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Mitochondrial DNA haplotype nucleotide mismatch distributions for Pacific cod phylogroups. (a) Northwest Pacific; (b) northeast Pacific; (c) Georgia Basin. curves are fitted to bootstrapped mismatch distributions.
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Abstract Pleistocene ice-ages greatly influenced the historical abundances of Pacific cod, Gadus macrocephalus, in the North Pacific and its marginal seas. We surveyed genetic variation at 11 microsatellite loci and mitochondrial (mt) DNA in samples from twelve locations from the Sea of Japan to Washington State. Both microsatellite (mean H = 0.868...
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... from the Georgia Basin (F CT = 0.029, P = 0.037; F CT = 0.023, P = 0.036) (Table 4). This partition also produced the smallest divergences among populations within the two groups (F SC = 0.016; F SC = 0.010), even though both were significant (P £ 0.026). Nucleotide mismatch distributions were generally unimodal for each of the phylogroups (Fig. 5), although none conformed strictly to a sudden demographic or spatial expansion model (P values for Harpending's r = 0.090-0.980 for six tests). Expansion events for the three phylogroups dated to the mid-Pleistocene, ranging from ca. 297 to 218 kyr BP (Table 5). Pre-expansion estimates of N f0 were below 10 000 for all groups and ...
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... Hence, we expected that gene flow in A. clarkii would have varied across geological time according to various environmental factors known to act as barriers in the marine environment, such as temperature, salinity or oceanic currents (Oleksiak, 2019). Gene flow might thus have occurred shortly after populations split (Malinsky et al., 2015;Schumer et al., 2018)-or following a period without exchange between populations (secondary contact; Canino et al., 2010;Liu et al., 2012;Nikolic et al., 2020). ...
Even seemingly homogeneous on the surface, the oceans display high environmental heterogeneity across space and time. Indeed, different soft barriers structure the marine environment, which offers an appealing opportunity to study various evolutionary processes such as population differentiation and speciation. Here, we focus on Amphiprion clarkii (Actinopterygii; Perciformes), the most widespread of clownfishes that exhibits the highest colour polymorphism. Clownfishes can only disperse during a short pelagic larval phase before their sedentary adult lifestyle, which might limit connectivity among populations, thus facilitating speciation events. Consequently, the taxonomic status of A . clarkii has been under debate. We used whole‐genome resequencing data of 67 A . clarkii specimens spread across the Indian and Pacific Oceans to characterize the species' population structure, demographic history and colour polymorphism. We found that A . clarkii spread from the Indo‐Pacific Ocean to the Pacific and Indian Oceans following a stepping‐stone dispersal and that gene flow was pervasive throughout its demographic history. Interestingly, colour patterns differed noticeably among the Indonesian populations and the two populations at the extreme of the sampling distribution (i.e. Maldives and New Caledonia), which exhibited more comparable colour patterns despite their geographic and genetic distances. Our study emphasizes how whole‐genome studies can uncover the intricate evolutionary past of wide‐ranging species with diverse phenotypes, shedding light on the complex nature of the species concept paradigm.
... Hence, we expected that gene flow in A. clarkii would have varied across geological time according 482 to various environmental factors known to act as barriers in the marine environment, such as temperature, salinity, 483 or oceanic currents (Oleksiak, 2019). Gene flow might thus have occurred shortly after populations split (Malinsky 484 et al., 2015;Schumer et al., 2018) -or following a period without exchange between populations (secondary 485 contact; Canino et al., 2010, Nikolic et al., 2020 Although the migration level was heterogeneous across populations and time (Table 1, Table S11), the extent of 487 gene flow was considerably higher compared to what was previously found between sympatric species of 488 clownfishes (ranging from 1.29E-8 to 7.08E-7; Marcionetti 2021) and was more comparable to population-level 489 gene flow in other marine species (ranging from 3E-6 to 4E-6; Nikolic et al., 2020). Additionally, A. clarkii 490 populations diverged in the recent past, with at least 10 times lower divergence times among their populations 491 than the divergence times found in sympatric clownfish species (about 45,697 generations; Marcionetti 2021). ...
