skip to main content


Title: Transcriptomic responses to extreme low salinity among locally adapted populations of Olympia oyster ( Ostrea lurida )
Abstract

The Olympia oyster (Ostrea lurida) is a foundation species inhabiting estuaries along the North American west coast. In California estuaries,O. luridais adapted to local salinity regimes and populations differ in low salinity tolerance. In this study, oysters from three California populations were reared for two generations in a laboratory common garden and subsequently exposed to low salinity seawater. Comparative transcriptomics was then used to understand species‐level responses to hyposmotic stress and population‐level mechanisms underlying divergent salinity tolerances. Gene expression patterns indicate Olympia oysters are sensitive to hyposmotic stress: All populations respond to low salinity by up‐regulating transcripts indicative of protein unfolding,DNAdamage and cell cycle arrest after sub‐lethal exposure. AmongO. luridapopulations, transcriptomic profiles differed constitutively and in response to low salinity. Despite two generations in common‐garden conditions, transcripts encoding apoptosis modulators were constitutively expressed at significantly different levels in the most tolerant population. Expression of cell death regulators may facilitate cell fate decisions when salinity declines. Following low salinity exposure, oysters from the more tolerant population expressed a small number of mRNAs at significantly higher levels than less tolerant populations. Proteins encoded by these transcripts regulate ciliary activity within the mantle cavity and may function to prolong valve closure and reduce mortality in low salinity seawater. Collectively, gene expression patterns suggest sub‐lethal impacts of hyposmotic stress in Olympia oysters are considerable and that even oysters with greater low salinity tolerance may be vulnerable to future freshwater flooding events.

 
more » « less
NSF-PAR ID:
10076884
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
Volume:
27
Issue:
21
ISSN:
0962-1083
Page Range / eLocation ID:
p. 4225-4240
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Inducible prey defences occur when organisms undergo plastic changes in phenotype to reduce predation risk. When predation pressure varies persistently over space or time, such as when predator and prey co‐occur over only part of their biogeographic ranges, prey populations can become locally adapted in their inducible defences. In California estuaries, native Olympia oyster (Ostrea lurida) populations have evolved disparate phenotypic responses to an invasive predator, the Atlantic oyster drill (Urosalpinx cinerea). In this study, oysters from an estuary with drills, and oysters from an estuary without drills, were reared for two generations in a laboratory common garden, and subsequently exposed to cues from Atlantic drills. Comparative proteomics was then used to investigate molecular mechanisms underlying conserved and divergent aspects of their inducible defences. Both populations developed smaller, thicker, and harder shells after drill exposure, and these changes in shell phenotype were associated with upregulation of calcium transport proteins that could influence biomineralization. Inducible defences evolve in part because defended phenotypes incur fitness costs when predation risk is low. Immune proteins were downregulated by both oyster populations after exposure to drills, implying a trade‐off between biomineralization and immune function. Following drill exposure, oysters from the population that co‐occurs with drills grew smaller shells than oysters inhabiting the estuary not yet invaded by the predator. Variation in the response to drills between populations was associated with isoform‐specific protein expression. This trend suggests that a stronger inducible defence response evolved in oysters that co‐occur with drills through modification of an existing mechanism.

     
    more » « less
  2. 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 inO. lurida, 13,424 single nucleotide polymorphisms (SNPs) 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 235SNPs across 129GBSloci, 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 ofO. lurida.

