The Complete Genome Sequences of 2 Species of Geukensia (Brachidontinae, Mytilidae).

We present the complete genome sequences of Geukensia demissa and Geukensia granosissima. Illumina sequencing was performed on genetic material from museum specimens. The reads were assembled using a de novo method followed by a finishing step. The raw and assembled data are available via Genbank.

Evidence of introgression, ecological divergence and adaptation in Asterias sea stars.

Hybrid zones are important windows into the evolutionary dynamics of populations, revealing how processes like introgression and adaptation structure population genomic variation. Importantly, they are useful for understanding speciation and how species respond to their environments. Here, we investigate two closely related sea star species, Asterias rubens and A. forbesi, distributed along rocky European and North American coastlines of the North Atlantic, and use genome-wide molecular markers to infer the distribution of genomic variation within and between species in this group. Using genomic data and environmental niche modelling, we document hybridization occurring between northern New England and the southern Canadian Maritimes. We investigate the factors that maintain this hybrid zone, as well as the environmental variables that putatively drive selection within and between species. We find that the two species differ in their environmental niche breadth; Asterias forbesi displays a relatively narrow environmental niche while conversely, A. rubens has a wider niche breadth. Species distribution models accurately predict hybrids to occur within environmental niche overlap, thereby suggesting environmental selection plays an important role in the maintenance of the hybrid zone. Our results imply that the distribution of genomic variation in North Atlantic sea stars is influenced by the environment, which will be crucial to consider as the climate changes.

Twenty-year record of white pox disease in the Florida Keys: importance of environmental risk factors as drivers of coral health.

Declining coral populations worldwide place a special premium on identifying risks and drivers that precipitate these declines. Understanding the relationship between disease outbreaks and their drivers can help to anticipate when the risk of a disease pandemic is high. Populations of the iconic branching Caribbean elkhorn coral Acropora palmata have collapsed in recent decades, in part due to white pox disease (WPX). To assess the role that biotic and abiotic factors play in modulating coral disease, we present a predictive model for WPX in A. palmata using 20 yr of disease surveys from the Florida Keys plus environmental information collected simultaneously in situ and via satellite. We found that colony size was the most influential predictor for WPX occurrence, with larger colonies being at higher risk. Water quality parameters of dissolved oxygen saturation, total organic carbon, dissolved inorganic nitrogen, and salinity were implicated in WPX likelihood. Both low and high wind speeds were identified as important environmental drivers of WPX. While high temperature has been identified as an important cause of coral mortality in both bleaching and disease scenarios, our model indicates that the relative influence of HotSpot (positive summertime temperature anomaly) was low and actually inversely related to WPX risk. The predictive model developed here can contribute to enabling targeted strategic management actions and disease surveillance, enabling managers to treat the disease or mitigate disease drivers, thereby suppressing the disease and supporting the persistence of corals in an era of myriad threats.

Latitudinal variation and plasticity in response to temperature in Geukensia demissa.

As global temperatures warm, species must adapt to a changing climate or transition to a different location suitable for their survival. Understanding the extent to which species are able to do so, particularly keystone species, is imperative to ensuring the survival of key ecosystems. The ribbed mussel Geukensia demissa is an integral part of salt marshes along the Atlantic coast of North America. Spatial patterns of genomic and phenotypic divergence have been previously documented, although their link with coastal environmental variation is unknown. Here, we study how populations of G. demissa in the northern (Massachusetts) and southern (Georgia) portions of the species range respond to changes in temperature. We combine assays of variation in oxygen consumption and RNA transcriptomic data with genomic divergence analyses to identify how separate populations of G. demissa may vary in distinct thermal environments. Our results show differences in constitutive oxygen consumption between mussels from Georgia and Massachusetts, as well as shared and disparate patterns of gene expression across temperature profiles. We also find that metabolic genes seem to be a strong component of divergence between these two populations. Our analysis highlights the importance of studying integrative patterns of genomic and phenotypic variation in species that are key for particular ecosystems, and how they might respond to further changes in climate.

