Ian R. Bradbury

Global patterns in marine dispersal estimates: the influence of geography, taxonomic category and life history

We examine estimates of dispersal in a broad range of marine species through an analysis of published values, and evaluate how well these values represent global patterns through a comparison with correlates of dispersal. Our analysis indicates a historical focus in dispersal studies on low-dispersal/low-latitude species, and we hypothesize that these studies are not generally applicable and representative of global patterns. Large-scale patterns in dispersal were examined using a database of correlates of dispersal such as planktonic larval duration (PLD, 318 species) and genetic differentiation (FST, 246 species). We observed significant differences in FST (p<0.001) and PLD (p<0.001) between taxonomic groups (e.g. fishes, cnidarians, etc.). Within marine fishes (more than 50% of datasets), the prevalence of demersal eggs was negatively associated with PLD (R2=0.80, p<0.001) and positively associated with genetic structure (R2=0.74, p<0.001). Furthermore, dispersal within marine fishes (i.e. PLD and FST) increased with latitude, adult body size and water depth. Of these variables, multiple regression identified latitude and body size as persistent predictors across taxonomic levels. These global patterns of dispersal represent a first step towards understanding and predicting species-level and regional differences in dispersal, and will be improved as more comprehensive data become available.

Parallel adaptive evolution of Atlantic cod on both sides of the Atlantic Ocean in response to temperature

Despite the enormous economic and ecological importance of marine organisms, the spatial scales of adaptation and biocomplexity remain largely unknown. Yet, the preservation of local stocks that possess adaptive diversity is critical to the long-term maintenance of productive stable fisheries and ecosystems. Here, we document genomic evidence of range-wide adaptive differentiation in a broadcast spawning marine fish, Atlantic cod (Gadus morhua), using a genome survey of single nucleotide polymorphisms. Of 1641 gene-associated polymorphisms examined, 70 (4.2%) tested positive for signatures of selection using a Bayesian approach. We identify a subset of these loci (n = 40) for which allele frequencies show parallel temperature-associated clines (p < 0.001, r2 = 0.89) in the eastern and western north Atlantic. Temperature associations were robust to the statistical removal of geographic distance or latitude effects, and contrasted ‘neutral’ loci, which displayed no temperature association. Allele frequencies at temperature-associated loci were significantly correlated, spanned three linkage groups and several were successfully annotated supporting the involvement of multiple independent genes. Our results are consistent with the evolution and/or selective sweep of multiple genes in response to ocean temperature, and support the possibility of a new conservation paradigm for non-model marine organisms based on genomic approaches to resolving functional and adaptive diversity.

Genomic islands of divergence and their consequences for the resolution of spatial structure in an exploited marine fish

As populations diverge, genomic regions associated with adaptation display elevated differentiation. These genomic islands of adaptive divergence can inform conservation efforts in exploited species, by refining the delineation of management units, and providing genomic tools for more precise and effective population monitoring and the successful assignment of individuals and products. We explored heterogeneity in genomic divergence and its impact on the resolution of spatial population structure in exploited populations of Atlantic cod, Gadus morhua, using genome wide expressed sequence derived single nucleotide polymorphisms in 466 individuals sampled across the range. Outlier tests identified elevated divergence at 5.2% of SNPs, consistent with directional selection in one‐third of linkage groups. Genomic regions of elevated divergence ranged in size from a single position to several cM. Structuring at neutral loci was associated with geographic features, whereas outlier SNPs revealed genetic discontinuities in both the eastern and western Atlantic. This fine‐scale geographic differentiation enhanced assignment to region of origin, and through the identification of adaptive diversity, fundamentally changes how these populations should be conserved. This work demonstrates the utility of genome scans for adaptive divergence in the delineation of stock structure, the traceability of individuals and products, and ultimately a role for population genomics in fisheries conservation.

Estimating contemporary early life-history dispersal in an estuarine fish: integrating molecular and otolith elemental approaches