Even seemingly homogeneous on the surface, the oceans display high environmental heterogeneity across space and time. Indeed, different soft barriers structure the marine environment, which offers an appealing opportunity to study various evolutionary processes such as population differentiation and speciation. Here, we focus on Amphiprion clarkii (Actinopterygii; Perciformes), the most widespread of clownfishes that exhibits the highest colour polymorphism. Clownfishes can only disperse during a short pelagic larval phase before their sessile adult lifestyle, which might limit connectivity among populations, thus facilitating speciation events. Consequently, the taxonomic status of A. clarkii has been under debate. We used whole-genome resequencing data of 67 A. clarkii specimens spread across the Indian and Pacific Oceans to characterise the species’ population structure, demographic history, and colour polymorphism. We found that A. clarkii spread from the Indo-Pacific Ocean to the Pacific and Indian Oceans following a stepping-stone dispersal and that gene flow was pervasive throughout its demographic history. Moreover, edge populations exhibited more similar colouration patterns compared to central populations. However, we demonstrate that colour polymorphism is not associated with population structure, thus, colour phenotype is unreliable in assessing the taxonomic status of A. clarkii . Our study further highlights the power of whole-genome comparative studies to determine the taxonomy of geographically wide-ranging and phenotypically diverse species, supporting the status of A. clarkii as a single species.
... This analysis revealed three main regions of large genetic distances: two on the eastern edge [British Columbia (CAN) and Eastern Gulf of Alaska (EGA)] and one on the western edge [Kamchatka (KAM); Commander, Aleutian Islands (CAA); Shirshov, Russia (SUR); and West Bering Sea (WBS)]. This pattern is also consistent with northward colonization, as suggested for the Pacific cod Gadus macrocephalus (Canino et al., 2010), and walleye pollock Gadus chalcogrammus . Geographic patterns of genetic diversity can also provide insight into modes of postglacial colonization (Bernatchez and Wilson, 1998). ...
... During the past 20000 years, the ranges of species in the North Pacific have been modified, fragmented, and/or merged because of paleoclimatic events (Theodoridis et al., 2018). Species that experience boom-bust cycles in abundance may show reductions in genetic diversity, reflecting historical population bottlenecks or deviations from mutationdrift equilibria (Canino et al., 2010). However, when gene flow is strong and/or populations are large, as is typical of marine organisms, divergence progresses slowly at selectively neutral loci (Palumbi, 1996). ...
The sablefish Anoplopoma fimbria is distributed on the continental shelf of the North Pacific, has a high commercial value for both fisheries and aquaculture, and represents a shared resource between countries in the North Pacific basin. In the present study, we extend the geographic range surveyed in previous studies and reexamine the population's genetic structure by integrating phylogeographic patterns of mitochondrial DNA and microsatellite DNA markers. Our results contradict the proposal that sablefish constitute a single population throughout their distributional range. We observed a signal of ancient divergence in mtDNA that differentiates the North Pacific West Coast from the rest of the sample sites, and microsatellite markers reveal a contemporary isolation of Mexican sablefish. Our findings show genetic differences between localities that should be explored in more detail to fully understand the interconnectedness that appears to exist between populations.
... A complex genetic history of multiple trans-Arctic divergence events from the Pacific to the Atlantic is also supported in the nudibranch Aeolidia papillosa (Linnaeus, 1761), the predator of M. senile (see Carmona et al., 2013;Laakkonen et al., 2020). Beringia has also been identified as one of several putative refugia and source populations for fish and invertebrates (see Ishida and Taylor 2007;Canino et al., 2010;Yamamoto et al., 2014). ...
Members of the sea anemone genus Metridium are abundant in temperate rocky habitats and fouling communities. Their biogeographic history is expected to reflect changes in currents and habitats that have influenced benthic communities, such as the climate-influenced changes that occurred during the Last Glacial Maximum. More recently, however, anthropogenic influences such as shipping transportation and the creation of artificial habitat have altered and affected the composition of modern-day marine communities. Here we use sequence-capture data to examine the genetic structure of Metridium across its shallow-water distribution to (1) evaluate species boundaries within Metridium, (2) elucidate the dispersal history of Metridium between and among oceans, and (3) assess the influence of anthropogenic movement on modern-day populations. We find strong evidence for two species within Metridium: M. farcimen and M. senile. Dispersal from the Pacific to the Atlantic included a subsequent isolation of a small population in or above the Bering Sea, which has presumably moved southward. Within the native range of M. senile, admixture is prevalent even between oceans as a result of anthropogenic activities. The nonnative populations in Chile and the Falkland Islands came from at least two distinct introduction events originating from both coasts of the United States in the North Pacific and North Atlantic Oceans. Hybridization between M. senile and M. farcimen is documented as occurring in anthropogenically influenced habitats. The heavy influence from anthropogenic activities will continue to impact our understanding of marine organisms, particularly within the native range and for those that are easily transported across long distances.
