Decimation by sea star wasting disease and rapid genetic change in a keystone species, Pisaster ochraceus

Lauren M. Schiebelhut; Jonathan B. Puritz; Michael N Dawson

doi:10.1073/pnas.1800285115

New Research In

Edited by Nancy Knowlton, Smithsonian Institution, Washington, DC, and approved May 14, 2018 (received for review January 10, 2018)

Significance

Opportunities to study microevolution in wild populations are rare and challenging. Annual monitoring allowed us to capture both the prelude to and aftermath of one of the largest marine mass mortality events on record in a keystone marine species. Median mortality of 81% across populations was recorded along with significant allele frequency shifts at multiple loci in the adult population. Shifts were consistent across locations and also occurred in new recruits, with few exceptions. These results indicate a long-term species-wide change in allele frequencies will persist through future generations. Population genomic monitoring, at a time when marine diseases and mass mortalities are on the rise, will be essential for documenting rapid genetic shifts in response to chronic and extreme events.

Abstract

Standing genetic variation enables or restricts a population’s capacity to respond to changing conditions, including the extreme disturbances expected to increase in frequency and intensity with continuing anthropogenic climate change. However, we know little about how populations might respond to extreme events with rapid genetic shifts, or how population dynamics may influence and be influenced by population genomic change. We use a range-wide epizootic, sea star wasting disease, that onset in mid-2013 and caused mass mortality in Pisaster ochraceus to explore how a keystone marine species responded to an extreme perturbation. We integrated field surveys with restriction site-associated DNA sequencing data to (i) describe the population dynamics of mortality and recovery, and (ii) compare allele frequencies in mature P. ochraceus before the disease outbreak with allele frequencies in adults and new juveniles after the outbreak, to identify whether selection may have occurred. We found P. ochraceus suffered 81% mortality in the study region between 2012 and 2015, and experienced a concurrent 74-fold increase in recruitment beginning in late 2013. Comparison of pre- and postoutbreak adults revealed significant allele frequency changes at three loci, which showed consistent changes across the large majority of locations. Allele frequency shifts in juvenile P. ochraceus (spawned from premortality adults) were consistent with those seen in adult survivors. Such parallel shifts suggest detectable signals of selection and highlight the potential for persistence of this change in subsequent generations, which may influence the resilience of this keystone species to future outbreaks.

Footnotes

↵¹To whom correspondence should be addressed. Email: lschiebelhut{at}ucmerced.edu.

Author contributions: L.M.S. and M.ND. designed research; L.M.S. and M.ND. performed research; M.ND. contributed new reagents/analytic tools; L.M.S. and J.B.P. analyzed data; and L.M.S., J.B.P., and M.ND. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the National Center for Biotechnology Information short read archive (accession no. SRP136569). Commented bioinformatics code, raw SNP calls, filtered SNPs, and final haplotype calls are deposited at University of California, Merced Dash (https://doi.org/10.6071/M3WW84).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1800285115/-/DCSupplemental.

Published under the PNAS license.

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