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.

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.

Is It in the Stars? Exploring the Relationships between Species' Traits and Sea Star Wasting Disease.

AbstractAn explanation for variation in impacts of sea star wasting disease across asteroid species remains elusive. Although various traits have been suggested to play a potential role in sea star wasting susceptibility, currently we lack a thorough comparison that explores how life-history and natural history traits shape responses to mass mortality across diverse asteroid taxa. To explore how asteroid traits may relate to sea star wasting, using available data and recognizing the potential for biological correlations to be driven by phylogeny, we generated a supertree, tested traits for phylogenetic association, and evaluated associations between traits and sea star wasting impact. Our analyses show no evidence for a phylogenetic association with sea star wasting impact, but there does appear to be phylogenetic association for a subset of asteroid life-history traits, including diet, substrate, and reproductive season. We found no relationship between sea star wasting and developmental mode, diet, pelagic larval duration, or substrate but did find a relationship with minimum depth, reproductive season, and rugosity (or surface complexity). Species with the greatest sea star wasting impacts tend to have shallower minimum depth distributions, they tend to have their median reproductive period 1.5 months earlier, and they tend to have higher rugosities relative to species less affected by sea star wasting. Fully understanding sea star wasting remains challenging, in part because dramatic gaps still exist in our understanding of the basic biology and phylogeny of asteroids. Future studies would benefit from a more robust phylogenetic understanding of sea stars, as well as leveraging intra- and interspecific comparative transcriptomics and genomics to elucidate the molecular pathways responding to sea star wasting.

Gene family amplification facilitates adaptation in freshwater unionid bivalve Megalonaias nervosa.

Freshwater unionid bivalves currently face severe anthropogenic challenges. Over 70% of species in the United States are threatened, endangered or extinct due to pollution, damming of waterways and overfishing. These species are notable for their unusual life history strategy, parasite-host co-evolution and biparental mitochondrial inheritance. Among this clade, the washboard mussel Megalonaias nervosa is one species that remains prevalent across the Southeastern United States, with robust population sizes. We have created a reference genome for M. nervosa to determine how genome content has evolved in the face of these widespread environmental challenges. We observe dynamic changes in genome content, with a burst of recent transposable element proliferation causing a 382 Mb expansion in genome content. Birth-death models suggest rapid expansions among gene families, with a mutation rate of 1.16 × 10-8 duplications per gene per generation. Cytochrome P450 gene families have experienced exceptional recent amplification beyond expectations based on genome-wide birth-death processes. These genes are associated with increased rates of amino acid changes, a signature of selection driving evolution of detox genes. Fitting evolutionary models of adaptation from standing genetic variation, we can compare adaptive potential across species and mutation types. The large population size in M. nervosa suggests a 4.7-fold advantage in the ability to adapt from standing genetic variation compared with a low diversity endemic E. hopetonensis. Estimates suggest that gene family evolution may offer an exceptional substrate of genetic variation in M. nervosa, with Psgv  = 0.185 compared with Psgv  = 0.067 for single nucleotide changes. Hence, we suggest that gene family evolution is a source of 'hopeful monsters' within the genome that may facilitate adaptation when selective pressures shift. These results suggest that gene family expansion is a key driver of adaptive evolution in this key species of freshwater Unionidae that is currently facing widespread environmental challenges. This work has clear implications for conservation genomics on freshwater bivalves as well as evolutionary theory. This genome represents a first step to facilitate reverse ecological genomics in Unionidae and identify the genetic underpinnings of phenotypic diversity.

Global biogeography of marine dispersal potential.

