Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes

A fundamental problem for the evolution of pregnancy, the most specialized form of parental investment among vertebrates, is the rejection of the nonself-embryo. Mammals achieve immunological tolerance by down-regulating both major histocompatibility complex pathways (MHC I and II). Although pregnancy has evolved multiple times independently among vertebrates, knowledge of associated immune system adjustments is restricted to mammals. All of them (except monotremata) display full internal pregnancy, making evolutionary reconstructions within the class mammalia meaningless. Here, we study the seahorse and pipefish family (syngnathids) that have evolved male pregnancy across a gradient from external oviparity to internal gestation. We assess how immunological tolerance is achieved by reconstruction of the immune gene repertoire in a comprehensive sample of 12 seahorse and pipefish genomes along the “male pregnancy” gradient together with expression patterns of key immune and pregnancy genes in reproductive tissues. We found that the evolution of pregnancy coincided with a modification of the adaptive immune system. Divergent genomic rearrangements of the MHC II pathway among fully pregnant species were identified in both genera of the syngnathids: The pipefishes (Syngnathus) displayed loss of several genes of the MHC II pathway while seahorses (Hippocampus) featured a highly divergent invariant chain (CD74). Our findings suggest that a trade-off between immunological tolerance and embryo rejection accompanied the evolution of unique male pregnancy. That pipefishes survive in an ocean of microbes without one arm of the adaptive immune defense suggests a high degree of immunological flexibility among vertebrates, which may advance our understanding of immune-deficiency diseases

Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic

The mode and extent of rapid evolution and genomic change in response to human harvesting are key conservation issues. Although experiments and models have shown a high potential for both genetic and phenotypic change in response to fishing, empirical examples of genetic responses in wild populations are rare. Here, we compare whole-genome sequence data of Atlantic cod (Gadus morhua) that were collected before (early 20th century) and after (early 21st century) periods of intensive exploitation and rapid decline in the age of maturation from two geographically distinct populations in Newfoundland, Canada, and the northeast Arctic, Norway. Our temporal, genome-wide analyses of 346,290 loci show no substantial loss of genetic diversity and high effective population sizes. Moreover, we do not find distinct signals of strong selective sweeps anywhere in the genome, although we cannot rule out the possibility of highly polygenic evolution. Our observations suggest that phenotypic change in these populations is not constrained by irreversible loss of genomic variation and thus imply that former traits could be reestablished with demographic recovery.publishedVersio

An evaluation of the role of adaptation in salmon evolution using genome based approaches

Thesis (Ph.D.)--University of Washington, 2013Studying the results of selection may provide insights into the extent of adaptation, processes affecting population divergence, and gene diversity. Here, the role of adaptation in salmon evolution was evaluated at different taxonomic levels using genome based approaches. The first part of this thesis was aimed at developing a bioinformatic methodology to detect genes under selection on a large scale in non-model species. In such species, coding sequences can be incomplete because of limited genomic resources. However, these sequences are information rich, and can be used to estimate neutral versus non neutral divergence across species. Incomplete DNA sequences can complicate estimates of non-neutral divergence based on comparisons between synonymous (dS) and non-synonymous (dN) nucleotide substitutions, commonly used to study selection between species. The first chapter describes a series of steps that can be used to examine positive selection on a large scale between non model species using partial sequences. The methodology is described for six species of salmonids, where approaches are complicated by the fact that a whole duplication event occurred in the lineage leading to these species. Therefore, challenges associated with duplicated genomes, specifically the separation of orthologs from paralogs, were also addressed. We found that multi-way BLAST optimized the number of alignments between partial coding sequences. We recommend that reading frames should be manually detected after alignment with sequences in Genbank using the BLASTX program. Finally, phylogenetic approaches were determined to be suitable to separate orthologs from paralogs in duplicated genomes. The second part of the thesis was aimed at conducting a genome-wide assessment of the role of adaptive evolution of Chinook salmon in the Columbia River in the Pacific Northwest of the USA. The first step involved the construction of a dense linkage map for Chinook salmon, thus providing the necessary resources for a genome-wide analysis in wild populations (Chapter 2). We mapped 7146 RAD loci on the 34 chromosomes of Chinook salmon, spanning 4163cM. All the chromosome arms were identified through centromere mapping. Placement of 799 duplicated loci revealed that they were preferentially distributed on distal regions of eight pairs of chromosome arms. This result suggests that homeologs diverged at different rates following whole genome duplication. Our results supported near complete interference during recombination for Chinook salmon, and confirmed previously identified homologies between Chinook salmon and rainbow trout. In the third chapter, we aimed to determine the role of adaptive divergence in the evolution of Chinook salmon in the Columbia River Basin. A population survey of divergence was conducted using 14105 RAD markers in eleven populations in the Columbia River Basin, representative of the three main lineages identified in previous studies. Our results supported the hypothesis of colonization of the Columbia River Basin from two main refugia following the last glaciation event. We identified 301 outlier loci that did not conform to neutral evolution, consistent with adaptive divergence. Of these, 148 and 153 were associated with the pre- and post- glaciation divergence respectively. Using the linkage map created in the second chapter, we identified chromosomal regions of high divergence, most of which were located in distal regions from the centromere. Although some regions of elevated divergence were observed in common between lineages, many appeared to be specific to pre- or post-glaciation divergence. Finally we investigated whether we could find molecular evidence supporting observations of parallel evolution in a phenotypic trait across populations, adult return timing. Random forest analyses, a regression-based approach, detected some loci that predicted run timing, specifically Spring and Fall return timing, two of which mapped to the same position on the linkage map. In this chapter, beyond improving our understanding of Chinook salmon evolution, we have demonstrated the usefulness of dense linkage maps in identifying regions of the genome that may have been involved in adaptive evolution. The research presented in this thesis will facilitate the study of adaptive divergence between non-model species. Novel and extensive genomic resources for Chinook salmon have also been developed. These resources have provided insights into chromosome evolution following whole genome duplication, and have greatly contributed to the understanding of adaptive evolution of populations of Chinook salmon in the Columbia River Basin