     
    more » « less
  3. Abstract

    The eastern oyster (Crassostrea virginica) is a protandrous hermaphrodite of commercial importance. As with many marine invertebrates, little is known about sex determination and differentiation systems in this species. Such knowledge has important implications not only for understanding the evolution of sex but also for applied questions in aquaculture. In order to examine mechanistic differences in reproductive development between the sexes, we compared the transcriptomes of gonad and mantle tissues from six male and six female oysters. A total of 7675 transcripts were differentially expressed between male and female gonads (3936 and 3739 were upregulated in males and females, respectively). Transcripts identified include those associated with sex in other invertebrate and vertebrate species such asDmrt1,Sox‐30,Bindin,Dpy‐30, andHistone H4in males andFoxl2,Vitellogenin, andBystinin females. GO terms associated with transcripts upregulated in male gonads include protein modification, reproductive process, and cell projection organization, whereas RNA metabolic process and amino acid metabolic process were associated with transcripts upregulated in females. Far fewer transcripts were differentially expressed between male and female mantle tissues, with 87 transcripts upregulated in females and 16 upregulated in males. However, 41% of transcripts identified as differentially expressed between mantle tissues were also differentially expressed between male and female gonads includingHistone H4andBystin. This study represents the first characterization of eastern oyster male and female gonad transcriptomes. We further identify differing expression profiles between male and female mantle tissues, which provides evidence for sex‐specific functions of the mantle and suggests that this tissue could harbor biomarkers for identifying oyster sex non‐destructively.

     
    more » « less
  4. Premise

    Cold tolerance is an important factor limiting the geographic distribution and growing season for many plant species, yet few studies have examined variation in cold tolerance extensively within and among closely related species and compared that to their geographic distribution.

    Methods

    This study examines cold tolerance within and among species in the genusArabidopsis. We assessed cold tolerance by measuring electrolyte leakage from detached leaves in multiple populations of fiveArabidopsistaxa. The temperature at which 50% of cells were lysed was considered the lethal temperature (LT50).

    Results

    We found variability within and among taxa in cold tolerance. There was no significant within‐species relationship between latitude and cold tolerance. However, the northern taxa,A. kamchatica,A. lyratasubsp.petraea, andA. lyratasubsp.lyrata, were more cold tolerant thanA. thalianaandA. hallerisubsp.gemmiferaboth before and after cold acclimation. Cold tolerance increased after cold acclimation (exposure to low, but nonfreezing temperatures) for all taxa, although the difference was not significant forA. hallerisubsp.gemmifera. For all taxa exceptA. lyratasubsp.lyrata, theLT50values for cold‐acclimated plants were higher than the January mean daily minimum temperature (Tmin), indicating that if plants were not insulated by snow cover, they would not likely survive winter at the northern edge of their range.

    Conclusions

    Arabidopsis lyrataandA. kamchaticawere far more cold tolerant thanA. thaliana. These extremely cold‐tolerant taxa are excellent candidates for studying both the molecular and ecological aspects of cold tolerance.

     
    more » « less
  5. Abstract

    Myo‐inositol oxygenase (MIOX) is the first enzyme in the inositol route to ascorbate (L‐ascorbic acid, AsA, vitamin C). We have previously shown that Arabidopsis plants constitutively expressingMIOXhave elevated foliar AsA content and displayed enhanced growth rate, biomass accumulation, and increased tolerance to multiple abiotic stresses. In this work, we used a combination of transcriptomics, chromatography, microscopy, and physiological measurements to gain a deeper understanding of the underlying mechanisms mediating the phenotype of theAtMIOX4 line. Transcriptomic analysis revealed increased expression of genes involved in auxin synthesis, hydrolysis, transport, and metabolism, which are supported by elevated auxin levels both in vitro and in vivo, and confirmed by assays demonstrating their effect on epidermal cell elongation in theAtMIOX4 over‐expressers. Additionally, we detected up‐regulation of transcripts involved in photosynthesis and this was validated by increased efficiency of the photosystem II and proton motive force. We also found increased expression of amylase leading to higher intracellular glucose levels. Multiple gene families conferring plants tolerance/expressed in response to cold, water limitation, and heat stresses were found to be elevated in theAtMIOX4 line. Interestingly, the high AsA plants also displayed up‐regulation of transcripts and hormones involved in defense including jasmonates, defensin, glucosinolates, and transcription factors that are known to be important for biotic stress tolerance. These results overall indicate that elevated levels of auxin and glucose, and enhanced photosynthetic efficiency in combination with up‐regulation of abiotic stresses response genes underly the higher growth rate and abiotic stresses tolerance phenotype of theAtMIOX4 over‐expressers.

     
    more » « less