Jeffrey Robert Guyon

Discovery of a spawning ground reveals diverse migration strategies in Atlantic bluefin tuna (Thunnus thynnus)

Significance We present unequivocal evidence that Atlantic bluefin tuna spawn in the Slope Sea, counter to the current assumption that the Gulf of Mexico and Mediterranean Sea are the exclusive spawning grounds. We also demonstrate that age at maturity of western bluefin tuna is currently overestimated, that this stock exhibits size-structured spawning migrations, and that migratory connections exist between western and eastern Atlantic spawning grounds. Atlantic bluefin tuna support a highly contentious international fishery, and our results present an alternate life history model to inform the management of this species. The implications of our work are most pronounced for western Atlantic bluefin tuna, which have a life history less vulnerable to overexploitation and extinction than is currently estimated. Atlantic bluefin tuna are a symbol of both the conflict between preservationist and utilitarian views of top ocean predators, and the struggle to reach international consensus on the management of migratory species. Currently, Atlantic bluefin tuna are managed as an early-maturing eastern stock, which spawns in the Mediterranean Sea, and a late-maturing western stock, which spawns in the Gulf of Mexico. However, electronic tagging studies show that many bluefin tuna, assumed to be of a mature size, do not visit either spawning ground during the spawning season. Whether these fish are spawning in an alternate location, skip-spawning, or not spawning until an older age affects how vulnerable this species is to anthropogenic stressors including exploitation. We use larval collections to demonstrate a bluefin tuna spawning ground in the Slope Sea, between the Gulf Stream and northeast United States continental shelf. We contend that western Atlantic bluefin tuna have a differential spawning migration, with larger individuals spawning in the Gulf of Mexico, and smaller individuals spawning in the Slope Sea. The current life history model, which assumes only Gulf of Mexico spawning, overestimates age at maturity for the western stock. Furthermore, individual tuna occupy both the Slope Sea and Mediterranean Sea in separate years, contrary to the prevailing view that individuals exhibit complete spawning-site fidelity. Overall, this complexity of spawning migrations questions whether there is complete independence in the dynamics of eastern and western Atlantic bluefin tuna and leads to lower estimates of the vulnerability of this species to exploitation and other anthropogenic stressors.

Recent physical connections may explain weak genetic structure in western Alaskan chum salmon (Oncorhynchus keta) populations

Low genetic divergence at neutral loci among populations is often the result of high levels of contemporary gene flow. Western Alaskan summer-run chum salmon (Oncorhynchus keta) populations demonstrate weak genetic structure, but invoking contemporary gene flow as the basis for the low divergence is problematic because salmon home to their natal streams and some of the populations are thousands of kilometers apart. We used genotypes from microsatellite and single nucleotide polymorphism loci to investigate alternative explanations for the current genetic structure of chum salmon populations from western Alaska. We also estimated current levels of gene flow among Kuskokwim River populations. Our results suggest that weak genetic structure is best explained by physical connections that occurred after the Holocene Thermal Maximum among the Yukon, Kuskokwim, and Nushagak drainages that allowed gene flow to occur among now distant populations.

Potentially adaptive mitochondrial haplotypes as a tool to identify divergent nuclear loci

Summary Genetic tools are commonly used for conservation and management of at-risk species. Individuals are often sampled from mixtures that are composed of many populations, which creates a need to assign individuals to their source. This can be problematic when the genetic divergence among source populations is weak but can be improved using adaptive genetic loci, which should show stronger levels of divergence. We previously reported a signature of positive selection in the mitochondrial-encoded ND5 subunit of complex I in diverse taxa. The respiratory machinery of the mitochondria in salmonids is composed of more than 80 nuclear genes and there is substantial interaction between nuclear and mitochondrial expressed gene products. Recent studies report adaptive variation in mitochondrial function as well as co-evolution between mitochondrial and nuclear genomes. We used potentially adaptive ND5-based mitochondrial haplotypes to identify nuclear loci that would display increased levels of genetic divergence compared to neutral nuclear loci in chum salmon (Oncorhynchus keta). Populations in a geographic area the size of France have previously demonstrated weak genetic divergence even after substantial discovery efforts by multiple laboratories for allozymes, microsatellites and SNPs over the last two decades. We used RAD-based next-generation sequencing and identified a nuclear-encoded subunit of mitochondrial complex I that was a significant FST outlier and 14 other divergent nuclear markers that improve genetic assignment of individuals to their population of origin relative to assignments based on neutral markers alone. This work demonstrates how a known adaptive marker can be leveraged to increase the probability of identifying divergent markers for applied genetics tools that may be biologically linked to it.

