology: generation of the first version of the Atlantic cod genome
Abstract The genome of Atlantic cod (Gadus morhua L.) published in 2011 was the first example of a teleost genome obtained using a pure high-throughput sequencing (HTS) technology strategy, and the first large vertebrate genome generated by exclusively using Roche/454 sequencing technology. At the start of the sequencing project in 2009, two HTS technologies were available, the Roche/454 and Illumina technologies. Because of the longer read length of the Roche/454 technology and a wider range of suitable software utilizing those data at the time, we chose to use this technology for the first version of the Atlantic cod genome. In this chapter, we describe the process leading to the assembly…
Whole genome sequencing data and de novo draft assemblies for 66 teleost species
Teleost fishes comprise more than half of all vertebrate species, yet genomic data are only available for 0.2% of their diversity. Here, we present whole genome sequencing data for 66 new species of teleosts, vastly expanding the availability of genomic data for this important vertebrate group. We report on de novo assemblies based on low-coverage (9–39×) sequencing and present detailed methodology for all analyses. To facilitate further utilization of this data set, we present statistical analyses of the gene space completeness and verify the expected phylogenetic position of the sequenced genomes in a large mitogenomic context. We further present a nuclear marker set used for phylogenetic…
Ancient DNA reveals the Arctic origin of Viking Age cod from Haithabu, Germany
Knowledge of the range and chronology of historic trade and long-distance transport of natural resources is essential for determining the impacts of past human activities on marine environments. However, the specific biological sources of imported fauna are often difficult to identify, in particular if species have a wide spatial distribution and lack clear osteological or isotopic differentiation between populations. Here, we report that ancient fish-bone remains, despite being porous, brittle, and light, provide an excellent source of endogenous DNA (15-46%) of sufficient quality for whole-genome reconstruction. By comparing ancient sequence data to that of modern specimens, we determine …
Successive Losses of Central Immune Genes Characterize the Gadiformes' Alternate Immunity.
Great genetic variability among teleost immunomes, with gene losses and expansions of central adaptive and innate components, has been discovered through genome sequencing over the last few years. Here, we demonstrate that the innate Myxovirus resistance gene (Mx) is lost from the ancestor of Gadiformes and the closely related Stylephorus chordatus, thus predating the loss of Major Histocompatibility Complex class II (MHCII) in Gadiformes. Although the functional implication of Mx loss is still unknown, we demonstrate that this loss is one of several ancient events appearing in successive order throughout the evolution of teleost immunity. In particular, we find that the loss of Toll-like r…
Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic
Significance Both theory and experiments suggest that fishing can drive the evolution of an earlier maturation age. However, determining whether changes in the wild are the result of fisheries-induced evolution has been difficult. Temporal, genome-wide datasets can directly reveal responses to selection. Here, we investigate the genomes of two wild Atlantic cod populations from samples that pre- and postdate periods of intensive fishing. Although phenotypic changes suggest fisheries-induced evolution, we do not find evidence for any strong genomic change or loss of genetic diversity. While evolution could have occurred through undetectable frequency changes at many loci, the irreversible lo…
Genomic characterization of the Atlantic cod sex-locus
AbstractA variety of sex determination mechanisms can be observed in evolutionary divergent teleosts. Sex determination is genetic in Atlantic cod (Gadus morhua), however the genomic location or size of its sex-locus is unknown. Here, we characterize the sex-locus of Atlantic cod using whole genome sequence (WGS) data of 227 wild-caught specimens. Analyzing more than 55 million polymorphic loci, we identify 166 loci that are associated with sex. These loci are located in six distinct regions on five different linkage groups (LG) in the genome. The largest of these regions, an approximately 55 Kb region on LG11, contains the majority of genotypes that segregate closely according to a XX-XY s…
Trans-oceanic genomic divergence of Atlantic cod ecotypes is associated with large inversions
Chromosomal rearrangements such as inversions can play a crucial role in maintaining polymorphism underlying complex traits and contribute to the process of speciation. In Atlantic cod (Gadus morhua), inversions of several megabases have been identified that dominate genomic differentiation between migratory and nonmigratory ecotypes in the Northeast Atlantic. Here, we show that the same genomic regions display elevated divergence and contribute to ecotype divergence in the Northwest Atlantic as well. The occurrence of these inversions on both sides of the Atlantic Ocean reveals a common evolutionary origin, predating the >100 000-year-old trans-Atlantic separation of Atlantic cod. The long…
Evolution of the immune system influences speciation rates in teleost fishes.