The distance travelled by marine larvae varies by seven orders of magnitude. Dispersal shapes marine biodiversity, and must be understood if marine systems are to be well managed. Because warmer temperatures quicken larval development, larval durations might be systematically shorter in the tropics relative to those at high latitudes. Nevertheless, life history and hydrodynamics also covary with latitude-these also affect dispersal, precluding any clear expectation of how dispersal changes at a global scale. Here we combine data from the literature encompassing >750 marine organisms from seven phyla with oceanographic data on current speeds, to quantify the overall latitudinal gradient in larval dispersal distance. We find that planktonic duration increased with latitude, confirming predictions that temperature effects outweigh all others across global scales. However, while tropical species have the shortest planktonic durations, realized dispersal distances were predicted to be greatest in the tropics and at high latitudes, and lowest at mid-latitudes. At high latitudes, greater dispersal distances were driven by moderate current speed and longer planktonic durations. In the tropics, fast currents overwhelmed the effect of short planktonic durations. Our results contradict previous hypotheses based on biology or physics alone; rather, biology and physics together shape marine dispersal patterns.

An initial comparative genomic autopsy of wasting disease in sea stars.

Beginning in 2013, sea stars throughout the Eastern North Pacific were decimated by wasting disease, also known as "asteroid idiopathic wasting syndrome" (AIWS) due to its elusive aetiology. The geographic extent and taxonomic scale of AIWS meant events leading up to the outbreak were heterogeneous, multifaceted, and oftentimes unobserved; progression from morbidity to death was rapid, leaving few tell-tale symptoms. Here, we take a forensic genomic approach to discover candidate genes that may help explain sea star wasting syndrome. We report the first genome and annotation for Pisaster ochraceus, along with differential gene expression (DGE) analyses in four size classes, three tissue types, and in symptomatic and asymptomatic individuals. We integrate nucleotide polymorphisms associated with survivors of the wasting disease outbreak, DGE associated with temperature treatments in P. ochraceus, and DGE associated with wasting in another asteroid Pycnopodia helianthoides. In P. ochraceus, we found DGE across all tissues, among size classes, and between asymptomatic and symptomatic individuals; the strongest wasting-associated DGE signal was in pyloric caecum. We also found previously identified outlier loci co-occur with differentially expressed genes. In cross-species comparisons of symptomatic and asymptomatic individuals, consistent responses distinguish genes associated with invertebrate innate immunity and chemical defence, consistent with context-dependent stress responses, defensive apoptosis, and tissue degradation. Our analyses thus highlight genomic constituents that may link suspected environmental drivers (elevated temperature) with intrinsic differences among individuals (age/size, alleles associated with susceptibility) that elicit organismal responses (e.g., coelomocyte proliferation) and manifest as sea star wasting mass mortality.

Evidence That Microorganisms at the Animal-Water Interface Drive Sea Star Wasting Disease.

Sea star wasting (SSW) disease describes a condition affecting asteroids that resulted in significant Northeastern Pacific population decline following a mass mortality event in 2013. The etiology of SSW is unresolved. We hypothesized that SSW is a sequela of microbial organic matter remineralization near respiratory surfaces, one consequence of which may be limited O2 availability at the animal-water interface. Microbial assemblages inhabiting tissues and at the asteroid-water interface bore signatures of copiotroph proliferation before SSW onset, followed by the appearance of putatively facultative and strictly anaerobic taxa at the time of lesion genesis and as animals died. SSW lesions were induced in Pisaster ochraceus by enrichment with a variety of organic matter (OM) sources. These results together illustrate that depleted O2 conditions at the animal-water interface may be established by heterotrophic microbial activity in response to organic matter loading. SSW was also induced by modestly (∼39%) depleted O2 conditions in aquaria, suggesting that small perturbations in dissolved O2 may exacerbate the condition. SSW susceptibility between species was significantly and positively correlated with surface rugosity, a key determinant of diffusive boundary layer thickness. Tissues of SSW-affected individuals collected in 2013-2014 bore δ15N signatures reflecting anaerobic processes, which suggests that this phenomenon may have affected asteroids during mass mortality at the time. The impacts of enhanced microbial activity and subsequent O2 diffusion limitation may be more pronounced under higher temperatures due to lower O2 solubility, in more rugose asteroid species due to restricted hydrodynamic flow, and in larger specimens due to their lower surface area to volume ratios which affects diffusive respiratory potential.

