Population structure, genetic connectivity, and adaptation in the Olympia oyster (Ostrea lurida) along the west coast of North America

Abstract

Effective management of threatened and exploited species requires an understanding of both the genetic connectivity among populations and local adaptation. The Olympia oyster ( Ostrea lurida ), patchily distributed from Baja California to the central coast of Canada, has a long history of population declines due to anthropogenic stressors. For such coastal marine species, population structure could follow a continuous isolation‐by‐distance model, contain regional blocks of genetic similarity separated by barriers to gene flow, or be consistent with a null model of no population structure. To distinguish between these hypotheses in O. lurida , 13,424 single nucleotide polymorphisms ( SNP s) were used to characterize rangewide population structure, genetic connectivity, and adaptive divergence. Samples were collected across the species range on the west coast of North America, from southern California to Vancouver Island. A conservative approach for detecting putative loci under selection identified 235 SNP s across 129 GBS loci, which were functionally annotated and analyzed separately from the remaining neutral loci. While strong population structure was observed on a regional scale in both neutral and outlier markers, neutral markers had greater power to detect fine‐scale structure. Geographic regions of reduced gene flow aligned with known marine biogeographic barriers, such as Cape Mendocino, Monterey Bay, and the currents around Cape Flattery. The outlier loci identified as under putative selection included genes involved in developmental regulation, sensory information processing, energy metabolism, immune response, and muscle contraction. These loci are excellent candidates for future research and may provide targets for genetic monitoring programs. Beyond specific applications for restoration and management of the Olympia oyster, this study lends to the growing body of evidence for both population structure and adaptive differentiation across a range of marine species exhibiting the potential for panmixia. Computational notebooks are available to facilitate reproducibility and future open‐sourced research on the population structure of O. lurida .

Temperature and salinity, not acidification, predict near-future larval growth and larval habitat suitability of Olympia oysters in the Salish Sea

“…The presence of reproductive adults in an area implies the presence of suitable habitat for a species, so short PLD and dispersal distance would increase chances that larvae would retain access to such suitable adult habitat. While recent population genetic studies on Olympia oysters suggest high larval exchange at least at scale of the sub-basins within the Salish Sea 54 , 55 , the widespread historical distribution of Olympia oyster beds in the Salish Sea 21 , 56 suggests that adult habitat availability is probably not limiting so high population connectivity may persist even with shorter PLDs. Moreover, shortened PLDs might decrease wastage of larvae as larvae are disproportionately vulnerable and experience exponential decreases in survivorship over time 6 .…”

Standing genetic variation fuels rapid adaptation to ocean acidification

“…Though the mechanisms maintaining such significant levels of genetic variation in natural populations have been historically debated, recent population genomic surveys have begun to elucidate the role of spatially and temporally variable selection pressures in this process 8 . For example, environmental gradients in marine systems can maintain signatures of balanced polymorphisms between populations at multiple, putatively functional loci, even amidst high levels of gene flow 9–12 . While this variation has enabled the persistence of natural populations inhabiting the contemporary and historic regimes of environmental variability, it is unclear whether it will facilitate the magnitude and rate of adaptation necessary for species persistence under the conditions expected as a result of global climate change 13 .…”

Carryover effects of temperature and pCO2 across multiple Olympia oyster populations

“…Another consideration in this study was the genetic composition of test organisms. Ostrea lurida exhibits varying phenotypes among distinct populations (Silliman ), which can influence their sensitivity to environmental stressors (Bible and Sanford , Heare et al. , Bible et al.…”