skip to main content


Title: Influence of environmental conditions at spawning sites and migration routes on adaptive variation and population connectivity in Chinook salmon
Abstract

Many species that undergo long breeding migrations, such as anadromous fishes, face highly heterogeneous environments along their migration corridors and at their spawning sites. These environmental challenges encountered at different life stages may act as strong selective pressures and drive local adaptation. However, the relative influence of environmental conditions along the migration corridor compared with the conditions at spawning sites on driving selection is still unknown. In this study, we performed genome–environment associations (GEA) to understand the relationship between landscape and environmental conditions driving selection in seven populations of the anadromous Chinook salmon (Oncorhynchus tshawytscha)—a species of important economic, social, cultural, and ecological value—in the Columbia River basin. We extracted environmental variables for the shared migration corridors and at distinct spawning sites for each population, and used a Pool‐seq approach to perform whole genome resequencing. Bayesian and univariate GEA tests with migration‐specific and spawning site‐specific environmental variables indicated many more candidate SNPs associated with environmental conditions at the migration corridor compared with spawning sites. Specifically, temperature, precipitation, terrain roughness, and elevation variables of the migration corridor were the most significant drivers of environmental selection. Additional analyses of neutral loci revealed two distinct clusters representing populations from different geographic regions of the drainage that also exhibit differences in adult migration timing (summer vs. fall). Tests for genomic regions under selection revealed a strong peak on chromosome 28, corresponding to the GREB1L/ROCK1 region that has been identified previously in salmonids as a region associated with adult migration timing. Our results show that environmental variation experienced throughout migration corridors imposed a greater selective pressure on Chinook salmon than environmental conditions at spawning sites.

 
more » « less
Award ID(s):
1757324
NSF-PAR ID:
10371032
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
11
Issue:
23
ISSN:
2045-7758
Format(s):
Medium: X Size: p. 16890-16908
Size(s):
["p. 16890-16908"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Fujiwara, Masami (Ed.)
    The migration timing of Pacific salmon in the Columbia River basin is subject to multiple influences related to climate, human water resource management, and lagged effects such as oceanic conditions. We apply an information theory-based approach to analyze drivers of adult Chinook salmon migration within the spring and fall spawning seasons and between years based on salmon counts at dams along the Columbia and Snake Rivers. Time-lagged mutual information and information decomposition measures, which characterize lagged and nonlinear dependencies as reductions in uncertainty, are used to detect interactions between salmon counts and lagged streamflows, air and water temperatures, precipitation, snowpack, climate indices and downstream salmon counts. At a daily timescale, these interdependencies reflect migration timing and show differences between fall and spring run salmon, while dependencies based on variables at an annual resolution reflect long-term predictability. We also highlight several types of joint dependencies where predictability of salmon counts depends on the knowledge of multiple lagged sources. This study illustrates how co-varying human and natural drivers could propagate to influence salmon migration timing or overall returns, and how nonlinear types of dependencies between variables enhance predictability of a target. This information-based framework is broadly applicable to assess driving factors in other types of complex water resources systems or species life cycles. 
    more » « less
  2. Abstract

    The timing of life history events in many plants and animals depends on the seasonal fluctuations of specific environmental conditions. Climate change is altering environmental regimes and disrupting natural cycles and patterns across communities. Anadromous fishes that migrate between marine and freshwater habitats to spawn are particularly sensitive to shifting environmental conditions and thus are vulnerable to the effects of climate change. However, for many anadromous fish species the specific environmental mechanisms driving migration and spawning patterns are not well understood. In this study, we investigated the upstream spawning migrations of river herringAlosaspp. in 12 coastal Massachusetts streams. By analyzing long‐term data sets (8–28 years) of daily fish counts, we determined the local influence of environmental factors on daily migration patterns and compared seasonal run dynamics and environmental regimes among streams. Our results suggest that water temperature was the most consistent predictor of both daily river herring presence–absence and abundance during migration. We found inconsistent effects of streamflow and lunar phase, likely due to the anthropogenic manipulation of flow and connectivity in different systems. Geographic patterns in run dynamics and thermal regimes suggest that the more northerly runs in this region are relatively vulnerable to climate change due to migration occurring later in the spring season, at warmer water temperatures that approach thermal maxima, and during a narrower temporal window compared to southern runs. The phenology of river herring and their reliance on seasonal temperature patterns indicate that populations of these species may benefit from management practices that reduce within‐stream anthropogenic water temperature manipulations and maintain coolwater thermal refugia.