Spatio-Temporal Population Genetic Structure and Mating System of Red King Crab (Paralithodes Camtschaticus) in Alaska

Red king crab, Paralithodes camtschaticus Tilesius, 1815, an economically and culturally important species in the state of Alaska, experienced drastic reductions in abundance over large portions of their Alaskan range by 1980. Abundance of crabs in some of the most important historical fishing areas have failed to rebound, some even in the absence of fishing, highlighting the need for additional research to infer genetic structure and reproductive biology of the species that can then be used to inform management efforts. Red king crab samples were collected from eleven locations throughout Alaska ( n = 845 ), of these, six locations were sampled at least one generation apart. Results of this study suggest moderate rates of gene flow within the Gulf of Alaska/Western Alaska region. Levels of genetic differentiation among populations within Southeast Alaska were higher than seen elsewhere, and there was strong evidence of multiple distinct populations. Red king crab in Bristol Bay and in two areas in Southeast Alaska show signs of recent population bottlenecks and shifts in allele frequencies not observed in previous studies that used less polymorphic genetic markers. In addition to population genetic structure analyses, 24 female red king crab and their broods were collected for purposes of inferring mating system. There was no evidence of multiple paternity in any brood. The results of this study support continued management of distinct geographic groups within the Gulf of Alaska/Western Alaska region and suggest that finer-scale management may be beneficial in Southeast Alaska.

Genetic stock identification of overwintering chum salmon in the North Pacific Ocean

Understanding stock and age-specific seasonal migrations of Pacific salmon during ocean residence is essential to both the conservation and management of this important resource. Based upon 11 microsatellites assayed on 265 individuals collected aboard international research surveys during winter 2009, we found substantial differences in the age-specific origin of chum salmon (Oncorhynchus keta) in the North Pacific Ocean. Overall, Asian stocks dominated the collections, however, ocean age 1 fish were primarily of Japanese origin and ocean age 2–3+ fish were predominantly of Russian origin. These results suggest that cohorts of chum salmon stocks migrate nonrandomly in the North Pacific Ocean and adjacent seas.

Genetic stock composition analysis of the chinook salmon (Oncorhynchus tshawytscha) bycatch from the 2016 Bering Sea walleye pollock (Gadus chalcogrammus) trawl fishery

A genetic analysis of samples from the Chinook salmon (Oncorhynchus tshawytscha) bycatch of the 2016 Bering Sea-Aleutian Island (BSAI) trawl fishery for walleye pollock (Gadus chalcogrammus) was undertaken to determine the overall stock composition of the bycatch. Samples were genotyped for 43 single nucleotide polymorphism (SNP) DNA markers and results were estimated using the Alaska Department of Fish and Game (ADF&G) SNP baseline. In 2016, genetic samples from the Bering Sea were collected using a systematic random sampling protocol where one out of every 10 Chinook salmon encountered was sampled. Based on the analysis of 1,910 Chinook salmon bycatch samples collected throughout the 2016 BSAI walleye pollock trawl fishery, Coastal Western Alaska and British Columbia regions (34% and 29% respectively) dominated the sample set with smaller contributions from West Coast US (14%), and North Alaska Peninsula (13%) regions. Analysis of temporal groupings within the pollock “A” and “B” seasons revealed changes in stock composition during the course of the year with lower contributions of Coastal Western Alaska and North Alaska Peninsula regions and higher contributions of West Coast US, British Columbia, and NW Gulf of Alaska, regions during the “B” season when compared to the “A” season.

Reply to Safina and Walter et al.: Multiple lines of evidence for size-structured spawning migrations in western Atlantic bluefin tuna

Walter et al. (1) and Safina (2) raise numerous concerns regarding our study (3). Specifically, they question our conclusions that (i) a majority of spawning occurs outside the Gulf of Mexico, (ii) western North Atlantic bluefin tuna mature earlier than currently estimated, and (iii) additional spawning locations and younger age at maturity mean that the western Atlantic bluefin tuna are less vulnerable to anthropogenic impacts, including exploitation.

Genetic stock composition analysis of the Chinook salmon bycatch samples from the 2014 Gulf of Alaska trawl fishery