Maintenance of a Genetic Cline in the Barnacle Balanus glandula.

The barnacle Balanus glandula is a broadly distributed species in the temperate northeastern Pacific that is notable for a robust genetic cline between about 36° and 40° N latitude. Prior work established the evolutionary origins of this pattern and proposed that it is maintained by environmental selection. In recent years, "climate velocity" studies in marine habitats have shown dramatic distributional shifts for many species as they track their preferred temperature range in a warming ocean. We re-sampled B. glandula across its entire geographic range to determine whether there has been any shift in this genetic distribution, a development signaling that temperature or other climate factors are maintaining this genetic cline. Additionally, we asked whether the spatially distributed mitochondrial lineages also vary in reproductive output with latitude, using location as a proxy for temperature and other coastal environmental factors. Here we show that although the distribution of the genetic cline has not appreciably changed, there is a notable association of decreased reproductive output at lower latitudes of the distribution in the "northern" lineage of B. glandula.

Draft Genome Sequences of 38 Serratia marcescens Isolates Associated with Acroporid Serratiosis.

Serratia marcescens is a Gram-negative bacterium causally linked to acroporid serratiosis, a form of white pox disease implicated in the decline of elkhorn corals. We report draft genomes of 38 S. marcescens isolates collected from host and nonhost sources. The availability of these genomes will aid future analyses of acroporid serratiosis.

Parallel Patterns of Host-Specific Morphology and Genetic Admixture in Sister Lineages of a Commensal Barnacle.

Symbiotic relationships are often species specific, allowing symbionts to adapt to their host environments. Host generalists, on the other hand, have to cope with diverse environments. One coping strategy is phenotypic plasticity, defined by the presence of host-specific phenotypes in the absence of genetic differentiation. Recent work indicates that such host-specific phenotypic plasticity is present in the West Pacific lineage of the commensal barnacle Chelonibia testudinaria (Linnaeus, 1758). We investigated genetic and morphological host-specific structure in the genetically distinct Atlantic sister lineage of C. testudinaria. We collected adult C. testudinaria from loggerhead sea turtles, horseshoe crabs, and blue crabs along the eastern U.S. coast between Delaware and Florida and in the Gulf of Mexico off Mississippi. We find that shell morphology, especially shell thickness, is host specific and comparable in similar host species between the Atlantic and West Pacific lineages. We did not detect significant genetic differentiation related to host species when analyzing data from 11 nuclear microsatellite loci and mitochondrial sequence data, which is comparable to findings for the Pacific lineage. The most parsimonious explanation for these parallel patterns between distinct lineages of C. testudinaria is that C. testudinaria maintained phenotypic plasticity since the lineages diverged 4-5 mya.

RNA expression and disease tolerance are associated with a "keystone mutation" in the ochre sea star Pisaster ochraceus.

An overdominant mutation in an intron of the elongation factor 1-α (EF1A) gene in the sea star Pisaster ochraceus has shown itself to mediate tolerance to "sea star wasting disease", a pandemic that has significantly reduced sea star populations on the Pacific coast of North America. Here we use RNA sequencing of healthy individuals to identify differences in constitutive expression of gene regions that may help explain this tolerance phenotype. Our results show that individuals carrying this mutation have lower expression at a large contingent of gene regions. Individuals without this mutation also appear to have a greater cellular response to temperature stress, which has been implicated in the outbreak of sea star wasting disease. Given the ecological significance of P. ochraceus, these results may be useful in predicting the evolutionary and demographic future for Pacific intertidal communities.

