Biodiversity differentially impacts disease dynamics across marine and terrestrial habitats.

The relationship between biodiversity and infectious disease, where increased biodiversity leads to decreased disease risk, originated from research in terrestrial disease systems and remains relatively underexplored in marine systems. Understanding the impacts of biodiversity on disease in marine versus terrestrial systems is key to continued marine ecosystem functioning, sustainable aquaculture, and restoration projects. We compare the biodiversity-disease relationship across terrestrial and marine systems, considering biodiversity at six levels: intraspecific host diversity, host microbiomes, interspecific host diversity, biotic vectors and reservoirs, parasite consumers, and parasites. We highlight gaps in knowledge regarding how these six levels of biodiversity impact diseases in marine systems and propose two model systems, the Perkinsus-oyster and Labyrinthula-seagrass systems, to address these gaps.

Limited plasticity in thermally tolerant ectotherm populations: evidence for a trade-off.

Many species face extinction risks owing to climate change, and there is an urgent need to identify which species' populations will be most vulnerable. Plasticity in heat tolerance, which includes acclimation or hardening, occurs when prior exposure to a warmer temperature changes an organism's upper thermal limit. The capacity for thermal acclimation could provide protection against warming, but prior work has found few generalizable patterns to explain variation in this trait. Here, we report the results of, to our knowledge, the first meta-analysis to examine within-species variation in thermal plasticity, using results from 20 studies (19 species) that quantified thermal acclimation capacities across 78 populations. We used meta-regression to evaluate two leading hypotheses. The climate variability hypothesis predicts that populations from more thermally variable habitats will have greater plasticity, while the trade-off hypothesis predicts that populations with the lowest heat tolerance will have the greatest plasticity. Our analysis indicates strong support for the trade-off hypothesis because populations with greater thermal tolerance had reduced plasticity. These results advance our understanding of variation in populations' susceptibility to climate change and imply that populations with the highest thermal tolerance may have limited phenotypic plasticity to adjust to ongoing climate warming.

Natural experiments and long-term monitoring are critical to understand and predict marine host-microbe ecology and evolution.

Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host's physiological capacities; however, the identity and functional role(s) of key members of the microbiome ("core microbiome") in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems' capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts' plastic and adaptive responses to environmental change requires (i) recognizing that individual host-microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions.

Social, economic, and environmental factors influencing the basic reproduction number of COVID-19 across countries.

OBJECTIVE: To assess whether the basic reproduction number (R0) of COVID-19 is different across countries and what national-level demographic, social, and environmental factors other than interventions characterize initial vulnerability to the virus. METHODS: We fit logistic growth curves to reported daily case numbers, up to the first epidemic peak, for 58 countries for which 16 explanatory covariates are available. This fitting has been shown to robustly estimate R0 from the specified period. We then use a generalized additive model (GAM) to discern both linear and nonlinear effects, and include 5 random effect covariates to account for potential differences in testing and reporting that can bias the estimated R0. FINDINGS: We found that the mean R0 is 1.70 (S.D. 0.57), with a range between 1.10 (Ghana) and 3.52 (South Korea). We identified four factors-population between 20-34 years old (youth), population residing in urban agglomerates over 1 million (city), social media use to organize offline action (social media), and GINI income inequality-as having strong relationships with R0, across countries. An intermediate level of youth and GINI inequality are associated with high R0, (n-shape relationships), while high city population and high social media use are associated with high R0. Pollution, temperature, and humidity did not have strong relationships with R0 but were positive. CONCLUSION: Countries have different characteristics that predispose them to greater intrinsic vulnerability to COVID-19. Studies that aim to measure the effectiveness of interventions across locations should account for these baseline differences in social and demographic characteristics.

Genomic signatures of selection in bats surviving white-nose syndrome.

Rapid evolution of advantageous traits following abrupt environmental change can help populations recover from demographic decline. However, for many introduced diseases affecting longer-lived, slower reproducing hosts, mortality is likely to outpace the acquisition of adaptive de novo mutations. Adaptive alleles must therefore be selected from standing genetic variation, a process that leaves few detectable genomic signatures. Here, we present whole genome evidence for selection in bat populations that are recovering from white-nose syndrome (WNS). We collected samples both during and after a WNS-induced mass mortality event in two little brown bat populations that are beginning to show signs of recovery and found signatures of soft sweeps from standing genetic variation at multiple loci throughout the genome. We identified one locus putatively under selection in a gene associated with the immune system. Multiple loci putatively under selection were located within genes previously linked to host response to WNS as well as to changes in metabolism during hibernation. Results from two additional populations suggested that loci under selection may differ somewhat among populations. Through these findings, we suggest that WNS-induced selection may contribute to genetic resistance in this slowly reproducing species threatened with extinction.