Evidence of hybridization between genetically distinct Baltic cod stocks during peak population abundance(s)

Abstract Range expansions can lead to increased contact of divergent populations, thus increasing the potential of hybridization events. Whether viable hybrids are produced will most likely depend on the level of genomic divergence and associated genomic incompatibilities between the different entities as well as environmental conditions. By taking advantage of historical Baltic cod (Gadus morhua) otolith samples combined with genotyping and whole genome sequencing, we here investigate the genetic impact of the increased spawning stock biomass of the eastern Baltic cod stock in the mid 1980s. The eastern Baltic cod is genetically highly differentiated from the adjacent western Baltic cod and locally adapted to the brackish environmental conditions in the deeper Eastern basins of the Baltic Sea unsuitable for its marine counterparts. Our genotyping results show an increased proportion of eastern Baltic cod in western Baltic areas (Mecklenburg Bay and Arkona Basin)—indicative of a range expansion westwards—during the peak population abundance in the 1980s. Additionally, we detect high frequencies of potential hybrids (including F1, F2 and backcrosses), verified by whole genome sequencing data for a subset of individuals. Analysis of mitochondrial genomes further indicates directional gene flow from eastern Baltic cod males to western Baltic cod females. Our findings unravel that increased overlap in distribution can promote hybridization between highly divergent populations and that the hybrids can be viable and survive under specific and favourable environmental conditions. However, the observed hybridization had seemingly no long‐lasting impact on the continuous separation and genetic differentiation between the unique Baltic cod stocks

Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes

A fundamental problem for the evolution of pregnancy, the most specialized form of parental investment among vertebrates, is the rejection of the nonself-embryo. Mammals achieve immunological tolerance by down-regulating both major histocompatibility complex pathways (MHC I and II). Although pregnancy has evolved multiple times independently among vertebrates, knowledge of associated immune system adjustments is restricted to mammals. All of them (except monotremata) display full internal pregnancy, making evolutionary reconstructions within the class mammalia meaningless. Here, we study the seahorse and pipefish family (syngnathids) that have evolved male pregnancy across a gradient from external oviparity to internal gestation. We assess how immunological tolerance is achieved by reconstruction of the immune gene repertoire in a comprehensive sample of 12 seahorse and pipefish genomes along the “male pregnancy” gradient together with expression patterns of key immune and pregnancy genes in reproductive tissues. We found that the evolution of pregnancy coincided with a modification of the adaptive immune system. Divergent genomic rearrangements of the MHC II pathway among fully pregnant species were identified in both genera of the syngnathids: The pipefishes (Syngnathus) displayed loss of several genes of the MHC II pathway while seahorses (Hippocampus) featured a highly divergent invariant chain (CD74). Our findings suggest that a trade-off between immunological tolerance and embryo rejection accompanied the evolution of unique male pregnancy. That pipefishes survive in an ocean of microbes without one arm of the adaptive immune defense suggests a high degree of immunological flexibility among vertebrates, which may advance our understanding of immune-deficiency diseases