... The pairwise F ST between the EBS and Washington coast was roughly double that between the Aleutian Islands and Bering Sea spawning populations (Table 3; Figure 3). This may be consistent with a framework in which gene flow acts to homogenize allele fre- Islands populations began diverging soon after they colonized the region following the recession of the last glacial maximum (Canino et al., 2010). ...
Patterns of genetic differentiation across the genome can provide insight into selective forces driving adaptation. We used pooled whole genome sequencing, gene annotation, and environmental covariates to evaluate patterns of genomic differentiation and to investigate mechanisms responsible for divergence among proximate Pacific cod (Gadus macrocephalus) populations from the Bering Sea and Aleutian Islands and more distant Washington Coast cod. Samples were taken from eight spawning locations, three of which were replicated to estimate consistency in allele frequency estimation. A kernel smoothing moving weighted average of relative divergence (FST) identified 11 genomic islands of differentiation between the Aleutian Islands and Bering Sea samples. In some islands of differentiation, there was also elevated absolute divergence (dXY) and evidence for selection, despite proximity and potential for gene flow. Similar levels of absolute divergence (dXY) but roughly double the relative divergence (FST) were observed between the distant Bering Sea and Washington Coast samples. Islands of differentiation were much smaller than the four large inversions among Atlantic cod ecotypes. Islands of differentiation between the Bering Sea and Aleutian Island were associated with SNPs from five vision system genes, which can be associated with feeding, predator avoidance, orientation, and socialization. We hypothesize that islands of differentiation between Pacific cod from the Bering Sea and Aleutian Islands provide evidence for adaptive differentiation despite gene flow in this commercially important marine species.
... Meanwhile, the high fidelity of Pacific cod (Spies, 2012) combined with the presence of barriers in the form of currents (Gaylord and Gaines, 2000), deep ocean trenches (Schüller, 2011) and temperature gradients (Stevenson and Lauth, 2019) likely decreased the genetic exchange and contributed to the population divergence of Pacific cod. Previous molecular phylogeographic studies revealed that since the Pleistocene ice-ages, Pacific cod has differentiated into two distinct genomic groups: the western population (WP) and the eastern population (EP) of the North Pacific (Grant et al., 1987;Canino et al., 2010). ...
... After this data cleaning procedure, a total of 2585 occurrence records were retained. According to the genetic differentiation studies of Grant (1987) and Canino (2010), Pacific cod has differentiated into two populations: the WP, with 371 occurrence records, and the EP, with 2214 occurrence records ( Fig. 1). ...
... Recently, however, more studies have demonstrated intraspecific differential response to climatic predictors and highlighted the importance of focusing on the population level when implementing SDMs (e. g., Collart et al., 2021;Hu et al., 2021;Ikeda et al., 2017;Zhang et al., 2021). The genetic differentiation evidenced by the previous molecular analyses coupled with the niche differentiation verified by this study for the WP and EP implied the significance of building SDMs at the population level to account for local adaptation (Grant et al., 1987;Canino et al., 2010). Our population-level SDMs demonstrated the variable responses of populations to environmental gradients, implying that pooling population data to construct a global SDM at the species level may mask local differences in response to environmental conditions. ...
Several studies have demonstrated the importance of integrating intraspecific genetic variation in forecasting the habitat suitability of species under climate change scenarios. The Pacific cod (Gadus macrocephalus) is an economically important fish species in the North Pacific that can be classified into western and eastern populations based on molecular phylogeographic data. Herein, we first quantified the realized niche of the two Pacific cod populations using n-dimensional hypervolumes and estimated the niche differentiation between the populations. We then projected the habitat suitability based on the georeferenced occurrence records and environmental predictors using species distribution models (SDMs) at the population and species levels. The low niche overlap demonstrated the marked niche differentiation between the two populations. The distinct responses of the populations to climate predictors implied that the population-level SDM produced more reliable projections than the corresponding species-level SDM. The model indicated that the eastern population expanded its suitable area northward, while maintaining most of its current habitat and exhibited resilience to climate impacts. However, the western population lost much of its current suitable area, while colonizing a new habitat in a small section of the offshore waters of the Japanese Sea, implying the vulnerability of this population to climate change. This study highlights the necessity of incorporating intraspecific genetic variation into SDMs to predict the habitat suitability of Pacific cod on the global scale. The spatiotemporal predictive maps of habitat suitability provide crucial information for designing climate-adaptive conservation and management strategies based on more precise taxonomic units for the sustainability of Pacific cod.