Dispersal during the early life history of the anadromous rainbow smelt, Osmerus mordax, was examined using assignment testing and mixture analysis of multilocus genotypes and otolith elemental composition. Six spawning areas and associated estuarine nurseries were sampled throughout southeastern Newfoundland. Samples of adults and juveniles isolated by > 25 km displayed moderate genetic differentiation (FST ~ 0.05), whereas nearby (< 25 km) spawning and nursery samples displayed low differentiation (FST < 0.01). Self‐assignment and mixture analysis of adult spawning samples supported the hypothesis of independence of isolated spawning locations (> 80% self‐assignment) with nearby runs self‐assigning at rates between 50 % and 70%. Assignment and mixture analysis of juveniles using adult baselines indicated high local recruitment at several locations (70–90%). Nearby (< 25 km) estuaries at the head of St Marys Bay showed mixtures of individuals (i.e. 20–40% assignment to adjacent spawning location). Laser ablation inductively coupled mass spectrometry transects across otoliths of spawning adults of unknown dispersal history were used to estimate dispersal among estuaries across the first year of life. Single‐element trends and multivariate discriminant function analysis (Sr:Ca and Ba:Ca) classified the majority of samples as estuarine suggesting limited movement between estuaries (< 0.5%). The mixtures of juveniles evident in the genetic data at nearby sites and a lack of evidence of straying in the otolith data support a hypothesis of selective mortality of immigrants. If indeed selective mortality of immigrants reduces the survivorship of dispersers, estimates of dispersal in marine environments that neglect survival may significantly overestimate gene flow.

Conservation genomics of anadromous Atlantic salmon across its North American range: outlier loci identify the same patterns of population structure as neutral loci

Anadromous Atlantic salmon (Salmo salar) is a species of major conservation and management concern in North America, where population abundance has been declining over the past 30 years. Effective conservation actions require the delineation of conservation units to appropriately reflect the spatial scale of intraspecific variation and local adaptation. Towards this goal, we used the most comprehensive genetic and genomic database for Atlantic salmon to date, covering the entire North American range of the species. The database included microsatellite data from 9142 individuals from 149 sampling locations and data from a medium‐density SNP array providing genotypes for >3000 SNPs for 50 sampling locations. We used neutral and putatively selected loci to integrate adaptive information in the definition of conservation units. Bayesian clustering with the microsatellite data set and with neutral SNPs identified regional groupings largely consistent with previously published regional assessments. The use of outlier SNPs did not result in major differences in the regional groupings, suggesting that neutral markers can reflect the geographic scale of local adaptation despite not being under selection. We also performed assignment tests to compare power obtained from microsatellites, neutral SNPs and outlier SNPs. Using SNP data substantially improved power compared to microsatellites, and an assignment success of 97% to the population of origin and of 100% to the region of origin was achieved when all SNP loci were used. Using outlier SNPs only resulted in minor improvements to assignment success to the population of origin but improved regional assignment. We discuss the implications of these new genetic resources for the conservation and management of Atlantic salmon in North America.

Transatlantic secondary contact in Atlantic Salmon, comparing microsatellites, a single nucleotide polymorphism array and restriction‐site associated DNA sequencing for the resolution of complex spatial structure

Identification of discrete and unique assemblages of individuals or populations is central to the management of exploited species. Advances in population genomics provide new opportunities for re‐evaluating existing conservation units but comparisons among approaches remain rare. We compare the utility of RAD‐seq, a single nucleotide polymorphism (SNP) array and a microsatellite panel to resolve spatial structuring under a scenario of possible trans‐Atlantic secondary contact in a threatened Atlantic Salmon, Salmo salar, population in southern Newfoundland. Bayesian clustering indentified two large groups subdividing the existing conservation unit and multivariate analyses indicated significant similarity in spatial structuring among the three data sets. mtDNA alleles diagnostic for European ancestry displayed increased frequency in southeastern Newfoundland and were correlated with spatial structure in all marker types. Evidence consistent with introgression among these two groups was present in both SNP data sets but not the microsatellite data. Asymmetry in the degree of introgression was also apparent in SNP data sets with evidence of gene flow towards the east or European type. This work highlights the utility of RAD‐seq based approaches for the resolution of complex spatial patterns, resolves a region of trans‐Atlantic secondary contact in Atlantic Salmon in Newfoundland and demonstrates the utility of multiple marker comparisons in identifying dynamics of introgression.

Evaluating SNP ascertainment bias and its impact on population assignment in Atlantic cod, Gadus morhua.

