Tidal gradients, fine-scale homing and a potential cryptic ecotype of wild spawning pink salmon (Oncorhynchus gorbuscha).

The homing behaviour of salmon is a remarkable natural phenomenon, critical for shaping the ecology and evolution of populations yet the spatial scale at which it occurs is poorly understood. This study investigated the spatial scale and mechanisms driving homing as depicted by spawning site-choice behaviour in pink salmon (Oncorhynchus gorbuscha) in Prince William Sound, Alaska. Molecular pedigree analyses of over 30,000 adult spawners in four streams revealed that pink salmon exhibit fine-scale site fidelity within a stream, returning to within <100 m of their parents. Homing behaviours were driven in part by a salinity gradient between intertidal and freshwater environments, with individuals incubated in freshwater environments more than twice as likely to spawn upstream of tidal influence than those incubated in the intertidal. Our findings challenge the traditional view that pink salmon populations are genetically and phenotypically homogenous due to their short freshwater residency as juveniles and high rates of dispersal as returning adults (i.e. straying). This study has important implications for rates of inbreeding, local adaptation and gene flow within populations, and is particularly relevant to the management of salmon hatcheries, given the high incidence of hatchery-origin pink salmon, reared in freshwater hatchery environments, that stray into wild populations of Prince William Sound.

Genomic evidence for domestication selection in three hatchery populations of Chinook salmon, Oncorhynchus tshawytscha.

Fish hatcheries are widely used to enhance fisheries and supplement declining wild populations. However, substantial evidence suggests that hatchery fish are subject to differential selection pressures compared to their wild counterparts. Domestication selection, or adaptation to the hatchery environment, poses a risk to wild populations if traits specific to success in the hatchery environment have a genetic component and there is subsequent introgression between hatchery and wild fish. Few studies have investigated domestication selection in hatcheries on a genomic level, and even fewer have done so in parallel across multiple hatchery-wild population pairs. In this study, we used low-coverage whole-genome sequencing to investigate signals of domestication selection in three separate hatchery populations of Chinook salmon, Oncorhynchus tshawytscha, after approximately seven generations of divergence from their corresponding wild progenitor populations. We sequenced 192 individuals from populations across Southeast Alaska and estimated genotype likelihoods at over six million loci. We discovered a total of 14 outlier peaks displaying high genetic differentiation (F ST) between hatchery-wild pairs, although no peaks were shared across the three comparisons. Peaks were small (53 kb on average) and often displayed elevated absolute genetic divergence (D xy) and linkage disequilibrium, suggesting some level of domestication selection has occurred. Our study provides evidence that domestication selection can lead to genetic differences between hatchery and wild populations in only a few generations. Additionally, our data suggest that population-specific adaptation to hatchery environments likely occurs through different genetic pathways, even for populations with similar standing genetic variation. These results highlight the need to collect paired genotype-phenotype data to understand how domestication may be affecting fitness and to identify potential management practices that may mitigate genetic risks despite multiple pathways of domestication.

Reliability of trans-generational genetic mark-recapture (tGMR) for enumerating Pacific salmon.

As Pacific salmon (Oncorhynchus spp.) decline across much of their range, it is imperative to further develop minimally invasive tools to quantify population abundance. One such advancement, trans-generational genetic mark-recapture (tGMR), uses parentage analysis to estimate the size of wild populations. Our study examined the precision and accuracy of tGMR through a comparison to a traditional mark-recapture estimate for Chilkat River Chinook salmon (O. tshawytscha) in Southeast Alaska. We examined how adult sampling location and timing impact tGMR by comparing estimates derived using samples collected in the lower river mainstem to those using samples obtained in upriver spawning tributaries. Results indicated that tGMR estimates using a representative sample of mainstem adults were most concordant with, and 3% more precise than, the traditional mark-recapture estimate for this stock. Importantly, the timing and location of adult sampling were found to impact abundance estimates, depending on what proportion of the population dies or moves to unsampled areas between downriver and upriver sampling events. Additionally, we identified potential sources of bias in tGMR arising from violations of key assumptions using a novel individual-based modeling framework, parameterized with empirical values from the Chilkat River. Simulations demonstrated that increased reproductive success and sampling selectivity of older, larger individuals, introduced negative bias into tGMR estimates. Our individual-based model offers a customizable and accessible method to identify and quantify these biases in tGMR applications (https://github.com/swrosenbaum/tGMR_simulations). We underscore the critical role of system-specific sampling design considerations in ensuring the precision and accuracy of tGMR projects. This study validates tGMR as a potentially useful tool for improved population enumeration in semelparous species.

Reduced relative fitness in hatchery-origin Pink Salmon in two streams in Prince William Sound, Alaska.

Previous studies generally report that hatchery-origin Pacific Salmon (Oncorhynchus spp.) have lower relative reproductive success (RRS) than their natural-origin counterparts. We estimated the RRS of Pink Salmon (O. gorbuscha) in Prince William Sound (PWS), Alaska using incomplete pedigrees. In contrast to other RRS studies, Pink Salmon have a short freshwater life history, freshwater habitats in PWS are largely unaltered by development, and sampling was conducted without the aid of dams or weirs resulting in incomplete sampling of spawning individuals. Pink Salmon released from large-scale hatchery programs in PWS have interacted with wild populations for more than 15 generations. Hatchery populations were established from PWS populations but have subsequently been managed as separate broodstocks. Gene flow is primarily directional, from hatchery strays to wild populations. We used genetic-based parentage analysis to estimate the RRS of a single generation of stray hatchery-origin Pink Salmon in two streams, and across the odd- and even-year lineages. Despite incomplete sampling, we assigned 1745 offspring to at least one parent. Reproductive success (RS), measured as sampled adult offspring that returned to their natal stream, was significantly lower for hatchery- vs. natural-origin parents in both lineages, with RRS ranging from 0.03 to 0.47 for females and 0.05 to 0.86 for males. Generalized linear modeling for the even-year lineage indicated that RRS was lower for hatchery-origin fish, ranging from 0.42 to 0.60, after accounting for sample date (run timing), sample location within the stream, and fish length. Our results strongly suggest that hatchery-origin strays have lower fitness in the wild. The consequences of reduced RRS on wild productivity depend on whether the mechanisms underlying reduced RRS are environmentally driven, and likely ephemeral, or genetically driven, and likely persistent across generations.