A Decade of Death and Other Dynamics: Deepening Perspectives on the Diversity and Distribution of Sea Stars and Wasting.

AbstractMass mortality events provide valuable insight into biological extremes and also ecological interactions more generally. The sea star wasting epidemic that began in 2013 catalyzed study of the microbiome, genetics, population dynamics, and community ecology of several high-profile species inhabiting the northeastern Pacific but exposed a dearth of information on the diversity, distributions, and impacts of sea star wasting for many lesser-known sea stars and a need for integration across scales. Here, we combine datasets from single-site to coast-wide studies, across time lines from weeks to decades, for 65 species. We evaluated the impacts of abiotic characteristics hypothetically associated with sea star wasting (sea surface temperature, pelagic primary productivity, upwelling wind forcing, wave exposure, freshwater runoff) and species characteristics (depth distribution, developmental mode, diet, habitat, reproductive period). We find that the 2010s sea star wasting outbreak clearly affected a little over a dozen species, primarily intertidal and shallow subtidal taxa, causing instantaneous wasting prevalence rates of 5%-80%. Despite the collapse of some populations within weeks, environmental and species variation protracted the outbreak, which lasted 2-3 years from onset until declining to chronic background rates of ∼2% sea star wasting prevalence. Recruitment began immediately in many species, and in general, sea star assemblages trended toward recovery; however, recovery was heterogeneous, and a marine heatwave in 2019 raised concerns of a second decline. The abiotic stressors most associated with the 2010s sea star wasting outbreak were elevated sea surface temperature and low wave exposure, as well as freshwater discharge in the north. However, detailed data speaking directly to the biological, ecological, and environmental cause(s) and consequences of the sea star wasting outbreak remain limited in scope, unavoidably retrospective, and perhaps always indeterminate. Redressing this shortfall for the future will require a broad spectrum of monitoring studies not less than the taxonomically broad cross-scale framework we have modeled in this synthesis.

A Review of Asteroid Biology in the Context of Sea Star Wasting: Possible Causes and Consequences.

AbstractSea star wasting-marked in a variety of sea star species as varying degrees of skin lesions followed by disintegration-recently caused one of the largest marine die-offs ever recorded on the west coast of North America, killing billions of sea stars. Despite the important ramifications this mortality had for coastal benthic ecosystems, such as increased abundance of prey, little is known about the causes of the disease or the mechanisms of its progression. Although there have been studies indicating a range of causal mechanisms, including viruses and environmental effects, the broad spatial and depth range of affected populations leaves many questions remaining about either infectious or non-infectious mechanisms. Wasting appears to start with degradation of mutable connective tissue in the body wall, leading to disintegration of the epidermis. Here, we briefly review basic sea star biology in the context of sea star wasting and present our current knowledge and hypotheses related to the symptoms, the microbiome, the viruses, and the associated environmental stressors. We also highlight throughout the article knowledge gaps and the data needed to better understand sea star wasting mechanistically, its causes, and potential management.

Corrigendum: Spatial Patterns of Thalassia testudinum Immune Status and Labyrinthula spp. Load Implicate Environmental Quality and History as Modulators of Defense Strategies and Wasting Disease in Florida Bay, United States.

[This corrects the article DOI: 10.3389/fpls.2021.612947.].

Minor Genetic Consequences of a Major Mass Mortality: Short-Term Effects in Pisaster ochraceus.

AbstractMass mortality events are increasing globally in frequency and magnitude, largely as a result of human-induced change. The effects of these mass mortality events, in both the long and short term, are of imminent concern because of their ecosystem impacts. Genomic data can be used to reveal some of the population-level changes associated with mass mortality events. Here, we use reduced-representation sequencing to identify potential short-term genetic impacts of a mass mortality event associated with a sea star wasting outbreak. We tested for changes in the population for genetic differentiation, diversity, and effective population size between pre-sea star wasting and post-sea star wasting populations of Pisaster ochraceus-a species that suffered high sea star wasting-associated mortality (75%-100% at 80% of sites). We detected no significant population-based genetic differentiation over the spatial scale sampled; however, the post-sea star wasting population tended toward more differentiation across sites than the pre-sea star wasting population. Genetic estimates of effective population size did not detectably change, consistent with theoretical expectations; however, rare alleles were lost. While we were unable to detect significant population-based genetic differentiation or changes in effective population size over this short time period, the genetic burden of this mass mortality event may be borne by future generations, unless widespread recruitment mitigates the population decline. Prior results from P. ochraceus indicated that natural selection played a role in altering allele frequencies following this mass mortality event. In addition to the role of selection found in a previous study on the genomic impacts of sea star wasting on P. ochraceus, our current study highlights the potential role the stochastic loss of many individuals plays in altering how genetic variation is structured across the landscape. Future genetic monitoring is needed to determine long-term genetic impacts in this long-lived species. Given the increased frequency of mass mortality events, it is important to implement demographic and genetic monitoring strategies that capture baselines and background dynamics to better contextualize species' responses to large perturbations.

Spatial Patterns of Thalassia testudinum Immune Status and Labyrinthula spp. Load Implicate Environmental Quality and History as Modulators of Defense Strategies and Wasting Disease in Florida Bay, United States.

