Einar Árnason

Withdrawal Statement: The authors have withdrawn their manuscript because they have discovered errors in the alignment of parts of the data. Miscommunication with the sequencing center led to a misunderstanding of the pooling design and incorrect merging of sequencing read files from different individuals into single bam files. Thus bam alignments for each individual sample of four out of 12 batches are based on a majority of reads from that individual but also on reads from one or two other individuals. Individuals in eight other batches were not affected by this. However, for this paper, the entire data was jointly genotyped to produce vcf files, and the joint genotyping may thus indirectly affect samples of other batches. Revising the paper by teasing apart the affected and non-affected parts of the data is not an option, and they, therefore, withdraw the preprint. They are reanalyzing the dataset. Therefore, the authors do not wish this work to be cited as reference for the project. If you have any questions, please contact the corresponding author.

Highly fecund natural populations characterized by high early mortality abound, yet our knowledge about their recruitment dynamics is somewhat rudimentary. This knowledge gap has implications for our understanding of genetic variation, population connectivity, local adaptation, and the resilience of highly fecund populations. The concept of sweepstakes reproductive success, which posits a considerable variance and skew in individual reproductive output, is key to understanding the distribution of individual reproductive success. However, it still needs to be determined whether highly fecund organisms reproduce through sweepstakes and, if they do, the relative roles of neutral and selective sweepstakes. Here, we use coalescent-based statistical analysis of population genomic data to show that selective sweepstakes likely explain recruitment dynamics in the highly fecund Atlantic cod. We show that the Kingman coalescent (modelling no sweepstakes) and the Xi-Beta coalescent (modelling random sweepstakes), including complex demography and background selection, do not provide an adequate fit for the data. The Durrett–Schweinsberg coalescent, in which selective sweepstakes result from recurrent and pervasive selective sweeps of new mutations, offers greater explanatory power. Our results show that models of sweepstakes reproduction and multiple-merger coalescents are relevant and necessary for understanding genetic diversity in highly fecund natural populations. These findings have fundamental implications for understanding the recruitment variation of fish stocks and general evolutionary genomics of high-fecundity organisms.

Highly fecund natural populations characterized by high early mortality abound, yet our knowledge about their recruitment dynamics is somewhat rudimentary. This knowledge gap has implications for our understanding of genetic variation, population connectivity, local adaptation, and the resilience of highly fecund populations. The concept of sweepstakes reproductive success, which posits a considerable variance and skew in individual reproductive output, is key to understanding the distribution of individual reproductive success. However, it still needs to be determined whether highly fecund organisms reproduce through sweepstakes and, if they do, the relative roles of neutral and selective sweepstakes. Here we use coalescent-based statistical analysis of population genomic data to show that selective sweepstakes likely explain recruitment dynamics in the highly fecund Atlantic cod. We show that the Kingman coalescent (modeling no sweepstakes) and the Xi-Beta coalescent (modeling random sweepstakes), including complex demography and background selection, do not provide an adequate fit for the data. The Durrett-Schweinsberg coalescent, in which selective sweepstakes result from recurrent and pervasive selective sweeps of new mutations, offers greater explanatory power. Our results show that models of sweepstakes reproduction and multiple-merger coalescents are relevant and necessary for understanding genetic diversity in highly fecund natural populations. These findings have fundamental implications for understanding the recruitment variation of fish stocks and general evolutionary genomics of high-fecundity organisms.

Detailed modeling of a species’ history is of prime importance for understanding how natural selection operates over time. Most methods designed to detect positive selection along sequenced genomes, however, use simplified representations of past histories as null models of genetic drift. Here, we present the first method that can detect signatures of strong local adaptation across the genome using arbitrarily complex admixture graphs, which are typically used to describe the history of past divergence and admixture events among any number of populations. The method—called graph-aware retrieval of selective sweeps (GRoSS)—has good power to detect loci in the genome with strong evidence for past selective sweeps and can also identify which branch of the graph was most affected by the sweep. As evidence of its utility, we apply the method to bovine, codfish, and human population genomic data containing panels of multiple populations related in complex ways. We find new candidate genes for important adaptive functions, including immunity and metabolism in understudied human populations, as well as muscle mass, milk production, and tameness in specific bovine breeds. We are also able to pinpoint the emergence of large regions of differentiation owing to inversions in the history of Atlantic codfish.

Genome sequencing of codfish supporting large fisheries shows rampant hybridization providing fuel for their adaptations.

Detailed modeling of a species’ history is of prime importance for understanding how natural selection operates over time. Most methods designed to detect positive selection along sequenced genomes, however, use simplified representations of past histories as null models of genetic drift. Here, we present the first method that can detect signatures of strong local adaptation across the genome using arbitrarily complex admixture graphs, which are typically used to describe the history of past divergence and admixture events among any number of populations. The method—called Graph-aware Retrieval of Selective Sweeps ( GRoSS )—has good power to detect loci in the genome with strong evidence for past selective sweeps and can also identify which branch of the graph was most affected by the sweep. As evidence of its utility, we apply the method to bovine, codfish and human population genomic data containing multiple population panels related in complex ways. We find new candidate genes for important adaptive functions, including immunity and metabolism in under-studied human populations, as well as muscle mass, milk production and tameness in specific bovine breeds. We are also able to pinpoint the emergence of large regions of differentiation due to inversions in the history of Atlantic codfish.

