Genetic Analysis Reveals Climate Exposure and Conservation Opportunities for a Vulnerable Life History in Steelhead (Oncorhynchus mykiss)

The loss of intraspecific diversity is a hidden crisis that threatens to disrupt ecological processes and ecosystem services, diminishing economic, subsistence, and cultural benefits to human communities. Conserving this diversity requires a deeper understanding of its evolutionary underpinnings and the ecological conditions necessary for its persistence amid rapid environmental change. Here, we integrate evolutionary principles and empirical evidence from recently developed genetic assays to examine the maintenance of run timing diversity within steelhead (Oncorhynchus mykiss), a widely distributed anadromous salmonid with distinct summer and winter adult migration timings. Using a GREB1L-based genetic assay, we analyzed nearly 2000 juvenile samples from the North Umpqua River, Oregon, USA to map watershed-scale distributions of run timing genotypes alongside climate-driven stream warming patterns. We found that summer-run genotypes dominate only in habitats located above seasonally passable barriers, such as natural waterfalls, that restrict or prevent passage by adult winter-run steelhead. This pattern supports the hypothesis that exclusive access to habitat provides a critical fitness advantage that compensates for the costs associated with summer run timing. Temperature modeling further revealed that habitats currently exclusive to summer-run steelhead are already thermally stressful and are projected to become increasingly so under end-of-century climate scenarios, reducing the quality of critical summer-run steelhead habitat. Because the persistence of summer-run steelhead under climate change depends on access to exclusive habitat of sufficient quality, we propose strategies to establish or maintain habitat exclusivity in more climate-resilient areas within the basin while minimizing impacts on winter-run steelhead and other anadromous species. More broadly, our study demonstrates how understanding the genetic basis of run timing and the fitness trade-offs associated with different life histories can inform the conservation of intraspecific diversity in migratory fish.