... It is among the top fished species in the world, with the major fishing grounds in the Bering Sea and Sea of Okhotsk (Bulatov, 2014). G. macrocephalus occur on continental shelves and slopes from 34 to 63 • N latitude on both sides of the North Pacific from the Yellow Sea to the Okhotsk and Bering seas, and across the northeastern Pacific to Oregon (Allen and Smith, 1988;Canino et al., 2010). Both G. chalcogrammus and G. macrocephalus prefer waters above 0 • C (Wyllie-Echeverria and Wooster, 1998; Kotwicki and Lauth, 2013) but otherwise tolerate a large temperature range (Baker and Hollowed, 2014). ...
We used genetic techniques to identify gadids (cods) to species in the Pacific Arctic during a time of substantial physical change in the marine ecosystem between 2012 and 2019. The dominant fish species in the Chukchi Sea is Arctic Cod (Boreogadus saida); however, other gadids such as Saffron Cod (Eleginus gracilis), Pacific Cod (Gadus macrocephalus) and Walleye Pollock (Gadus chalcogrammus) have been observed. Two aims in this study were to evaluate the accuracy of at sea morphological identification (which can be difficult for juveniles) with genetic species identification and to document potential variation in species composition and distribution of gadids in the Pacific Arctic in response to changing environmental conditions. Microsatellite and mtDNA genetic results revealed that most B. saida collected in the Chukchi Sea in 2012 and 2013 were correctly identified at sea. Conversely, genetic results from samples collected in 2017 and 2019 revealed a large number of G. chalcogrammus and some G. macrocephalus and E. gracilis that were initially identified at sea as B. saida. The majority of misidentification occurred between B. saida and G. chalcogrammus. This study indicates a northward shift of G. chalcogrammus and B. saida during warmer conditions. In addition, juvenile Polar Cod (A. glacialis), which is not typically found in the Chukchi Sea and was not identified at sea, was genetically detected on 3 hauls on the northern Chukchi Shelf, outside of its documented distribution. Accurate species identification, especially during a time of changing marine landscapes, is not only important for survey abundance estimates but for downstream analyses as well. This emphasizes the value of implementing strategies for correct identification of the gadid species to better capture and monitor responses to varying and likely changing conditions. Our results provide strong evidence of distributional shifts and range expansions of gadid species in the Arctic, which may be the result of changing climactic conditions.
... The reconstructed demographic history was plotted using the 'psmc plot.pl' script with a generation time of g = 6 years and a mutation rate of μ = 8.29 × 10 −9 site −1 year −1 (5.0 × 10 −8 site −1 generation −1 ) [26]. By default, the variance of N e was estimated using 100 bootstrap replicates. ...
... In the present study, reconstructing the Pleistocene demographic history of G. macrocephalus, revealed that G. macrocephalus population also experienced bottleneck and expansion. Similarly, Canino et al. reported that G. macrocephalus expansions were evident by using the mismatch distributions and Bayesian skyline plots of mitochondrial genome, but the start of expansions appeared to predate the last glacial maximum (21,000 years ago) [26]. This finding was consistent with our results. ...
Gadus macrocephalus (Pacific cod) is an economically important species on the northern coast of the Pacific. Although numerous studies on G. macrocephalus exist, there are few reports on its genomic data. Here, we used whole-genome sequencing data to elucidate the genomic characteristics and phylogenetic relationship of G. macrocephalus. From the 19-mer frequency distribution, the genome size was estimated to be 658.22 Mb. The heterozygosity, repetitive sequence content and GC content were approximately 0.62%, 27.50% and 44.73%, respectively. The draft genome sequences were initially assembled, yielding a total of 500,760 scaffolds (N50 = 3,565 bp). A total of 789,860 microsatellite motifs were identified from the genomic data, and dinucleotide repeat was the most dominant simple sequence repeat motif. As a byproduct of whole-genome sequencing, the mitochondrial genome was assembled to investigate the evolutionary relationships between G. macrocephalus and its relatives. On the basis of 13 protein-coding gene sequences of the mitochondrial genome of Gadidae species, the maximum likelihood phylogenetic tree showed that complicated relationships and divergence times among Gadidae species. Demographic history analysis revealed changes in the G. macrocephalus population during the Pleistocene by using the pairwise sequentially Markovian coalescent model. These findings supplement the genomic data of G. macrocephalus, and make a valuable contribution to the whole-genome studies on G. macrocephalus.
... There is both habitat and climate variability across the North Pacific Ocean (Mundy, 2005), and likely significant cod population variability as well (Cunningham et al., 2009;NOAA, 2010). Variability in fish populations extends to longer time periods, though few studies have employed longterm (i.e., >200 yr) data sets to understand the broader context of these shifts (e.g., Baumgartner et al., 1992;Finney et al., 2002;Canino et al., 2010). Climate conditions have changed broadly across the North Pacific since the Pleistocene-Holocene transition, and these changes had variable effects on local environments (e.g., Mann et al., 1998). ...
