Anthropogenic habitat alteration leads to rapid loss of adaptive variation and restoration potential in wild salmon populations

Thompson, Tasha Q.; Bellinger, Renee M.; O’Rourke, Sean; Prince, Daniel J.; Stevenson, Alexander E.; Rodrigues, Antonia; Sloat, Matthew R.; Speller, Camilla; Yang, Dongya; Butler, Virginia L.; Banks, Michael; Miller, Michael R.

doi:10.1101/310714

Cited by 40 publications

(68 citation statements)

References 49 publications

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“…Applying modern genetic techniques to ancient tissue is an emerging and powerful tool for understanding historical contexts for conservation, such as verifying population extinctions (Iwamoto, Myers, & Gustafson, ) or loss in diversity (Thompson et al., ). Our work utilized such genetic tools to build upon previous studies that used century‐old salmon cannery data and reported similar declines for multiple species across the Northeast Pacific (Gresh, Lichatowich, & Schoonmaker, ).…”

Section: Discussionmentioning

confidence: 99%

Genetics of century‐old fish scales reveal population patterns of decline

Price

Connors

Candy

et al. 2019

CONSERVATION LETTERS

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Conservation scientists rarely have the information required to understand changes in abundance over more than a few decades, even for important species like Pacific salmon. Such lack of historical information can underestimate the magnitude of decline for depressed populations. We applied genetic tools to a unique collection of 100‐year‐old salmon scales to reveal declines of 56%–99% in wild sockeye populations across Canada's second largest salmon watershed, the Skeena River. These analyses reveal century‐long declines that are much greater than those based on modern era abundance data, which suggested that only 7 of 13 populations declined over the last five decades. Populations of larger‐bodied fish have declined the most in abundance, likely because of size‐selective commercial fisheries. Our findings illustrate how a deep historical perspective can expand our understanding of past abundances to a time before species incurred significant losses from fishing, and help inform conservation for diminished populations.

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Section: Discussionmentioning

confidence: 99%

Genetics of century‐old fish scales reveal population patterns of decline

Price

Connors

Candy

et al. 2019

CONSERVATION LETTERS

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“…The first step to effectively apply genomics data to conservation is to identify the single gene or multigene combinations that underpin the focal trait of interest. In some cases, single large‐effect genes may underlie important traits (Barson et al, ; Hess, Zendt, Matala, & Narum, ; Narum, Genova, Micheletti, & Maass, ; Pearse, Miller, Abadía‐Cardoso, & Garza, ; Prince et al, ; Thompson et al, ). However, the reigning paradigm in quantitative genetics posits that most complex traits are controlled by many genes of small effect (Bernatchez, ; Lynch & Walsh, ; Pavey et al, ).…”

Section: Introductionmentioning

confidence: 99%

Evidence for the genetic basis and epistatic interactions underlying ocean‐ and river‐maturing ecotypes of Pacific Lamprey (Entosphenus tridentatus) returning to the Klamath River, California

et al. 2019

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Surveys of genomic variation have improved our understanding of the relationship between fitness‐related phenotypes and their underlying genetic basis. In some cases, single large‐effect genes have been found to underlie important traits; however, complex traits are expected to be under polygenic control and elucidation of multiple gene interactions may be required to fully understand the genetic basis of the trait. In this study, we investigated the genetic basis of the ocean‐ and river‐maturing ecotypes in anadromous Pacific lamprey (Entosphenus tridentatus). In Pacific lamprey, the ocean‐maturing ecotype is distinguished by advanced maturity of females (e.g., large egg mass) at the onset of freshwater migration relative to immature females of the river‐maturing ecotype. We examined a total of 219 adult Pacific lamprey that were collected at‐entry to the Klamath River over a 12‐month period. Each individual was genotyped at 308 SNPs representing known neutral and adaptive loci and measured at morphological traits, including egg mass as an indicator of ocean‐ and river‐maturing ecotype for females. The two ecotypes did not exhibit genetic structure at 148 neutral loci, indicating that ecotypic diversity exists within a single population. In contrast, we identified the genetic basis of maturation ecotypes in Pacific lamprey as polygenic, involving two unlinked gene regions that have a complex epistatic relationship. Importantly, these gene regions appear to show stronger effects when considered in gene interaction models than if just considered additive, illustrating the importance of considering epistatic effects and gene networks when researching the genetic basis of complex traits in Pacific lamprey and other species.

