Project: Collaborative Proposal: Selection and Genetic Succession in the Intertidal -- Population Genomics of Pisaster ochraceus During a Wasting Disease Outbreak and its Aftermath

NSF abstract:

This project seeks to understand the outcomes of predator-disease dynamics by exploring a recent pandemic that decimated 90% of ochre sea stars (Pisaster ochraceus) in the eastern North Pacific in 2013. The research team will explore how recovery may depend upon often difficult-to-see processes such as the interplay of migration and natural selection in marine species. While the population of sea stars is currently rebounding due to several years of unusually high recruitment, the sea star wasting disease continues to persist at low levels. This project aims to determine the genetic consequences of the pandemic and subsequent recovery. The team will determine whether the majority of susceptible sea stars have died and identify possible refuges where susceptible sea stars survived. They will examine the potential for heritable variation in resistance to this disease in order to assess whether the new recruits are tolerant or susceptible to wasting. Resolving these issues will enable predictions about the trajectory of their recovery and the potential responses to future large scale disease outbreaks. Research findings will be shared with resource managers and scientists at a collaborative workshop that will focus on state-of-the-art methods to advance research on marine diseases. The public will have the opportunity to learn more about sea star wasting disease through a partnership with the UCSC Seymour Marine Discovery Center and can track the incidence of disease using an online interactive map available at www.seastarwasting.org. Results will be incorporated into professional development for teachers with CalTeach and adapted for teaching materials up to college-level. This project will train diverse early career scientists - undergraduates, graduates, and a postdoctoral scholar - in integration of ecological and genomic methods.

Understanding the consequences of large-scale pandemics in the broader contexts of geographic heterogeneity and chronic changes in ocean pH and temperature is an emerging contemporary issue. This project employs long-term characterization of population dynamics and genetic consequences of a sea star wasting disease (SSWD) outbreak, which caused median 90% mortality in Pisaster ochraceus populations in the northeastern Pacific, to estimate potential long-term consequences for the species. While the largest recorded influx of new recruits occurred in 2014-2016, it is unknown where they originated from, whether recruits and surviving adults remained susceptible to the disease, which persisted at low levels, and for how long these dynamics might continue. This long-term dataset provides a unique opportunity for exploring the short and long term repercussions of such large-scale disease outbreaks and the population dynamics that they precipitate. This project builds on long-term field studies of wild populations to describe host population dynamics, the disease, and genomic diversity. The goal is to discover genetic variation associated with SSWD and to dissociate that variation from population genomic effects attributable to abiotic environmental variation. Objectives are: (1) Census P. ochraceus at 24 sites throughout its range to describe population dynamics, the prevalence of SSWD, and measure abiotic variables. (2) Conduct laboratory experiments coupled with RNAseq analyses to determine loci differentially regulated during exposure to SSWD, temperature, salinity, and pCO2 anomalies. (3) Map ddRAD, RNAseq, and candidate loci under selection to a P. ochraceus genome. (4) Conduct range-wide population genomic analyses for 3 years to assess genetic (SNP) variation among wild-caught specimens with, versus without, SSWD across a geographic mosaic of abiotic variation. (5) Explore links between SSWD and candidate loci, such as EF1A. These analyses will describe the immediate genomic consequences of the disease outbreak, the population dynamics that the outbreak set in motion, and the interplay of factors and mechanisms - such as disease, temperature, migration, selection - that affected these changes. The results will advance understanding of general processes and interactions that shape population genomic structure in coastal ecosystems, providing resources to inform future research and applications in design of management strategies for coastal living resources.

Proposal abstract

Extreme disturbances are expected to increase in frequency and intensity with climate change; their consequences for marine species will depend upon the often enigmatic interplay of dispersal and selection (and drift). This project seeks to understand the population and genomic consequences of a decimating epizootic of the sea star Pisaster ochraceus. Existing collections, which immediately preceded and followed the outbreak and documented >90% mortality of adults and massive subsequent recruitment, will be coupled with continuing annual surveys and population genomic, transcriptomic, and candidate locus analyses. The project aims to determine the extent to which this disease outbreak may (or may not) lead to long-term changes in the frequencies of alleles associated with survival of SSWD.

Understanding the consequences of large perturbations set against a backdrop of geographic heterogeneity and gradual environmental change is an emerging contemporary issue. It requires long-term characterization of population dynamics, genetic consequences, and future implications. In 2013, sea star wasting disease (SSWD) swept through P. ochraceus populations in the northeastern Pacific. We captured this epizootic in long-term ecological-genetic studies, which documented median 90% mortality coast-wide (site-specific rates 51–96%). In the aftermath of the initial outbreak, we quantified the largest influx of new recruitments on record. The disease currently persists at low-levels among surviving populations, and recruitment continues to be above average. Given heterogeneity in the environment and in mortality rates, and because 2013 recruits may have been spawned by adults pre-outbreak, but 2014-to-current recruits are progeny of adults that survived, the genomic consequences of the outbreak and the implications for future population and disease dynamics are uncertain.

This project builds on long-term field studies of wild populations of P. ochraceus to describe population dynamics, the disease, and genomic diversity. Goals are to discover genetic variation associated with SSWD and to dissociate that variation from population genomic effects attributable to abiotic environmental variation. Objectives are: (1) Census P. ochraceus at 24 sites throughout its range to describe population dynamics, the prevalence of SSWD, and measure abiotic variables. (2) Conduct laboratory experiments coupled with RNAseq analyses to determine loci differentially regulated during exposure to SSWD, temperature, salinity, and pCO2 anomalies. (3) Map ddRAD, RNAseq, and candidate loci under selection to a P. ochraceus genome. (4) Conduct range-wide population genomic analyses for 3 years, including intensive study of a focal region, in which we will assess genetic (RAD) variation among wild-caught specimens with versus without SSWD and experiencing the geographic mosaic of abiotic variation. (5) Explore links between SSWD and candidate loci, such as EF1A.

Preliminary results are consistent with an association between SSWD, very high mortality (90%), and differential susceptibility of P. ochraceus linked to variation in ddRAD markers, expression of RNAseq loci, and overdominance at a candidate locus (EF1A). RAD analyses show site-specific differences between P. ochraceus adults despite high gene flow, and while intertidal juveniles and adults were selected by SSWD in 2013, the subsequent pulse of new recruits was most genetically similar to the pre-outbreak population. The consequences of the SSWD outbreak are still unfurling in a dynamic eco-evolutionary landscape.

Research mentoring

This project trains a postdoc, 3 graduate students, >= 6 undergraduates. The postdoc and graduates will be cross-trained in field, lab, and genomics. Undergraduates will participate in field and laboratory research, have opportunities for internships, and be involved in outreach activities addressing environmental change. UCM and UCSC are designated Hispanic Serving Institutions. Teaching. Collaboration with the CalTeach program at UC Merced, lab research experience for high school students at Cornell, and an interactive web-based instructional exercise at UCSC will draw upon the iconic natures of Pisaster, the rocky intertidal, and keystone predators in education, policy, and management, interweaving project outcomes. Public understanding. Outreach efforts will target general public and marine resource managers using a website and interactive map for tracking sea star wasting (www.seastarwasting.org). Scientific understanding. An end-of-project workshop will host several groups working on different aspects of SSWD and its consequences.