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.

Natural history collections recapitulate 200 years of faunal change.

Changing species assemblages represent major challenges to ecosystems around the world. Retracing these changes is limited by our knowledge of past biodiversity. Natural history collections represent archives of biodiversity and are therefore an unparalleled source to study biodiversity changes. In the present study, we tested the value of natural history collections for reconstructing changes in the abundance and presence of species over time. In total, we scrutinized 17 080 quality-checked records for 242 epibenthic invertebrate species from the North and Baltic Seas collected throughout the last 200 years. Our approaches identified eight previously reported species introductions, 10 range expansions, six of which are new to science, as well as the long-term decline of 51 marine invertebrate species. The cross-validation of our results with published accounts of endangered species and neozoa of the area confirmed the results for two of the approaches for 49 to 55% of the identified species, and contradicted our results for 9 to 10%. The results based on relative record trends were less validated. We conclude that, with the proper approaches, natural history collections are an unmatched resource for recovering early species introductions and declines.

Phylogeography in an "oyster" shell provides first insights into the genetic structure of an extinct Ostrea edulis population.

The historical phylogeography of Ostrea edulis was successfully depicted in its native range for the first time using ancient DNA methods on dry shells from museum collections. This research reconstructed the historical population structure of the European flat oyster across Europe in the 1870s-including the now extinct population in the Wadden Sea. In total, four haplogroups were identified with one haplogroup having a patchy distribution from the North Sea to the Atlantic coast of France. This irregular distribution could be the result of translocations. The other three haplogroups are restricted to narrow geographic ranges, which may indicate adaptation to local environmental conditions or geographical barriers to gene flow. The phylogenetic reconstruction of the four haplogroups suggests the signatures of glacial refugia and postglacial expansion. The comparison with present-day O. edulis populations revealed a temporally stable population genetic pattern over the past 150 years despite large-scale translocations. This historical phylogeographic reconstruction was able to discover an autochthonous population in the German and Danish Wadden Sea in the late nineteenth century, where O. edulis is extinct today. The genetic distinctiveness of a now-extinct population hints at a connection between the genetic background of O. edulis in the Wadden Sea and for its absence until today.

Testing adaptive hypotheses on the evolution of larval life history in acorn and stalked barnacles.

Despite strong selective pressure to optimize larval life history in marine environments, there is a wide diversity with regard to developmental mode, size, and time larvae spend in the plankton. In the present study, we assessed if adaptive hypotheses explain the distribution of the larval life history of thoracican barnacles within a strict phylogenetic framework. We collected environmental and larval trait data for 170 species from the literature, and utilized a complete thoracican synthesis tree to account for phylogenetic nonindependence. In accordance with Thorson's rule, the fraction of species with planktonic-feeding larvae declined with water depth and increased with water temperature, while the fraction of brooding species exhibited the reverse pattern. Species with planktonic-nonfeeding larvae were overall rare, following no apparent trend. In agreement with the "size advantage" hypothesis proposed by Strathmann in 1977, egg and larval size were closely correlated. Settlement-competent cypris larvae were larger in cold water, indicative of advantages for large juveniles when growth is slowed. Planktonic larval duration, on the other hand, was uncorrelated to environmental variables. We conclude that different selective pressures appear to shape the evolution of larval life history in barnacles.

Coming and going - Historical distributions of the European oyster Ostrea edulis Linnaeus, 1758 and the introduced slipper limpet Crepidula fornicata Linnaeus, 1758 in the North Sea.

Natural history collections are fundamental for biodiversity research as well as for any applied environment-related research. These collections can be seen as archives of earth´s life providing the basis to address highly relevant scientific questions such as how biodiversity changes in certain environments, either through evolutionary processes in a geological timescale, or by man-made transformation of habitats throughout the last decades and/or centuries. A prominent example is the decline of the European flat oyster Ostrea edulis Linneaus, 1758 in the North Sea and the concomitant invasion of the common limpet slipper Crepidula fornicata, which has been implicated to have negative effects on O. edulis. We used collections to analyse population changes in both species in the North Sea. In order to reconstruct the change in distribution and diversity over the past 200 years, we combined the temporal and spatial information recorded with the collected specimens contained in several European natural history collections. Our data recover the decline of O. edulis in the North Sea from the 19th century to the present and the process of invasion of C. fornicata. Importantly, the decline of O. edulis was nearly completed before C. fornicata appeared in the North Sea, suggesting that the latter had nothing to do with the local extinction of O. edulis in the North Sea.

Towards a barnacle tree of life: integrating diverse phylogenetic efforts into a comprehensive hypothesis of thecostracan evolution.