Current status and potential of genomic selection to improve selective breeding in the main aquaculture species of International Council for the Exploration of the Sea (ICES) member countries

Selective breeding has been successfully applied to improve profitability and sustainability in numerous aquatic species. Recent developments of high throughput genotyping technology now enable the implementation of genomic selection, a method aiming to predict the breeding value of candidates based on their genotype at genome-wide markers. In this review article, we review the state of the arts, challenges and prospects for the application of genomic selection in aquaculture species. The particular focus is on the status of genomic selection in several major aquaculture species of International Council for the Exploration of the Sea (ICES) member countries: Atlantic salmon, rainbow trout, Atlantic cod, American catfish, Pacific oyster, European sea bass and gilthead sea bream. While the potential of genomic selection is clear, tailored species-specific applications will be needed to maximise its benefit for the aquaculture sector

Current status and potential of genomic selection to improve selective breeding in the main aquaculture species of International Council for the Exploration of the Sea (ICES) member countries

Selective breeding has been successfully applied to improve profitability and sustainability in numerous aquatic species. Recent developments of high throughput genotyping technology now enable the implementation of genomic selection, a method aiming to predict the breeding value of candidates based on their genotype at genome-wide markers. In this review article, we review the state of the arts, challenges and prospects for the application of genomic selection in aquaculture species. The particular focus is on the status of genomic selection in several major aquaculture species of International Council for the Exploration of the Sea (ICES) member countries: Atlantic salmon, rainbow trout, Atlantic cod, American catfish, Pacific oyster, European sea bass and gilthead sea bream. While the potential of genomic selection is clear, tailored species-specific applications will be needed to maximise its benefit for the aquaculture sector

Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic

The mode and extent of rapid evolution and genomic change in response to human harvesting are key conservation issues. Although experiments and models have shown a high potential for both genetic and phenotypic change in response to fishing, empirical examples of genetic responses in wild populations are rare. Here, we compare whole-genome sequence data of Atlantic cod (Gadus morhua) that were collected before (early 20th century) and after (early 21st century) periods of intensive exploitation and rapid decline in the age of maturation from two geographically distinct populations in Newfoundland, Canada, and the northeast Arctic, Norway. Our temporal, genome-wide analyses of 346,290 loci show no substantial loss of genetic diversity and high effective population sizes. Moreover, we do not find distinct signals of strong selective sweeps anywhere in the genome, although we cannot rule out the possibility of highly polygenic evolution. Our observations suggest that phenotypic change in these populations is not constrained by irreversible loss of genomic variation and thus imply that former traits could be reestablished with demographic recovery

Historical demographic processes dominate genetic variation in ancient Atlantic cod mitogenomes

Ancient DNA (aDNA) approaches have been successfully used to infer the long-term impacts of climate change, domestication, and human exploitation in a range of terrestrial species. Nonetheless, studies investigating such impacts using aDNA in marine species are rare. Atlantic cod (Gadus morhua), is an economically important species that has experienced dramatic census population declines during the last century. Here, we investigated 48 ancient mitogenomes from historical specimens obtained from a range of archeological excavations in northern Europe dated up to 6,500 BCE. We compare these mitogenomes to those of 496 modern conspecifics sampled across the North Atlantic Ocean and adjacent seas. Our results confirm earlier observations of high levels of mitogenomic variation and a lack of mutation-drift equilibrium—suggestive of population expansion. Furthermore, our temporal comparison yields no evidence of measurable mitogenomic changes through time. Instead, our results indicate that mitogenomic variation in Atlantic cod reflects past demographic processes driven by major historical events (such as oscillations in sea level) and subsequent gene flow rather than contemporary fluctuations in stock abundance. Our results indicate that historical and contemporaneous anthropogenic pressures such as commercial fisheries have had little impact on mitogenomic diversity in a wide-spread marine species with high gene flow such as Atlantic cod. These observations do not contradict evidence that overfishing has had negative consequences for the abundance of Atlantic cod and the importance of genetic variation in implementing conservation strategies. Instead, these observations imply that any measures toward the demographic recovery of Atlantic cod in the eastern Atlantic, will not be constrained by recent loss of historical mitogenomic variation

Sex-dependent dominance maintains migration supergene in rainbow trout

publishedVersio