Considering Commercial Vessels as Potential Vectors of Stony Coral Tissue Loss Disease.

Stony coral tissue loss disease (SCTLD) is a troubling new disease that is spreading rapidly across the greater Caribbean region, but the etiological agent(s) and the mechanisms(s) of spread are both unknown. First detected off the coast of Miami, Florida, major ocean currents alone do not explain the pattern of spread, with outbreaks occurring across geographically disjunct and distant locations. This has raised concerns by researchers and resource managers that commercial vessels may contribute as vectors to spread of the disease. Despite existing regulatory and management strategies intended to limit coastal marine invasion risks, the efficacy of these measures is still unresolved for ship-borne microorganisms, and disease transport via ballast water and hull biofouling are under examination given the high ship traffic in the region. Here, to help inform the discussion of ships as possible vectors of SCTLD, we provide an overview of the current state of knowledge about ships and their potential to transfer organisms in the greater Caribbean, focusing in particular on ballast water, and outline a set of recommendations for future research.

Environmental factors drive the release of Perkinsus marinus from infected oysters.

Since the discovery of Perkinsus marinus as the cause of dermo disease in Crassostrea virginica, salinity and temperature have been identified as the main environmental drivers of parasite prevalence. However, little is known about how these variables affect the movement of the parasite from host to water column. In order to elucidate how environmental factors can influence the abundance of this parasite in the water column, we conducted a series of experiments testing the effects of time of day, temperature and salinity on the release of P. marinus cells from infected oysters. We found that P. marinus cells were released on a diurnal cycle, with most cells released during the hottest and brightest period of the day (12:00-18:00). Temperature also had a strong and immediate effect on the number of cells released, but salinity did not, only influencing the intensity of infection over the course of several months. Taken together, our results demonstrate that (1) the number of parasites in the water column fluctuates according to a diurnal cycle, (2) temperature and salinity act on different timescales to influence parasite abundance, and (3) live infected oysters may substantially contribute to the abundance of transmissive parasites in the water column under particular environmental conditions.

Ecology, histopathology, and microbial ecology of a white-band disease outbreak in the threatened staghorn coral Acropora cervicornis.

This study is a multi-pronged description of a temperature-induced outbreak of white-band disease (WBD) that occurred in Acropora cervicornis off northern Miami Beach, Florida (USA), from July to October 2014. We describe the ecology of the disease and examine diseased corals using both histopathology and next-generation bacterial 16S gene sequencing, making it possible to better understand the effect this disease has on the coral holobiont, and to address some of the seeming contradictions among previous studies of WBD that employed either a purely histological or molecular approach. The outbreak began in July 2014, as sea surface temperatures reached 29°C, and peaked in mid-September, a month after the sea surface temperature maximum. The microscopic anatomy of apparently healthy portions of colonies displaying active disease signs appeared normal except for some tissue atrophy and dissociation of mesenterial filaments deep within the branch. Structural changes were more pronounced in visibly diseased fragments, with atrophy, necrosis, and lysing of surface and basal body wall and polyp structures at the tissue-loss margin. The only bacteria evident microscopically in both diseased and apparently healthy tissues with Giemsa staining was a Rickettsiales-like organism (RLO) occupying mucocytes. Sequencing also identified bacteria belonging to the order Rickettsiales in all fragments. When compared to apparently healthy fragments, diseased fragments had more diverse bacterial communities made up of many previously suggested potential primary pathogens and secondary (opportunistic) colonizers. Interactions between elevated seawater temperatures, the coral host, and pathogenic members of the diseased microbiome all contribute to the coral displaying signs of WBD.

Complex interactions between potentially pathogenic, opportunistic, and resident bacteria emerge during infection on a reef-building coral.

Increased bacterial diversity on diseased corals can obscure disease etiology and complicate our understanding of pathogenesis. To untangle microbes that may cause white band disease signs from microbes responding to disease, we inoculated healthy Acropora cervicornis corals with an infectious dose from visibly diseased corals. We sampled these dosed corals and healthy controls over time for sequencing of the bacterial 16S region. Endozoicomonas were associated with healthy fragments from 4/10 colonies, dominating microbiomes before dosing and decreasing over time only in corals that displayed disease signs, suggesting a role in disease resistance. We grouped disease-associated bacteria by when they increased in abundance (primary vs secondary) and whether they originated in the dose (colonizers) or the previously healthy corals (responders). We found that all primary responders increased in all dosed corals regardless of final disease state and are therefore unlikely to cause disease signs. In contrast, primary colonizers in the families Pasteurellaceae and Francisellaceae increased solely in dosed corals that ultimately displayed disease signs, and may be infectious foreign bacteria involved in the development of disease signs. Moving away from a static comparison of diseased and healthy bacterial communities, we provide a framework to identify key players in other coral diseases.