The increasing use of single nucleotide polymorphisms (SNPs) in studies of nonmodel organisms accentuates the need to evaluate the influence of ascertainment bias on accurate ecological or evolutionary inference. Using a panel of 1641 expressed sequence tag–derived SNPs developed for northwest Atlantic cod (Gadus morhua), we examined the influence of ascertainment bias and its potential impact on assignment of individuals to populations ranging widely in origin. We hypothesized that reductions in assignment success would be associated with lower diversity in geographical regions outside the location of ascertainment. Individuals were genotyped from 13 locations spanning much of the contemporary range of Atlantic cod. Diversity, measured as average sample heterozygosity and number of polymorphic loci, declined (c. 30%) from the western (He = 0.36) to eastern (He = 0.25) Atlantic, consistent with a signal of ascertainment bias. Assignment success was examined separately for pools of loci representing differing degrees of reductions in diversity. SNPs displaying the largest declines in diversity produced the most accurate assignment in the ascertainment region (c. 83%) and the lowest levels of correct assignment outside the ascertainment region (c. 31%). Interestingly, several isolated locations showed no effect of assignment bias and consistently displayed 100% correct assignment. Contrary to expectations, estimates of accurate assignment range‐wide using all loci displayed remarkable similarity despite reductions in diversity. Our results support the use of large SNP panels in assignment studies of high geneflow marine species. However, our evidence of significant reductions in assignment success using some pools of loci suggests that ascertainment bias may influence assignment results and should be evaluated in large‐scale assignment studies.

Does fish larval dispersal differ between high and low latitudes

Several factors lead to expectations that the scale of larval dispersal and population connectivity of marine animals differs with latitude. We examine this expectation for demersal shorefishes, including relevant mechanisms, assumptions and evidence. We explore latitudinal differences in (i) biological (e.g. species composition, spawning mode, pelagic larval duration, PLD), (ii) physical (e.g. water movement, habitat fragmentation), and (iii) biophysical factors (primarily temperature, which could strongly affect development, swimming ability or feeding). Latitudinal differences exist in taxonomic composition, habitat fragmentation, temperature and larval swimming, and each difference could influence larval dispersal. Nevertheless, clear evidence for latitudinal differences in larval dispersal at the level of broad faunas is lacking. For example, PLD is strongly influenced by taxon, habitat and geographical region, but no independent latitudinal trend is present in published PLD values. Any trends in larval dispersal may be obscured by a lack of appropriate information, or use of ‘off the shelf’ information that is biased with regard to the species assemblages in areas of concern. Biases may also be introduced from latitudinal differences in taxa or spawning modes as well as limited latitudinal sampling. We suggest research to make progress on the question of latitudinal trends in larval dispersal.

Population structure of Atlantic Mackerel inferred from RAD‐seq derived SNP markers: effects of sequence clustering parameters and hierarchical SNP selection

Restriction‐site‐associated DNA sequencing (RAD‐seq) and related methods are revolutionizing the field of population genomics in nonmodel organisms as they allow generating an unprecedented number of single nucleotide polymorphisms (SNPs) even when no genomic information is available. Yet, RAD‐seq data analyses rely on assumptions on nature and number of nucleotide variants present in a single locus, the choice of which may lead to an under‐ or overestimated number of SNPs and/or to incorrectly called genotypes. Using the Atlantic mackerel (Scomber scombrus L.) and a close relative, the Atlantic chub mackerel (Scomber colias), as case study, here we explore the sensitivity of population structure inferences to two crucial aspects in RAD‐seq data analysis: the maximum number of mismatches allowed to merge reads into a locus and the relatedness of the individuals used for genotype calling and SNP selection. Our study resolves the population structure of the Atlantic mackerel, but, most importantly, provides insights into the effects of alternative RAD‐seq data analysis strategies on population structure inferences that are directly applicable to other species.

genepopedit: a simple and flexible tool for manipulating multilocus molecular data in R.

Advances in genetic sequencing technologies and techniques have made large, genome‐wide data sets comprised of hundreds or even thousands of individuals and loci the norm rather than the exception even for nonmodel organisms. While such data present new opportunities for evaluating population structure and demographic processes, the large size of these genomic data sets brings new computational challenges for researchers needing to parse, convert and manipulate data often into a variety of software‐specific formats required of genomic analyses. We developed genepopedit as a flexible tool for the manipulation of multilocus molecular data sets. Functionality can be divided among diagnostic‐, manipulation‐, sampling‐, simulation‐, and transformation‐based tools. Metadata from large genomic data sets can be efficiently extracted, without the need to view data in a text‐editing program. genepopedit provides tools to manipulate loci, individual samples and populations included in genomic data sets, in addition to the ability to convert directly to a variety of software formats. Functions are compiled as an R package, which can integrate into existing analysis workflows. Importantly, genepopedit provides a simple yet robust code‐based tool for repeatable genomic data manipulation, which has been proven to be stable for data sets in excess of 200 000 SNPs. The latest version of the package and associated documentation are available on Github (github.com/rystanley/genepopedit).