Seagrass wasting disease, caused by protists of the genus Labyrinthula, is an important stressor of the dominant macrophyte in Florida Bay (FB), United States, Thalassia testudinum. FB exhibits countervailing gradients in plant morphology and resource availability. A synoptic picture of the Thalassia-Labyrinthula relationship was obtained by assessing the activity of four immune biomarkers in conjunction with pathogen prevalence and load [via quantitative PCR (qPCR)] at 15 sites across FB. We found downregulated immune status paired with moderate pathogen load among larger-bodied host phenotypes in western FB and upregulated immunity for smaller-bodied phenotypes in eastern FB. Among the highest immune response sites, a distinct inshore-offshore loading pattern was observed, where coastal basins exposed to freshwater runoff and riverine inputs had the highest pathogen loads, while adjacent offshore locations had the lowest. To explain this, we propose a simple, conceptual model that defines a framework for testable hypotheses based on recent advances in resistance-tolerance theory. We suggest that resource availability has the potential to drive not only plant size, but also tolerance to pathogen load by reducing investment in immunity. Where resources are more scarce, plants may adopt a resistance strategy, upregulating immunity; however, when physiologically challenged, this strategy appears to fail, resulting in high pathogen load. While evidence remains correlative, we argue that hyposalinity stress, at one or more temporal scales, may represent one of many potential drivers of disease dynamics in FB. Together, these data highlight the complexity of the wasting disease pathosystem and raise questions about how climate change and ongoing Everglades restoration might impact this foundational seagrass species.

Integrating host immune status, Labyrinthula spp. load and environmental stress in a seagrass pathosystem: Assessing immune markers and scope of a new qPCR primer set.

Recent trends suggest that marine disease outbreaks caused by opportunistic pathogens are increasing in frequency and severity. One such malady is seagrass wasting disease, caused by pathogens in the genus Labyrinthula. It is suspected that pathogenicity is intimately linked to the ability of the host to initiate defense responses; however, supportive evidence is lacking. To address this, we developed two techniques, including 1) a new qPCR-based pathogen detection method, and 2) an immune profiling panel via four host-biomarker assays (measuring peroxidase, exochitinase, polyphenol oxidase, and lysozyme activities). These techniques were then used to experimentally investigate the impact of environmental stressors (namely, elevated temperature and salinity) on host immunity and how immune status might affect susceptibility to Labyrinthula infection. In the first experiment, we subjected individual turtlegrass (Thalassia testudinum) shoots to short-term (7 d) abiotic stressors alone. In a second experiment, the same abiotic stressor conditions were followed by pathogen exposure (7 additional d), simulating a scenario where we attempt to isolate the impact of environmental stressors on the host seagrass species by removing the stressor as the pathogen is introduced. The qPCR assay successfully quantified the abundance of Labyrinthula spp. cells from both pure cultures and seagrass tissues across a broad range of predominately pathogenic strains, with high sensitivity. Immune enzyme assays revealed that all four biomarkers were constitutively active in turtlegrass individuals, but specific activities were largely unaffected by the chosen abiotic stressor conditions. We also identified positive correlations between pathogen load and two biomarkers (peroxidase, exochitinase), regardless of abiotic stress treatment, further demonstrating the potential utility of these biomarkers in future applications.

Isolation, expression analysis and characterization of NEFA-interacting nuclear protein 30 and RING finger and SPRY domain containing 1 in skeletal muscle.

Muscle atrophy results from a range of physiological conditions, including immobilization, spinal cord damage, inflammation and aging. In this study we describe two genes, NEFA-interacting nuclear protein 30 (Nip30) and RING Finger and SPRY domain containing 1 (Rspry1), which have not previously been characterized or shown to be expressed in skeletal muscle. Furthermore, Nip30 and Rspry1 were transcriptionally induced in response to neurogenic muscle wasting in mice and were also found to be expressed endogenously at the RNA and protein level in C2C12 mouse muscle cells. Interestingly, during analysis of Nip30 and Rspry1 it was observed that these genes share a 230 base pair common regulatory region that contains several putative transcription regulatory elements. In order to assess the transcriptional activity of the Nip30 and Rspry1 regulatory regions, a fragment of the promoter of each gene was cloned, fused to a reporter gene, and transfected into cells. The Nip30 and Rspry1 reporters were both found to have significant transcriptional activity in cultured cells. Furthermore, the Nip30-Rspry1 common regulatory region contains a conserved E-box enhancer, which is an element bound by myogenic regulatory factors that function in the regulation of muscle-specific gene expression. Therefore, in order to determine if the predicted E-box was functional, Nip30 and Rspry1 reporters were transfected into cells ectopically expressing the myogenic regulatory factor, MyoD1, resulting in significant induction of both reporter genes. In addition, mutation of the conserved E-box element eliminated MyoD1 activation of the Nip30 and Rspry1 reporters. Finally, GFP-tagged Nip30 was found to localize to the nucleus, while GFP-tagged Rspry1 was found to localize to the cytoplasm of muscle cells.