About the Blog Author: Dr. Tasha Thompson is a conservation geneticist and post-doctoral research associate at Michigan State University in the lab of Dr. Mariah Meek. She works on the genetic and evolutionary basis of adaptive variation in Pacific salmon and applications for conservation. [Note: The following recounts my personal experiences working on salmon run-timing genetics and the perspective presented is solely my own. For additional discussion of this work, please see the blog post by my coauthor Devon Pearse – Behind the Science: Implications of Large-Effect Loci for Conservation]
I began working on Chinook salmon run-timing genetics in 2015 as a first year graduate student at the University of California-Davis. A more senior graduate student, Dan Prince, was already leading a study that had discovered the genetic and evolutionary basis of Chinook run-timing and, ignorant new grad student that I was, I briefly feared this topic might already be played out. I had no idea what a wild ride I was in for between that first year and the completion of the review this blog post accompanies.
Run-timing (i.e., the time of year salmon migrate back up their natal river to spawn after multiple years in the ocean) is a critical trait for a multitude of reasons. For the salmon, the season of return is essential for accessing specialized spawning habitat at optimum times. For example, spring-run Chinook salmon typically spawn in higher reaches of the watershed and slightly earlier than fall-run Chinook salmon due to differences in temperature and flow conditions between the seasons. This also results in early- and late-returners transporting rich marine nutrients into different areas of the watershed (salmon die after spawning, fertilizing the local ecosystem). For indigenous tribes of the Pacific Northwest, spring-run Chinook salmon presented the first major food source after the winter and remain foundational to cultural and spiritual life.
The genetic and evolutionary basis of run-timing has been of scientific interest for a long time. Early studies based on allozymes and microsatellites reported that, in most coastal rivers, early- and late-returners within the same watershed were more closely related to each other than to their life-history counterparts in other watersheds. This was interpreted to mean that early run-timing had evolved independently many times and could re-evolve again from late-run populations on relatively short timescales. It was also assumed that run-timing was highly polygenic, akin to many other traits such as human height.
The easily-evolvable, highly polygenic paradigm was important from a conservation perspective because early-returners have been disproportionately affected by human activities such as dam construction and habitat degradation. Most early-returning populations are on the brink or have already been extirpated, even in watersheds where late-returners are still abundant. If the above paradigm was true, even strong selection against and extirpation of the early-run phenotype would not lead to complete loss of early-return alleles. Thus, the loss of early returners would be readily reversible if habitat was restored, and long-term evolutionary consequences would likely be minimal.
In 2017, I was part of a study that challenged the paradigm: we found run-timing was controlled by a single locus of very large effect and early-run alleles had a monophyletic origin (Prince et al., 2017). We also found that early-return alleles were co-dominant and not maintained as standing variation in populations that lacked the early-run phenotype (either naturally or through anthropogenic extirpation)–the loss of early returners is followed by loss of the ability to restore them (Thompson et al. 2019). Therefore, both the present and future of early-returners depends on the continuous maintenance of habitat that can support them in viable numbers.
Reactions to our findings were strong, and not always positive. The very first time I spoke at a conference, the moderator grabbed my arm as I approached the podium, leaned in, and whispered, “I hope this isn’t too controversial.” That was just the beginning, and downright cordial compared to some of what ensued. The reasons behind the controversy are complex, and I’m sure I don’t understand them in full. Natural skepticism of unexpected results may have been heightened by both the newness of the methods (many geneticists were still getting comfortable working with next-gen data) and the newness of the lab that led the work. However, it was the potential conservation implications that elicited the strongest feelings on all sides. Communication and egos also played prominent roles—perhaps with a different cast of characters the saga would have been less dramatic.
Over the next few years, other labs conducted their own studies, and soon the salmon genetics community was awash in data. However, the data was drawn from myriad populations that had been phenotyped in diverse ways using a variety of genotyping methods and several different reference genomes. Wading through it was not a simple task. Coming to agreement on what it meant for conservation was even more challenging. However, it inspired passionate ideas on many fronts.
