Bastiaan Star

The genome sequence of Atlantic cod reveals a unique immune system

Atlantic cod (Gadus morhua) is a large, cold-adapted teleost that sustains long-standing commercial fisheries and incipient aquaculture. Here we present the genome sequence of Atlantic cod, showing evidence for complex thermal adaptations in its haemoglobin gene cluster and an unusual immune architecture compared to other sequenced vertebrates. The genome assembly was obtained exclusively by 454 sequencing of shotgun and paired-end libraries, and automated annotation identified 22,154 genes. The major histocompatibility complex (MHC) II is a conserved feature of the adaptive immune system of jawed vertebrates, but we show that Atlantic cod has lost the genes for MHC II, CD4 and invariant chain (Ii) that are essential for the function of this pathway. Nevertheless, Atlantic cod is not exceptionally susceptible to disease under natural conditions. We find a highly expanded number of MHC I genes and a unique composition of its Toll-like receptor (TLR) families. This indicates how the Atlantic cod immune system has evolved compensatory mechanisms in both adaptive and innate immunity in the absence of MHC II. These observations affect fundamental assumptions about the evolution of the adaptive immune system and its components in vertebrates.

Adaptation to Low Salinity Promotes Genomic Divergence in Atlantic Cod (Gadus morhua L.)

How genomic selection enables species to adapt to divergent environments is a fundamental question in ecology and evolution. We investigated the genomic signatures of local adaptation in Atlantic cod (Gadus morhua L.) along a natural salinity gradient, ranging from 35‰ in the North Sea to 7‰ within the Baltic Sea. By utilizing a 12 K SNPchip, we simultaneously assessed neutral and adaptive genetic divergence across the Atlantic cod genome. Combining outlier analyses with a landscape genomic approach, we identified a set of directionally selected loci that are strongly correlated with habitat differences in salinity, oxygen, and temperature. Our results show that discrete regions within the Atlantic cod genome are subject to directional selection and associated with adaptation to the local environmental conditions in the Baltic- and the North Sea, indicating divergence hitchhiking and the presence of genomic islands of divergence. We report a suite of outlier single nucleotide polymorphisms within or closely located to genes associated with osmoregulation, as well as genes known to play important roles in the hydration and development of oocytes. These genes are likely to have key functions within a general osmoregulatory framework and are important for the survival of eggs and larvae, contributing to the buildup of reproductive isolation between the low-salinity adapted Baltic cod and the adjacent cod populations. Hence, our data suggest that adaptive responses to the environmental conditions in the Baltic Sea may contribute to a strong and effective reproductive barrier, and that Baltic cod can be viewed as an example of ongoing speciation.

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 outside this clade. Moreover, we identify an association between high MHC I copy number and elevated speciation rates using trait-dependent diversification models. Our results extend current understanding of the plasticity of the adaptive immune system and suggest an important role for immune-related genes in animal diversification.

Next generation sequencing shows high variation of the intestinal microbial species composition in Atlantic cod caught at a single location

BackgroundThe observation that specific members of the microbial intestinal community can be shared among vertebrate hosts has promoted the concept of a core microbiota whose composition is determined by host-specific selection. Most studies investigating this concept in individual hosts have focused on mammals, yet the diversity of fish lineages provides unique comparative opportunities from an evolutionary, immunological and environmental perspective. Here we describe microbial intestinal communities of eleven individual Atlantic cod (Gadus morhua) caught at a single location based on an extensively 454 sequenced 16S rRNA library of the V3 region.ResultsWe obtained a total of 280447 sequences and identify 573 Operational Taxonomic Units (OTUs) at 97% sequence similarity level, ranging from 40 to 228 OTUs per individual. We find that ten OTUs are shared, though the number of reads of these OTUs is highly variable. This variation is further illustrated by community diversity estimates that fluctuate several orders of magnitude among specimens. The shared OTUs belong to the orders of Vibrionales, which quantitatively dominate the Atlantic cod intestinal microbiota, followed by variable numbers of Bacteroidales, Erysipelotrichales, Clostridiales, Alteromonadales and Deferribacterales.ConclusionsThe microbial intestinal community composition varies significantly in individual Atlantic cod specimens caught at a single location. This high variation among specimens suggests that a complex combination of factors influence the species distribution of these intestinal communities.

Multilocus assignment analyses reveal multiple units and rare migration events in the recently expanded yellow-eyed penguin (Megadyptes antipodes).