Speciation often involves the splitting of a lineage and the adaptation of daughter lineages to different environments. It may also involve the merging of divergent lineages, thus creating a stable homoploid hybrid species ¹ that constructs a new ecological niche by transgressing ² the ecology of the parental types. Hybrid speciation may also contribute to enigmatic and cryptic biodiversity in the sea. ^3,4 The enigmatic walleye pollock, which is not a pollock at all but an Atlantic cod that invaded the Pacific 3.8 Mya, ⁵ differs considerably from its presumed closest relatives, the Pacific and Atlantic cod. Among the Atlantic cod, shallow-water coastal and deep-water migratory frontal ecotypes are associated with highly divergent genomic islands; ^6,7 however, intermediates remain an enigma. ⁸ Here, we performed whole-genome sequencing of over 200 individuals using up to 33 million SNPs based on genotype likelihoods ⁹ and showed that the evolutionary status of walleye pollock is a hybrid species: it is a hybrid between Arctic cod and Atlantic cod that transgresses the ecology of its parents. For the first time, we provide decisive evidence that the Atlantic cod coastal and frontal ecotypes are separate species that hybridized, leading to a true-breeding hybrid species that differs ecologically from its parents. We refute monophyly and dichotomous branching of these taxa, and stress the importance of looking beyond branching trees at admixture and hybridity. Our study demonstrates the power of whole-genome sequencing and population genomics in providing deep insights into fundamental processes of speciation. Our study was a starting point for further work aimed at examining the criteria of hybrid speciation, ¹⁰ selection, sterility and structural chromosomal variation ¹¹ among cod-fish, which are among the most important fish stocks in the world. The hybrid nature of both the walleye pollock and Atlantic cod raises the question concerning the extent to which very profitable fisheries ^12,13 depend on hybrid vigour. Our results have implications for management of marine resources in times of rapid climate change. ^14,15

The Pan I locus in Atlantic cod lies in a genomic island of divergence extending over a large genomic region. The locus has two divergent alleles, defined by a single DraI restriction site, that have been related to behavioral differences of habitat selection by depth and temperature. The Pan I locus is known to be under an unusual mix of balancing selection and selective sweeps within the functional types. Here we study nucleotide variation in a 12.5 kb region inside the genomic island harboring Pan I and neighboring loci for sortilin 1 (Sort1) and ataxin 7-like 2 (Atxn7l2) which we partially covered. Variation of the 31 gene copies throughout the region falls into two divergent haplogroups that correlate with the 25 copies of A and six copies of B alleles of Pan I. The unfolded site frequency spectrum for the part with Pacific cod used as the outgroup is trimodal with a mode at singletons and two high frequency modes at 6/31 and 25/31 representing the two genealogical lineages. The folded site frequency spectrum for the entire region similarly has a high frequency mode of mutations that have accumulated on the two lineages. The high frequency of singletons is accounted for by multiple merger coalescent models. Parameter estimates using these models indicate sweepstakes reproduction. The high frequency modes of the spectrum is evidence for balancing selection. Analysis of non-synonymous changes shows that Pan I is at least one focus of selection within the genomic island. There may be multiple sites of selection and epistatic interactions. There is extensive linkage disequilibrium throughout the region. We suggest that the genomic island of divergence is a supergene of co-adapted complexes possibly locked together by structural variation.

The Pan I locus in Atlantic cod lies in a genomic island of divergence extending over a large genomic region. The locus has two divergent alleles, defined by a single DraI restriction site, that have been related to behavioral differences of habitat selection by depth and temperature. The Pan I locus is known to be under an unusual mix of balancing selection and selective sweeps within the functional types. Here we study nucleotide variation in a 12.5 kb region inside the genomic island harboring Pan I and neighboring loci for sortilin 1 (Sort1) and ataxin 7-like 2 (Atxn7l2) which we partially covered. Variation of the 31 gene copies throughout the region falls into two divergent haplogroups that correlate with the 25 copies of A and six copies of B alleles of Pan I. The unfolded site frequency spectrum for the part with Pacific cod used as the outgroup is trimodal with a mode at singletons and two high frequency modes at 6/31 and 25/31 representing the two genealogical lineages. The folded site frequency spectrum for the entire region similarly has a high frequency mode of mutations that have accumulated on the two lineages. The high frequency of singletons is accounted for by multiple merger coalescent models. Parameter estimates using these models indicate sweepstakes reproduction. The high frequency modes of the spectrum is evidence for balancing selection. Analysis of non-synonymous changes shows that Pan I is at least one focus of selection within the genomic island. There may be multiple sites of selection and epistatic interactions. There is extensive linkage disequilibrium throughout the region. We suggest that the genomic island of divergence is a supergene of co-adapted complexes possibly locked together by structural variation.