In this paper, we compile estimates of cod size distributions based on zooarchaeological data and contemporary length-frequency data to look at variability in size composition through time across the North Pacific, from the northern Kuril Islands through the Aleutian Islands to southeast Alaska. The results suggest that a strong longitudinal trend in cod size has remained consistent over time, with the largest cod found to the west. We find that five of nine sites show that overall cod length and distribution of the largest fish remain relatively unchanged. Two sites where we find truncation of the length distributions-or loss of the largest fish-are places where the modern fisheries have the longest history and have been most intense, suggesting a potential for anthropogenic impacts on these local populations. We acknowledge two limitations in these data: (1) there are differences in selectivity between the ancient and modern fisheries; and (2) seasonal variability in fish availability was observed to be an important explanatory variable in the modern data set, but the season of harvest is poorly understood for the ancient collections. Therefore, while differences observed between the two data sets suggest possible anthropogenic influence on the size structure of Pacific cod, they are not conclusive.
... While many marine species are represented by large population sizes and high gene flow (albeit not lacking genetic structure ;Hauser & Carvalho, 2008), they also often include relatively isolated peripheral populations in environmentally distinct habitats (Canino et al., 2010;Knutsen et al., 2003;Ruzzante et al., 2000). Peripheral populations are commonly remnants of refugial populations, left behind after recolonization of current habitats at the end of the last glaciation (Hewitt, 1996;Provan, 2013). ...
... Peripheral populations are commonly remnants of refugial populations, left behind after recolonization of current habitats at the end of the last glaciation (Hewitt, 1996;Provan, 2013). Due to their long isolation, these populations exhibit relatively high genetic differentiation (Canino et al., 2010;Maggs et al., 2008) and may be uniquely adapted to their local environment. The importance of the genetic diversity of such populations has been recognized for some time (Hampe & Petit, 2005;Hewitt, 1996), but their potential contribution to adaptive changes in core populations via gene flow of beneficial alleles is still relatively unknown (Provan & Maggs, 2012), especially in marine fishes of commercial importance. ...
... Quality filtering and demultiplexing of raw sequences, de novo construction of a reference database of RAD loci, SNP discovery, and genotyping, was completed using a combination of the Stacks v1.44 pipeline (Catchen et al., 2011(Catchen et al., , 2013, Bowtie (Langmead et al., 2009), and NCBI's Basic Local Alignment Search Tool, BLAST (Altschul et al., 1990), according to the procedures outlined in Drinan et al. (2018) and Brieuc et al. (2014). Final F I G U R E 1 Map of sampling sites around the Korean Peninsula used for this study (labeled points), augmented with results from previous genetic analyses in the surrounding region (Canino et al., 2010;Smirnova et al., 2019;Suda et al., 2017). Point coloration represents the putative populations of each site according to the genetic structure described by RAD loci (this study) and microsatellite DNA (msDNA; previous studies). ...
Small and isolated peripheral populations, which are often remnants of glacial refugia, offer an opportunity to determine the magnitude and direction of fine-scale connectivity in high gene flow marine species. When located at the equatorial edge of a species’ range, these populations may also harbor genetic diversity related to survival and reproduction at higher temperatures, a critical resource for marine species facing warming ocean temperatures. Pacific cod (Gadus macrocephalus), a marine fish in the North Pacific, has already experienced major shifts in biomass and distribution linked to climate change. We estimated the magnitude and direction of connectivity between peripheral populations of Pacific cod at the southern edge of the species’ range, by conducting restriction site-associated DNA (RAD) sequencing and individual assignment on fish collected around the Korean Peninsula during the spawning season. Three populations on the western, eastern, and southern Korean coasts were highly differentiated (FST = 0.025–0.042) and relatively small (Ne = 433–1,777). Ten putative dispersers and estimates of contemporary migration rates revealed asymmetrical, west-to-east movement around the Korean Peninsula, at a higher rate than predicted by indirect estimates of connectivity (FST). Allele frequencies at 87 RAD loci were decisively correlated with strong marine temperature gradients between the warmer southern coast and the cooler waters of the eastern and western coasts. Despite relatively small sample sizes, our data suggest asymmetrical dispersal and gene flow, potentially involving adaptive alleles, between peripheral populations inhabiting markedly different thermal regimes. Our study emphasizes the conservation value of peripheral populations in high gene flow marine fish species.