The identification of demographically independent populations and the recognition of management units have been greatly facilitated by the continuing advances in genetic tools. Managements units now play a key role in short‐term conservation management programmes of declining species, but their importance in expanding populations receives comparatively little attention. The endangered yellow‐eyed penguin (Megadyptes antipodes) expanded its range from the subantarctic to New Zealands South Island a few hundred years ago and this new population now represents almost half of the species’ total census size. This dramatic expansion attests to M. antipodes’ high dispersal abilities and suggests the species is likely to constitute a single demographic population. Here we test this hypothesis of panmixia by investigating genetic differentiation and levels of gene flow among penguin breeding areas using 12 autosomal microsatellite loci along with mitochondrial control region sequence analyses for 350 individuals. Contrary to our hypothesis, however, the analyses reveal two genetically and geographically distinct assemblages: South Island vs. subantarctic populations. Using assignment tests, we recognize just two first‐generation migrants between these populations (corresponding to a migration rate of < 2%), indicating that ongoing levels of long‐distance migration are low. Furthermore, the South Island population has low genetic variability compared to the subantarctic population. These results suggest that the South Island population was founded by only a small number of individuals, and that subsequent levels of gene flow have remained low. The demographic independence of the two populations warrants their designation as distinct management units and conservation efforts should be adjusted accordingly to protect both populations.

Three chromosomal rearrangements promote genomic divergence between migratory and stationary ecotypes of Atlantic cod

Identification 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 several megabases long, covering approximately 4% of the Atlantic cod genome. These regions likely represent genomic inversions. The frequency of these distinct regions differ markedly between the ecotypes, spawning in the vicinity of each other, which contrasts with the low level of divergence in the rest of the genome. The observed patterns strongly suggest that these chromosomal rearrangements are instrumental in local adaptation and separation of Atlantic cod populations, leaving footprints of large genomic regions under selection. Our findings demonstrate the power of using genomic information in further understanding the population dynamics and defining management units in one of the world’s most economically important marine resources.

An improved genome assembly uncovers prolific tandem repeats in Atlantic cod

BackgroundThe 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.ResultsBy combining data from Illumina, 454 and the longer PacBio sequencing technologies, as well as integrating the results of multiple assembly programs, we have created a substantially improved version of the Atlantic cod genome assembly. The sequence contiguity of this assembly is increased fifty-fold and the proportion of gap-bases has been reduced fifteen-fold. Compared to other vertebrates, the assembly contains an unusual high density of tandem repeats (TRs). Indeed, retrospective analyses reveal that gaps in the first genome assembly were largely associated with these TRs. We show that 21% of the TRs across the assembly, 19% in the promoter regions and 12% in the coding sequences are heterozygous in the sequenced individual.ConclusionsThe inclusion of PacBio reads combined with the use of multiple assembly programs drastically improved the Atlantic cod genome assembly by successfully resolving long TRs. The high frequency of heterozygous TRs within or in the vicinity of genes in the genome indicate a considerable standing genomic variation in Atlantic cod populations, which is likely of evolutionary importance.

Why does the immune system of Atlantic cod lack MHC II

MHC II, a major feature of the adaptive immune system, is lacking in Atlantic cod, and there are different scenarios (metabolic cost hypothesis or functional shift hypothesis) that might explain this loss. The lack of MHC II coincides with an increased number of genes for MHC I and Toll-like receptors (TLRs).

Lost in translation or deliberate falsification? Genetic analyses reveal erroneous museum data for historic penguin specimens.

Historic museum specimens are increasingly used to answer a wide variety of questions in scientific research. Nevertheless, the scientific value of these specimens depends on the authenticity of the data associated with them. Here we use individual-based genetic analyses to demonstrate erroneous locality information for archive specimens from the late nineteenth century. Specifically, using 10 microsatellite markers, we analysed 350 contemporary and 43 historic yellow-eyed penguin (Megadyptes antipodes) specimens from New Zealands South Island and sub-Antarctic regions. Factorial correspondence analysis and an assignment test strongly suggest that eight of the historic specimens purportedly of sub-Antarctic origin were in fact collected from the South Island. Interestingly, all eight specimens were obtained by the same collector, and all are currently held in the same museum collection. Further inspection of the specimen labels and evaluation of sub-Antarctic voyages did not reveal whether the erroneous data are caused by incorrect labelling or whether deliberate falsification was at play. This study highlights a promising extension to the well-known applications of assignment tests in molecular ecology, which can complement methods that are currently being applied for error detection in specimen data. Our results also serve as a warning to all who use archive specimens to invest time in the verification of collection information.

Single-Locus Polymorphism in a Heterogeneous Two-Deme Model

Environmental heterogeneity has long been considered a likely explanation for the high levels of genetic variation found in most natural populations: selection in a spatially heterogeneous environment can maintain more variation. While this theoretical result has been extensively studied in models with limited parameters (e.g., two alleles, fixed gene flow, and particular selection schemes), the effect of spatial heterogeneity is poorly understood for models with a wider range of parameters (e.g., multiple alleles, different levels of gene flow, and more general selection schemes). We have compared the volume of fitness space that maintains variation in a single-deme model to the volume in a two-deme model for multiple alleles, random selection schemes, and various levels of migration. Furthermore, equilibrium allele-frequency vectors were examined to see if particular patterns of variation are more prevalent than first expected. The two-deme model maintains variation for substantially larger volumes of fitness space with lower heterozygote fitness than the single-deme model. This result implies that selection schemes in the two-deme model can have a wider range of fitness patterns while still maintaining variation. The equilibrium allele-frequency patterns emerging from the two-deme model are more variable and strongly influenced by gene flow.