The origin and remolding of genomic islands of differentiation in the European sea bass

Duranton, Maud; Allal, François; Fraïssé, Christelle; Bierne, Nicolas; Bonhomme, François; Gagnaire, Pierre‐Alexandre

doi:10.1038/s41467-018-04963-6

Cited by 112 publications

(221 citation statements)

References 77 publications

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“…It is not clear whether differential timing of spawning evolved in allopatry (allowing for multiple allele control) or in sympatry (favouring a one‐allele mechanism) but follow‐up studies using higher coverage genomes should investigate the history of these populations. Secondary contact, producing similar patterns of heterogeneous differentiation throughout the genome, has been documented in other marine species (e.g., European sea bass, Duranton et al, ; European anchovies, Le Moan, Gagnaire, & Bonhomme, ) and could have occurred between spring‐ and winter‐spawning cod that evolved in allopatry.…”

Section: Discussionsupporting

confidence: 52%

Novel signals of adaptive genetic variation in northwestern Atlantic cod revealed by whole‐genome sequencing

Clucas

Lou

Therkildsen

et al. 2019

Evolutionary Applications

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Selection can create complex patterns of adaptive differentiation among populations in the wild that may be relevant to management. Atlantic cod in the Northwest Atlantic are at a fraction of their historical abundance and a lack of recovery within the Gulf of Maine has created concern regarding the misalignment of fisheries management structures with biological population structure. To address this and investigate genome‐wide patterns of variation, we used low‐coverage sequencing to perform a region‐wide, whole‐genome analysis of fine‐scale population structure. We sequenced 306 individuals from 20 sampling locations in U.S. and Canadian waters, including the major spawning aggregations in the Gulf of Maine in addition to spawning aggregations from Georges Bank, southern New England, the eastern Scotian Shelf, and St. Pierre Bank. With genotype likelihoods estimated at almost 11 million loci, we found large differences in haplotype frequencies of previously described chromosomal inversions between Canadian and U.S. sampling locations and also among U.S. sampling locations. Our whole‐genome resolution also revealed novel outlier peaks, some of which showed significant genetic differentiation among sampling locations. Comparisons between allochronic winter‐ and spring‐spawning populations revealed highly elevated relative (FST) and absolute (dxy) genetic differentiation near genes involved in reproduction, particularly genes associated with the brain‐pituitary‐gonadal axis, which likely control timing of spawning, contributing to prezygotic isolation. We also found genetic differentiation associated with heat shock proteins and other genes of functional relevance, with complex patterns that may point to multifaceted selection pressures and local adaptation among spawning populations. We provide a high‐resolution picture of U.S. Atlantic cod population structure, revealing greater complexity than is currently recognized in management. Our genome‐scan approach likely underestimates the full suite of adaptive differentiation among sampling locations. Nevertheless, it should inform the revision of stock boundaries to preserve adaptive genetic diversity and evolutionary potential of cod populations.

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Section: Discussionsupporting

confidence: 52%

Novel signals of adaptive genetic variation in northwestern Atlantic cod revealed by whole‐genome sequencing

Clucas

Lou

Therkildsen

et al. 2019

Evolutionary Applications

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“…The development of next‐generation sequencing (NGS) technologies has offered an unprecedented way to study admixture and introgression in many hybridizing taxa including both model and nonmodel species (Allendorf, Hohenlohe, & Luikart, ; Angeloni, Wagemaker, Vergeer, & Ouborg, ; Hoffmann et al., ; Kohn, Murphy, Ostrander, & Wayne, ; Narum, Buerkle, Davey, Miller, & Hohenlohe, ; Ouborg, Pertoldi, Loeschcke, Bijlsma, & Hedrick, ; Primmer, ; Steiner, Putnam, Hoeck, & Ryder, ). However, only few studies have used local ancestry blocks to characterize the genomic landscape of admixture in conservation genomics (but see Duranton et al., ; Galaverni et al., ; VonHoldt, Kays, Pollinger, & Wayne, ).…”