Teleost fishes constitute the most species-rich vertebrate clade and exhibit extensive genetic and phenotypic variation, including diverse immune defense strategies. The genomic basis of a particularly aberrant strategy is exemplified by Atlantic cod, in which a loss of major histocompatibility complex (MHC) II functionality coincides with a marked expansion of MHC I genes. Through low-coverage genome sequencing (9–39×), assembly and comparative analyses for 66 teleost species, we show here that MHC II is missing in the entire Gadiformes lineage and thus was lost once in their common ancestor. In contrast, we find that MHC I gene expansions have occurred multiple times, both inside and outs…
Linking species habitat and past palaeoclimatic events to evolution of the teleost innate immune system
Host-intrinsic factors as well as environmental changes are known to be strong evolutionary drivers defining the genetic foundation of immunity. Using a novel set of teleost genomes and a time-calibrated phylogeny, we here investigate the family of Toll-like receptor ( TLR ) genes and address the underlying evolutionary processes shaping the diversity of the first-line defence. Our findings reveal remarkable flexibility within the evolutionary design of teleost innate immunity characterized by prominent TLR gene losses and expansions. In the order of Gadiformes, expansions correlate with the loss of major histocompatibility complex class II ( MHCII ) and diversifying selection analyses sup…
An improved genome assembly uncovers prolific tandem repeats in Atlantic cod
AbstractBackground: The first Atlantic cod (Gadus morhua) genome assembly published in 2011 was one of the early genome assemblies exclusively based on high-throughput 454 pyrosequencing. Since then, rapid advances in sequencing technologies have led to a multitude of assemblies generated for complex genomes, although many of these are of a fragmented nature with a significant fraction of bases in gaps. The development of long-read sequencing and improved software now enable the generation of more contiguous genome assemblies.Results: By combining data from Illumina, 454 and the longer PacBio sequencing technologies, as well as integrating the results of multiple assembly programs, we have …
Evolution of Hemoglobin Genes in Codfishes Influenced by Ocean Depth
AbstractUnderstanding the genetic basis of adaptation is one of the main enigmas of evolutionary biology. Among vertebrates, hemoglobin has been well documented as a key trait for adaptation to different environments. Here, we investigate the role of hemoglobins in adaptation to ocean depth in the diverse teleost order Gadiformes, with species distributed at a wide range of depths varying in temperature, hydrostatic pressure and oxygen levels. Using genomic data we characterized the full hemoglobin (Hb) gene repertoire for subset of species within this lineage. We discovered a correlation between expanded numbers of Hb genes and ocean depth, with the highest numbers in species occupying sha…
Data from: Genomics of speciation and introgression in Princess cichlid fishes from Lake Tanganyika
How variation in the genome translates into biological diversity and new species originate has endured as the mystery of mysteries in evolutionary biology. African cichlid fishes are prime model systems to address speciation-related questions for their remarkable taxonomic and phenotypic diversity, and the possible role of gene flow in this process. Here, we capitalize on genome sequencing and phylogenomic analyses to address the relative impacts of incomplete lineage sorting, introgression and hybrid speciation in the Neolamprologus savoryi-complex (the ‘Princess cichlids’) from Lake Tanganyika. We present a time-calibrated species tree based on whole-genome sequences and provide strong ev…
Data from: Ancient DNA reveals the Arctic origin of Viking Age cod from Haithabu, Germany
Knowledge of the range and chronology of historic trade and long-distance transport of natural resources is essential for determining the impacts of past human activities on marine environments. However, the specific biological sources of imported fauna are often difficult to identify, in particular if species have a wide spatial distribution and lack clear osteological or isotopic differentiation between populations. Here, we report that ancient fish-bone remains, despite being porous, brittle, and light, provide an excellent source of endogenous DNA (15–46%) of sufficient quality for whole-genome reconstruction. By comparing ancient sequence data to that of modern specimens, we determine …
Data from: Disentangling structural genomic and behavioral barriers in a sea of connectivity
Genetic divergence among populations arises through natural selection or drift and is counteracted by connectivity and gene flow. In sympatric populations, isolating mechanisms are thus needed to limit the homogenizing effects of gene flow to allow for adaptation and speciation. Chromosomal inversions act as an important mechanism maintaining isolating barriers, yet their role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question whether inversions play a role in the divergence of connected populations of the marine fish Atlantic cod, by exploring a unique dataset combining whole-genome sequencing data and behavioral data obtained w…
Data from: Genome architecture enables local adaptation of Atlantic cod despite high connectivity
Adaptation to local conditions is a fundamental process in evolution; however, mechanisms maintaining local adaptation despite high gene flow are still poorly understood. Marine ecosystems provide a wide array of diverse habitats that frequently promote ecological adaptation even in species characterized by strong levels of gene flow. As one example, populations of the marine fish Atlantic cod (Gadus morhua) are highly connected due to immense dispersal capabilities but nevertheless show local adaptation in several key traits. By combining population genomic analyses based on 12K single nucleotide polymorphisms with larval dispersal patterns inferred using a biophysical ocean model, we show…
Data from: Trans-oceanic genomic divergence of Atlantic cod ecotypes is associated with large inversions
Chromosomal rearrangements such as inversions can play a crucial role in maintaining polymorphism underlying complex traits and contribute to the process of speciation. In Atlantic cod (Gadus morhua), inversions of several megabases have been identified that dominate genomic differentiation between migratory and non-migratory ecotypes in the Northeast Atlantic. Here, we show that the same genomic regions display elevated divergence and contribute to ecotype divergence in the Northwest Atlantic as well. The occurrence of these inversions on both sides of the Atlantic Ocean reveals a common evolutionary origin, predating the more than 100,000 years old trans-Atlantic separation of Atlantic co…
Data from: Evolution of the immune system influences speciation rates in teleost fishes
Teleost fishes constitute the most species-rich vertebrate clade and exhibit extensive genetic and phenotypic variation, including diverse immune defense strategies. The genomic basis of a particularly aberrant strategy is exemplified by Atlantic cod, in which a loss of major histocompatibility complex (MHC) II functionality coincides with a marked expansion of MHC I genes. Through low-coverage genome sequencing (9–39×), assembly and comparative analyses for 66 teleost species, we show here that MHC II is missing in the entire Gadiformes lineage and thus was lost once in their common ancestor. In contrast, we find that MHC I gene expansions have occurred multiple times, both inside and outs…