Mitochondrial diversity in Gonionemus (Trachylina:Hydrozoa) and its implications for understanding the origins of clinging jellyfish in the Northwest Atlantic Ocean.

Determining whether a population is introduced or native to a region can be challenging due to inadequate taxonomy, the presence of cryptic lineages, and poor historical documentation. For taxa with resting stages that bloom episodically, determining origin can be especially challenging as an environmentally-triggered abrupt appearance of the taxa may be confused with an anthropogenic introduction. Here, we assess diversity in mitochondrial cytochrome oxidase I sequences obtained from multiple Atlantic and Pacific locations, and discuss the implications of our findings for understanding the origin of clinging jellyfish Gonionemus in the Northwest Atlantic. Clinging jellyfish are known for clinging to seagrasses and seaweeds, and have complex life cycles that include resting stages. They are especially notorious as some, although not all, populations are associated with severe sting reactions. The worldwide distribution of Gonionemus has been aptly called a "zoogeographic puzzle" and our results refine rather than resolve the puzzle. We find a relatively deep divergence that may indicate cryptic speciation between Gonionemus from the Northeast Pacific and Northwest Pacific/Northwest Atlantic. Within the Northwest Pacific/Northwest Atlantic clade, we find haplotypes unique to each region. We also find one haplotype that is shared between highly toxic Vladivostok-area populations and some Northwest Atlantic populations. Our results are consistent with multiple scenarios that involve both native and anthropogenic processes. We evaluate each scenario and discuss critical directions for future research, including improving the resolution of population genetic structure, identifying possible lineage admixture, and better characterizing and quantifying the toxicity phenotype.

Large-scale gene flow in the barnacle Jehlius cirratus and contrasts with other broadly-distributed taxa along the Chilean coast.

We evaluate the population genetic structure of the intertidal barnacle Jehlius cirratus across a broad portion of its geographic distribution using data from the mitochondrial cytochrome oxidase I (COI) gene region. Despite sampling diversity from over 3,000 km of the linear range of this species, there is only slight regional structure indicated, with overall Φ CT of 0.036 (p < 0.001) yet no support for isolation by distance. While these results suggest greater structure than previous studies of J. cirratus had indicated, the pattern of diversity is still far more subtle than in other similarly-distributed species with similar larval and life history traits. We compare these data and results with recent findings in four other intertidal species that have planktotrophic larvae. There are no clear patterns among these taxa that can be associated with intertidal depth or other known life history traits.

The oceanic concordance of phylogeography and biogeography: a case study in Notochthamalus.

Dispersal and adaptation are the two primary mechanisms that set the range distributions for a population or species. As such, understanding how these mechanisms interact in marine organisms in particular - with capacity for long-range dispersal and a poor understanding of what selective environments species are responding to - can provide useful insights for the exploration of biogeographic patterns. Previously, the barnacle Notochthamalus scabrosus has revealed two evolutionarily distinct lineages with a joint distribution that suggests an association with one of the two major biogeographic boundaries (~30°S) along the coast of Chile. However, spatial and genomic sampling of this system has been limited until now. We hypothesized that given the strong oceanographic and environmental shifts associated with the other major biogeographic boundary (~42°S) for Chilean coastal invertebrates, the southern mitochondrial lineage would dominate or go to fixation in locations further to the south. We also evaluated nuclear polymorphism data from 130 single nucleotide polymorphisms to evaluate the concordance of the signal from the nuclear genome with that of the mitochondrial sample. Through the application of standard population genetic approaches along with a Lagrangian ocean connectivity model, we describe the codistribution of these lineages through a simultaneous evaluation of coastal lineage frequencies, an approximation of larval behavior, and current-driven dispersal. Our results show that this pattern could not persist without the two lineages having distinct environmental optima. We suggest that a more thorough integration of larval dynamics, explicit dispersal models, and near-shore environmental analysis can explain much of the coastal biogeography of Chile.