Section: Introductionmentioning

confidence: 99%

Genomic consequences of a recent three‐way admixture in supplemented wild brown trout populations revealed by local ancestry tracts

et al. 2018

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Understanding the evolutionary consequences of human-mediated introductions of domesticated strains into the wild and their subsequent admixture with natural populations is of major concern in conservation biology. However, the genomic impacts of stocking from distinct sources (locally derived vs. divergent) on the genetic integrity of wild populations remain poorly understood. We designed an approach based on estimating local ancestry along individual chromosomes to provide a detailed picture of genomic admixture in supplemented populations. We used this approach to document admixture consequences in the brown trout Salmo trutta, for which decades of stocking practices have profoundly impacted the genetic make-up of wild populations. In southern France, small local Mediterranean populations have been subject to successive introductions of domestic strains derived from the Atlantic and Mediterranean lineages. To address the impact of stocking, we evaluate the extent of admixture from both domestic strains within populations, using 75,684 mapped SNPs obtained from double-digested restriction site-associated DNA sequencing. Then, the chromosomal ancestry profiles of admixed individuals reveal a wider diversity of hybrid and introgressed genotypes than estimated using classical methods for inferring ancestry and hybrid pedigrees. In addition, the length distribution of introgressed tracts retained different timings of introgression between the two domestic strains. We finally reveal opposite consequences of admixture on the level of polymorphism of the recipient populations between domestic strains. Our study illustrates the potential of using the information contained in the genomic mosaic of ancestry tracts in combination with classical methods based on allele frequencies for analysing multiple-way admixture with population genomic data.

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“…(b) The presence of hybrid incompatibilities (i.e., selection against introgressed alleles) may also result in lower foreign ancestry in low recombining regions (Schumer et al, 2018). Such a pattern has been observed in swordtail fish species where the retention of minor parent ancestry was more pronounced in highly recombining regions (Schumer et al, 2018), as well as in European sea bass (Duranton et al, 2018). Similarly, Martin et al (2019) observed stronger barriers to introgression within longer chromosomes displaying lower average recombination rate on average.…”

Section: Variability Of Selective Effects Revealed At Local Scalesmentioning

confidence: 94%

“…Moreover, antagonistic evolutionary mechanisms (e.g., positive and negative selection) may act differentially across the genome, especially if several pulses of hybridization have occurred, resulting in both historical and contemporary gene flow within a population from an exogenous source (Gravel, 2012;McFarlane & Pemberton, 2019). A few recent studies have investigated how the interaction between recombination rate and selection may modulate the genome-wide temporal dynamics of introgression (e.g., Duranton et al, 2018;Harris et al, 2019;Kim et al, 2018;Martin et al, 2019;Martin & Jiggins, 2017;Schumer et al, 2018).…”

mentioning

confidence: 99%

The role of recombination on genome‐wide patterns of local ancestry exemplified by supplemented brook charr populations

et al. 2019

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Assessing the immediate and long‐term evolutionary consequences of human‐mediated hybridization is of major concern for conservation biology. Several studies have documented how selection in interaction with recombination modulates introgression at a genome‐wide scale, but few have considered the dynamics of this process within and among chromosomes. Here, we used an exploited freshwater fish, the brook charr (Salvelinus fontinalis), for which decades of stocking practices have resulted in admixture between wild populations and an introduced domestic strain, to assess both the temporal dynamics and local chromosomal variation in domestic ancestry. We provide a detailed picture of the domestic ancestry patterns across the genome using about 33,000 mapped single nucleotide polymorphisms genotyped in 611 individuals from 24 supplemented populations. For each lake, we distinguished early‐ and late‐generation hybrids using information regarding admixture tracts. To assess the selective outcomes following admixture we then evaluated the relationship between recombination and admixture proportions at three different scales: the whole genome, chromosomes and within 2‐Mb windows. This allowed us to detect a wide range of evolutionary mechanisms varying along the genome, as reflected by the finding of favoured or disfavoured introgression of domestic haplotypes. Among these, the main factor modulating local ancestry was probably the presence of deleterious recessive mutations in the wild populations, which can be efficiently hidden to selection in the presence of long admixture tracts. Overall, our results emphasize the relevance of taking into consideration local ancestry information to assess both the temporal and the chromosomal variation in local admixture ancestry toward better understanding post‐hybridization evolutionary outcomes.

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The origin and remolding of genomic islands of differentiation in the European sea bass

Cited by 112 publications

References 77 publications

Novel signals of adaptive genetic variation in northwestern Atlantic cod revealed by whole‐genome sequencing

Novel signals of adaptive genetic variation in northwestern Atlantic cod revealed by whole‐genome sequencing

Genomic consequences of a recent three‐way admixture in supplemented wild brown trout populations revealed by local ancestry tracts

The role of recombination on genome‐wide patterns of local ancestry exemplified by supplemented brook charr populations

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