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“…Though such assessments have progressed toward unraveling complex relationships between fitness‐related traits and underlying genomic architectures in more easily accessible systems (e.g., Pacific salmonids [ Oncorhynchus spp., Salmo spp. ]; Ayllon et al, ; Barson et al, ; Prince et al, ; Thompson et al, ), applications of NGS to large pelagic fishes are just getting started, and recent studies illustrate the utility of genomic methods for resolving spatial patterns of connectivity in pelagic systems. For example, results from early comparisons of traditional markers (e.g., allozymes, mtDNA, microsatellites) in yellowfin tuna ( Thunnus albacares ) from the Atlantic, Pacific, and Indian oceans were either consistent with genetic homogeneity or offered only preliminary evidence for population subdivision (Appleyard, Grewe, Innes, & Ward, ; Dammannagoda, Hurwood, & Mather, ; Díaz‐Jaimes & Uribe‐Alcocer, , ; Ely et al, ; Scoles & Graves, ; Ward, Eiliott, Grewe, Smolenski, & Sea, ; Wu et al, ).…”

Section: Introductionmentioning

confidence: 99%

Genome‐wide SNPs resolve spatiotemporal patterns of connectivity within striped marlin (Kajikia audax), a broadly distributed and highly migratory pelagic species

Mamoozadeh

Graves

McDowell

2019

Evolutionary Applications

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Genomic methodologies offer unprecedented opportunities for statistically robust studies of species broadly distributed in environments conducive to high gene flow, providing valuable information for wildlife conservation and management. Here, we sequence restriction site‐associated DNA to characterize genome‐wide single nucleotide polymorphisms (SNPs) in a broadly distributed and highly migratory large pelagic fish, striped marlin (Kajikia audax). Assessment of over 4,000 SNPs resolved spatiotemporal patterns of genetic connectivity throughout the species range in the Pacific and, for the first time, Indian oceans. Individual‐based cluster analyses identified six genetically distinct populations corresponding with the western Indian, eastern Indian, western South Pacific, and eastern central Pacific oceans, as well as two populations in the North Pacific Ocean (FST = 0.0137–0.0819). FST outlier analyses identified a subset of SNPs (n = 59) putatively under the influence of natural selection and capable of resolving populations separated by comparatively high degrees of genetic differentiation. Temporal collections available for some regions demonstrated the stability of allele frequencies over three to five generations of striped marlin. Relative migration rates reflected lower levels of genetic connectivity between Indian Ocean populations (mR ≤ 0.37) compared with most populations in the Pacific Ocean (mR ≥ 0.57) and highlight the importance of the western South Pacific in facilitating gene flow between ocean basins. Collectively, our results provide novel insights into rangewide population structure for striped marlin and highlight substantial inconsistencies between genetically distinct populations and stocks currently recognized for fisheries management. More broadly, we demonstrate that species capable of long‐distance dispersal in environments lacking obvious physical barriers to movement can display substantial population subdivision that persists over multiple generations and that may be facilitated by both neutral and adaptive processes. Importantly, surveys of genome‐wide markers enable inference of population‐level relationships using sample sizes practical for large pelagic fishes of conservation concern.

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Anthropogenic habitat alteration leads to rapid loss of adaptive variation and restoration potential in wild salmon populations

Cited by 40 publications

References 49 publications

Genetics of century‐old fish scales reveal population patterns of decline

Genetics of century‐old fish scales reveal population patterns of decline

Evidence for the genetic basis and epistatic interactions underlying ocean‐ and river‐maturing ecotypes of Pacific Lamprey (Entosphenus tridentatus) returning to the Klamath River, California

Genome‐wide SNPs resolve spatiotemporal patterns of connectivity within striped marlin (Kajikia audax), a broadly distributed and highly migratory pelagic species

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