Identification of Candidate Coral Pathogens on White Band Disease-Infected Staghorn Coral.

Bacterial diseases affecting scleractinian corals pose an enormous threat to the health of coral reefs, yet we still have a limited understanding of the bacteria associated with coral diseases. White band disease is a bacterial disease that affects the two Caribbean acroporid corals, the staghorn coral Acropora cervicornis and the elkhorn coral A. palmate. Species of Vibrio and Rickettsia have both been identified as putative WBD pathogens. Here we used Illumina 16S rRNA gene sequencing to profile the bacterial communities associated with healthy and diseased A. cervicornis collected from four field sites during two different years. We also exposed corals in tanks to diseased and healthy (control) homogenates to reduce some of the natural variation of field-collected coral bacterial communities. Using a combination of multivariate analyses, we identified community-level changes between diseased and healthy corals in both the field-collected and tank-exposed datasets. We then identified changes in the abundances of individual operational taxonomic units (OTUs) between diseased and healthy corals. By comparing the diseased and healthy-associated bacteria in field-collected and tank-exposed corals, we were able to identify 16 healthy-associated OTUs and 106 consistently disease-associated OTUs, which are good candidates for putative WBD pathogens. A large percentage of these disease-associated OTUs belonged to the order Flavobacteriales. In addition, two of the putative pathogens identified here belong to orders previously suggested as WBD pathogens: Vibronales and Rickettsiales.

Up in Arms: Immune and Nervous System Response to Sea Star Wasting Disease.

Echinoderms, positioned taxonomically at the base of deuterostomes, provide an important system for the study of the evolution of the immune system. However, there is little known about the cellular components and genes associated with echinoderm immunity. The 2013-2014 sea star wasting disease outbreak is an emergent, rapidly spreading disease, which has led to large population declines of asteroids in the North American Pacific. While evidence suggests that the signs of this disease, twisting arms and lesions, may be attributed to a viral infection, the host response to infection is still poorly understood. In order to examine transcriptional responses of the sea star Pycnopodia helianthoides to sea star wasting disease, we injected a viral sized fraction (0.2 µm) homogenate prepared from symptomatic P. helianthoides into apparently healthy stars. Nine days following injection, when all stars were displaying signs of the disease, specimens were sacrificed and coelomocytes were extracted for RNA-seq analyses. A number of immune genes, including those involved in Toll signaling pathways, complement cascade, melanization response, and arachidonic acid metabolism, were differentially expressed. Furthermore, genes involved in nervous system processes and tissue remodeling were also differentially expressed, pointing to transcriptional changes underlying the signs of sea star wasting disease. The genomic resources presented here not only increase understanding of host response to sea star wasting disease, but also provide greater insight into the mechanisms underlying immune function in echinoderms.

Postglacial recolonization of eastern Blacknose Dace,Rhinichthys atratulus(Teleostei: Cyprinidae), through the gateway of New England.

During the last ice age, much of North America far south as 40°N was covered by glaciers (Hewitt 2000). About 20,000 years ago, as the glaciers retreated, the hydrologic landscape changed dramatically creating waterways for fish dispersal. The number of populations responsible for recolonization and the regions from which they recolonized are unknown for many freshwater fishes living in New England and southeastern Canada. The Blacknose Dace,Rhinichthys atratulus, is one of the freshwater fish species that recolonized this region. We hypothesize that the earliest deglaciated region, modern-day Connecticut, was recolonized byR. atratulusvia a single founding event by a single population. In this paper, we test this hypothesis phylogenetically with regard to the major drainage basins within Connecticut. The mitochondrial DNA exhibits low nucleotide diversity, high haplotype diversity, and a dominant haplotype found across the state. A small percentage of individuals in the Housatonic drainage basin, however, share a haplotype with populations in New York drainage basins, a haplotype not found elsewhere in Connecticut's drainage basins. We calculated a range for the rate of divergence for NADH dehydrogenase subunit 2 (nd2) and control region (ctr) of 4.43-6.76% and 3.84-8.48% per million years (my), respectively. While this range is higher than the commonly accepted rate of 2% for mitochondrial DNA, these results join a growing list of publications finding high rates of divergence for various taxa (Peterson and Masel 2009). The data support the conclusion that Connecticut as a whole was recolonized initially by a single founding event that came from a single refugium. Subsequently, the Housatonic basin alone experienced a secondary recolonization event.