     
    more » « less
  3. Salmonids are ideal models as many species follow a distinct developmental program from demersal eggs and a large yolk sac to hatching at an advanced developmental stage. Further, these economically important teleosts inhabit both marine- and freshwaters and experience diverse light environments during their life histories. At a genome level, salmonids have undergone a salmonid-specific fourth whole genome duplication event (Ss4R) compared to other teleosts that are already more genetically diverse compared to many non-teleost vertebrates. Thus, salmonids display phenotypically plastic visual systems that appear to be closely related to their anadromous migration patterns. This is most likely due to a complex interplay between their larger, more gene-rich genomes and broad spectrally enriched habitats; however, the molecular basis and functional consequences for such diversity is not fully understood. This study used advances in genome sequencing to identify the repertoire and genome organization of visual opsin genes (those primarily expressed in retinal photoreceptors) from six different salmonids [Atlantic salmon ( Salmo salar ), brown trout ( Salmo trutta ), Chinook salmon ( Oncorhynchus tshawytcha ), coho salmon ( Oncorhynchus kisutch ), rainbow trout ( Oncorhynchus mykiss ), and sockeye salmon ( Oncorhynchus nerka )] compared to the northern pike ( Esox lucius ), a closely related non-salmonid species. Results identified multiple orthologues for all five visual opsin classes, except for presence of a single short-wavelength-sensitive-2 opsin gene. Several visual opsin genes were not retained after the Ss4R duplication event, which is consistent with the concept of salmonid rediploidization. Developmentally, transcriptomic analyzes of Atlantic salmon revealed differential expression within each opsin class, with two of the long-wavelength-sensitive opsins not being expressed before first feeding. Also, early opsin expression in the retina was located centrally, expanding dorsally and ventrally as eye development progressed, with rod opsin being the dominant visual opsin post-hatching. Modeling by spectral tuning analysis and atomistic molecular simulation, predicted the greatest variation in the spectral peak of absorbance to be within the Rh2 class, with a ∼40 nm difference in λ max values between the four medium-wavelength-sensitive photopigments. Overall, it appears that opsin duplication and expression, and their respective spectral tuning profiles, evolved to maximize specialist color vision throughout an anadromous lifecycle, with some visual opsin genes being lost to tailor marine-based vision. 
    more » « less
  4. Abstract

    The timing of biological events in plants and animals, such as migration and reproduction, is shifting due to climate change. Anadromous fishes are particularly susceptible to these shifts as they are subject to strong seasonal cycles when transitioning between marine and freshwater habitats to spawn. We used linear models to determine the extent of phenological shifts in adult AlewifeAlosa pseudoharengusas they migrated from ocean to freshwater environments during spring to spawn at 12 sites along the northeastern USA. We also evaluated broadscale oceanic and atmospheric drivers that trigger their movements from offshore to inland habitats, including sea surface temperature, North Atlantic Oscillation index, and Gulf Stream index. Run timing metrics of initiation, median (an indicator of peak run timing), end, and duration were found to vary among sites. Although most sites showed negligible shifts towards earlier timing, statistically significant changes were detected in three systems. Overall, winter sea surface temperature, spring and fall transition dates, and annual run size were the strongest predictors of run initiation and median dates, while a combination of within‐season and seasonal‐lag effects influenced run end and duration timing. Disparate results observed across the 12 spawning runs suggest that regional environmental processes were not consistent drivers of phenology and local environmental and ecological conditions may be more important. Additional years of data to extend time series and monitoring of Alewife timing and movements in nearshore habitats may provide important information about staging behaviors just before adults transition between ocean and freshwater habitats.

     
    more » « less
  5. Abstract Context

    Processes that shape genomic and ecological divergence can reveal important evolutionary dynamics to inform the conservation of threatened species.Fontaineais a genus of rainforest shrubs and small trees including critically endangered and threatened species restricted to narrow, but complex geographic and ecological regions. Several species ofFontaineaare subject to spatially explicit conditions and experience limited intra-specific gene flow, likely generating genetic differentiation and local adaptation.

    Objectives

    Here, we explored the genetic and ecological mechanisms underlying patterns of diversification in two, closely related threatenedFontaineaspecies. Our aim was to compare spatial patterns of genetic variation between the vulnerableFontainea australis(Southern Fontainea) and critically endangeredF. oraria(Coastal Fontainea), endemic to the heterogeneous subtropical region of central, eastern Australia, where large-scale clearing has severely reduced rainforest habitat to a fraction (< 1%) of its pre-European settlement extent.

    Methods

    We used a set of 10,000 reduced-representation markers to infer genetic relationships and the drivers of spatial genetic variation across the two species. In addition, we employed a combination of univariate and multivariate genome-environment association analysis using a set of topo-climatic variables to explore potential patterns of local adaptation as a factor impacting genomic divergence.

    Results

    Our study revealed that Coastal Fontainea have a close genetic relationship with Southern Fontainea. We showed that isolation by distance has played a key role in their genetic variation, indicating that vicariance can explain the spatial genetic distribution of the two species. Genotype-environment analyses showed a strong association with temperature and topographic features, suggesting adaptation to localised thermal environments. We used a multivariate redundancy analysis to identify a range of putatively adapted loci associated with local environmental conditions.

    Conclusions

    Divergent selection at the local-habitat scale as a result of dispersal limitations and environmental heterogeneity (including physical barriers) are likely contributors to adaptive divergence between the twoFontaineaspecies. Our findings have presented evidence to indicate that Southern and Coastal Fontainea were comprised of distinct genetic groups and ecotypes, that together may form a single species continuum, with further phenotype research suggested to confirm the current species boundaries. Proactive conservation actions, including assisted migration to enhance the resilience of populations lacking stress-tolerant single nucleotide polymorphisms (SNPs) may be required to secure the long-term future of both taxa. This is especially vital for the critically endangered Coastal Fontainea given projections of habitat decline for the species under future climate scenarios.

     
    more » « less