Barnacles and their allies (Thecostraca) are a biologically diverse, monophyletic crustacean group, which includes both intensely studied taxa, such as the acorn and stalked barnacles, as well as cryptic taxa, for example, Facetotecta. Recent efforts have clarified phylogenetic relationships in many different parts of the barnacle tree, but the outcomes of these phylogenetic studies have not yet been combined into a single hypothesis for all barnacles. In the present study, we applied a new "synthesis" tree approach to estimate the first working Barnacle Tree of Life. Using this approach, we integrated phylogenetic hypotheses from 27 studies, which did not necessarily include the same taxa or used the same characters, with hierarchical taxonomic information for all recognized species. This first synthesis tree contains 2,070 barnacle species and subspecies, including 239 barnacle species with phylogenetic information and 198 undescribed or unidentified species. The tree had 442 bifurcating nodes, indicating that 79.3% of all nodes are still unresolved. We found that the acorn and stalked barnacles, the Thoracica, and the parasitic Rhizocephala have the largest amount of published phylogenetic information. About half of the thecostracan families for which phylogenetic information was available were polyphyletic. We queried publicly available geographic occurrence databases for the group, gaining a sense of geographic gaps and hotspots in our phylogenetic knowledge. Phylogenetic information is especially lacking for deep sea and Arctic taxa, but even coastal species are not fully incorporated into phylogenetic studies.

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.

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.

Microsatellite loci discovery from next-generation sequencing data and loci characterization in the epizoic barnacle Chelonibia testudinaria (Linnaeus, 1758).

Microsatellite markers remain an important tool for ecological and evolutionary research, but are unavailable for many non-model organisms. One such organism with rare ecological and evolutionary features is the epizoic barnacle Chelonibia testudinaria (Linnaeus, 1758). Chelonibia testudinaria appears to be a host generalist, and has an unusual sexual system, androdioecy. Genetic studies on host specificity and mating behavior are impeded by the lack of fine-scale, highly variable markers, such as microsatellite markers. In the present study, we discovered thousands of new microsatellite loci from next-generation sequencing data, and characterized 12 loci thoroughly. We conclude that 11 of these loci will be useful markers in future ecological and evolutionary studies on C. testudinaria.

The unexpected mating system of the androdioecious barnacle Chelonibia testudinaria (Linnaeus 1758).

Androdioecy was first described by Darwin in his seminal work on barnacle diversity; he identified males and hermaphrodites in the same reproductive population. Today, we realize that many androdioecious plants and animals share astonishing similarities, particularly with regard to their evolutionary history and mating system. Notably, these species were ancestrally dioecious, and their mating system has the following characteristics: hermaphrodites self-fertilize frequently, males are more successful in large mating groups, and males have a mating advantage. A male mating advantage makes androdioecy more likely to persist over evolutionary times. Androdioecious barnacles, however, appear to persist as an outlier with a different evolutionary trajectory: they originate from hermaphroditic species. Although sexual systems of androdioecious barnacles are known, no information on the mating system of androdioecious barnacles is available. This study assessed the mating system of the androdioecious barnacle Chelonibia testudinaria. In contrast to other androdioecious species, C. testudinaria does not self-fertilize, males do not have a mating advantage over hermaphrodites, and the average mating group is quite small, averaging only three individuals. Mating success is increased by proximity to the mate and penis length. Taken together, the mating system of C. testudinaria is unusual in comparison with other androdioecious plants and animals, and the lack of a male mating advantage suggests that the mating system alone does not provide an explanation for the maintenance of androdioecy in this species. Instead, we propose that sex-specific life history equalizes male and hermaphroditic overall fitness.

Functional morphology of the copulatory system of box crabs with long second gonopods (Calappidae, Eubrachyura, Decapoda, Crustacea).

Male True Crabs use two pairs of gonopods to deliver mating products during copulation. Commonly, the second pair is shorter than the first pair, and most research to date has focused on species with short second gonopods. We investigated male and female copulatory organs in Calappula saussurei and Calappa pelii, two species of box crabs (Calappidae) with second gonopods which are longer than the first pair. Scanning electron microscopy and histological cross sectioning show that the female copulatory system is unique in several aspects: the genital duct is part concave and part simple type. The seminal receptacle is divided into two chambers, a ventral chamber of ectodermal and mesodermal origin, and a dorsal chamber of ectodermal origin. This dorsal chamber is the location of spermatophore reception during copulation. A sperm plug closes the dorsal chamber off. We propose that long second gonopods deliver male mating products directly into the dorsal chamber. To date, spermatophore reception has been associated with the mesodermal tissue of the seminal receptacle. The copulatory system of box crabs with long second gonopods shows novel deviations from this general pattern.