A genetic analysis of samples from the Chinook salmon (Oncorhynchus tshawytscha) bycatch of the 2014 Gulf of Alaska (GOA) trawl fisheries for walleye pollock (Gadus chalcogrammus), rockfish (Sebastes spp.), and arrowtooth flounder (Atheresthes stomias) was undertaken to determine the stock composition of the sample sets. Samples were genotyped for 43 single nucleotide polymorphism (SNP) DNA markers and results were estimated using the Alaska Department of Fish and Game (ADF&G) SNP baseline. In 2014, genetic samples were collected from Chinook salmon taken in the bycatch of the Gulf of Alaska (GOA) pollock trawl fisheries using a simple random sample protocol with trip being the primary unit. This is the first year for this sampling protocol and resulted in the largest available genetic sample set to date with 10.7% of the salmon bycatch successfully genotyped. Based on the analysis of 1,163 Chinook salmon bycatch samples, British Columbia (43%), West Coast U.S. (35%), Coastal Southeast Alaska (16%), and Northwest Gulf of Alaska stocks (5%) comprised the largest stock groups. Weighting the available sample sets to the total bycatch by season and statistical area did not appreciably change the overall stock composition. In 2014, genetic samples from the bycatch of the rockfish catcher vessel (CV) fishery in the central GOA were collected by the fishing industry using a census sampling protocol where every Chinook salmon encountered was sampled. Based on the genotyping of 398 Chinook salmon bycatch samples collected from the 2014 GOA rockfish CV trawl fishery in NMFS Statistical Areas 620 and 630, West Coast U.S. stocks (WA/OR/CA) represented the largest stock grouping (72%) with smaller contributions from British Columbia (17%), Coastal Southeast Alaska (7%), and Northwest GOA (3%) stocks. Based on the genotyping of 404 Chinook salmon bycatch samples collected throughout the 2014 GOA arrowtooth flounder trawl fishery from the catcher-processors (CP) FV Vaerdal and FV US C4 GOA Chinook Genetics Rpt APRIL 2016

Genetic stock composition analysis of the Chinook salmon bycatch from the 2014 Bering Sea walleye pollock (Gadus chalcogrammus) trawl fishery

A genetic analysis of samples from the Chinook salmon (Oncorhynchus tshawytscha) bycatch of the 2015 Bering Sea-Aleutian Island (BSAI) trawl fishery for walleye pollock (Gadus chalcogrammus) was undertaken to determine the overall stock composition of the bycatch. Samples were genotyped for 43 single nucleotide polymorphism (SNP) DNA markers and results were estimated using the Alaska Department of Fish and Game (ADF&G) SNP baseline. In 2015, genetic samples from the Bering Sea were collected using a systematic random sampling protocol where one out of every 10 Chinook salmon encountered was sampled. Based on the analysis of 1,757 Chinook salmon bycatch samples collected throughout the 2015 BSAI walleye pollock trawl fishery, Coastal Western Alaska stocks dominated the sample set (40%) with smaller contributions from British Columbia (22%), West Coast U.S. (WA/OR/CA) (15%), and North Alaska Peninsula (11%) stocks. Analysis of temporal groupings within the pollock “A” and “B” seasons revealed changes in stock composition during the course of the year with lower contributions of Coastal Western Alaska, North Alaska Peninsula, and Upper Yukon stocks and higher contributions of West Coast U.S. (WA/OR/CA), British Columbia, NW Gulf of Alaska, and Coastal Southeast Alaska stocks during the “B” season.

Genetic stock composition analysis of Chinook salmon bycatch samples from the rockfish and arrowtooth flounder 2013 Gulf of Alaska trawl fisheries and the Gulf of Alaska salmon excluder device test

A genetic analysis of samples from the Chinook salmon (Oncorhynchus tshawytscha) bycatch of the 2013 Gulf of Alaska (GOA) trawl fisheries for Pacific rockfish (Sebastes spp.) and arrowtooth (Atheresthes stomias) flounder was undertaken to determine the stock composition of the sample sets. Samples were genotyped for 43 single nucleotide polymorphism (SNP) DNA markers and results were estimated using the Alaska Department of Fish and Game (ADF&G) SNP baseline. In 2013, genetic samples from the bycatch of the GOA rockfish fishery were collected by the fishing industry using a census sampling protocol where every Chinook salmon encountered was sampled. Based on the analysis of 2,029 Chinook salmon bycatch samples collected throughout the 2013 GOA rockfish trawl fishery, West Coast U.S. stocks (WA/OR/CA) represented the largest stock grouping (60%) with smaller contributions from British Columbia (31%), Coastal Southeast Alaska (6%), and Northwest GOA (2%) stocks. Genetic samples were also collected from Chinook salmon taken in the bycatch of the 2013 GOA arrowtooth flounder trawl fisheries. Those samples were collected opportunistically from a single vessel; consequently, the resulting stock composition estimates should be considered as stock compositions of the sample set rather than a representative composition of the overall bycatch. Based on the analysis of 279 Chinook salmon bycatch samples, West Coast U.S. (43%), British Columbia (39%), Coastal Southeast Alaska (14%), and Northwest GOA (3%) stocks comprised the largest stock groups. We also produced a stock composition estimate of Chinook salmon from a single test haul of the salmon excluder device performed in April 2013 in an area near Kodiak Island in Shelikof Strait. Stock composition results showed that the majority of those 95 Chinook salmon originated from West Coast U.S. (79%), British Columbia (17%), and Coastal Southeast Alaska (3%) stocks.