There was a great need for consensus building, and Robin Waples, Mike Ford, and Krista Nichols of the NOAA Northwest Fisheries Science Center stepped up to the plate. In early 2020, on the cusp of the pandemic, representatives from the labs working on Chinook run-timing genetics, as well as a few government policy folks, met in Seattle for a two day workshop to hash through the data. It was highly productive and only occasionally tense. Afterwards we put together a behemoth of a report (Ford et al. 2020) summarizing the data available to date and points of agreement and disagreement.
The next goal was to refine and distill the report into the more succinct, but still comprehensive, peer-reviewed publication this blog post accompanies. Robin Waples took the lead and assigned sections of the manuscript to small working groups. I, along with Mike Ford, was tasked with leading the empirical data section. An ambitious but seemingly plausible timeline was set to finalize the manuscript by September 2020.
Clearly it took a bit longer than proposed. I certainly contributed to the delay, some of which was due to interesting events in my own life. I’d started a new post-doc position, I was displaced for weeks when my house almost burned down in a wildfire, I got married, and I gave birth to twins. Like many families in the pandemic, childcare was sporadic or nonexistent much of the time, and a substantial portion of my work was accomplished after the babies were put to bed each night. The many, many rounds of editing also stretched the timeline—as noted already, Chinook run-timing inspires great passion.
I think, though, that the manuscript ultimately benefited from the delay. Several studies with valuable data were published in the interim that wouldn’t have been thoroughly discussed otherwise. Furthermore, major conservation decisions regarding spring-run Chinook were made as the manuscript neared completion. The discussion of those decisions became an important part of the paper.
The section dealing with the conservation implications and recent policy decisions was the last part to be finalized and, not surprisingly, proved to be the crux of the paper. While the wording throughout the review was heavily scrutinized, the conservation implications section took the scrutiny to a new level. Blood, sweat, and tears went into reaching consensus on that section. Nearly every word was fought for. A few low blows were made. I’m pretty sure Robin Waples and Mike Ford were ready to tear their hair out (or tear up the whole manuscript and be done with it) in their effort to get the other coauthors to come to agreement.
Yet, agreement was eventually reached, on that section and the rest of the manuscript. Significantly, I believe we accomplished consensus without a watering-down of substance. Each word is meaningful and intended and, in my view, well worth all the trouble. I hope you enjoy our review.
Prince DJ, O’Rourke SM, Thompson TQ, Ali OA, Lyman HS, Saglam IK, Hotaling TJ, Spidle AP, Miller MR. 2017. The evolutionary basis of premature migration in Pacific salmon highlights the utility of genomics for informing conservation. Sci Adv. 3:e1603198.
Thompson TQ, Bellinger MR, O’Rourke SM, Prince DJ, Stevenson AE, Rodrigues AT, Sloat MR, Speller CF, Yang DY, Butler VL, et al. 2019. Anthropogenic habitat alteration leads to rapid loss of adaptive variation and restoration potential in wild salmon populations. Proc Natl Acad Sci USA. 116:177–186.
Ford MD, Nichols KM, Waples RS, et al. 2020. Reviewing and synthesizing the state of the science regarding associations between adult run timing and specific genotypes in Chinook salmon and steelhead: report of a workshop held in Seattle, Washington, 27–28 February 2020. NWFSC processed report 2020-06. Available from: https://repository.library.noaa.gov/view/noaa/24980
Waples RS, Ford, MJ, Nichols, K, Kardos M, Myers J, Thompson TQ, Anderson EC, Koch, IJ, McKinney G, Miller MR, Naish K, Narum SR, O’Malley KG, Pearse, D, Pess, GR, Quinn, TP, Seamons, TR, Spidle, A, Warheit, K, Willis, SC. 2022. Implications of large-effect loci for conservation: a review and case study with Pacific salmon. Journal of Heredity. esab069