Decimation by sea star wasting disease and rapid genetic change in a keystone species, \u3cem\u3ePisaster ochraceus\u3c/em\u3e

Standing genetic variation enables or restricts a population’s capacity to respond to changing conditions, including the extreme disturbances expected to increase in frequency and intensity with continuing anthropogenic climate change. However, we know little about how populations might respond to extreme events with rapid genetic shifts, or how population dynamics may influence and be influenced by population genomic change. We use a range-wide epizootic, sea star wasting disease, that onset in mid-2013 and caused mass mortality in Pisaster ochraceus to explore how a keystone marine species responded to an extreme perturbation. We integrated field surveys with restriction site-associated DNA sequencing data to (i) describe the population dynamics of mortality and recovery, and (ii) compare allele frequencies in mature P. ochraceus before the disease outbreak with allele frequencies in adults and new juveniles after the outbreak, to identify whether selection may have occurred. We found P. ochraceus suffered 81% mortality in the study region between 2012 and 2015, and experienced a concurrent 74-fold increase in recruitment beginning in late 2013. Comparison of pre- and postoutbreak adults revealed significant allele frequency changes at three loci, which showed consistent changes across the large majority of locations. Allele frequency shifts in juvenile P. ochraceus (spawned from premortality adults) were consistent with those seen in adult survivors. Such parallel shifts suggest detectable signals of selection and highlight the potential for persistence of this change in subsequent generations, which may influence the resilience of this keystone species to future outbreaks

A Chromosome-level genome assembly of the highly heterozygous sea urchin Echinometra sp. EZ reveals adaptation in the regulatory regions of stress response genes

Echinometra is the most widespread genus of sea urchin and has been the focus of a wide range of studies in ecology, speciation, and reproduction. However, available genetic data for this genus are generally limited to a few select loci. Here, we present a chromosome-level genome assembly based on 10x Genomics, PacBio, and Hi-C sequencing for Echinometra sp. EZ from the Persian/Arabian Gulf. The genome is assembled into 210 scaffolds totaling 817.8 Mb with an N50 of 39.5 Mb. From this assembly, we determined that the E. sp. EZ genome consists of 2n = 42 chromosomes. BUSCO analysis showed that 95.3% of BUSCO genes were complete. Ab initio and transcript-informed gene modeling and annotation identified 29,405 genes, including a conserved Hox cluster. E. sp. EZ can be found in high-temperature and high-salinity environments, and we therefore compared E. sp. EZ gene families and transcription factors associated with environmental stress response (“defensome”) with other echinoid species with similar high-quality genomic resources. While the number of defensome genes was broadly similar for all species, we identified strong signatures of positive selection in E. sp. EZ noncoding elements near genes involved in environmental response pathways as well as losses of transcription factors important for environmental response. These data provide key insights into the biology of E. sp. EZ as well as the diversification of Echinometra more widely and will serve as a useful tool for the community to explore questions in this taxonomic group and beyond

Integrating genomics with the fossil record to explore the evolutionary history of Echinoidea

Echinoidea constitutes one of five major clades of living echinoderms, marine animals uniquely characterized by a pentaradial symmetry. Approximately 1,000 living and 10,000 extinct species have been described, including many commonly known as sea urchins, heart urchins and sand dollars. Today, echinoids are ubiquitous in benthic marine environments, where they strongly affect the functioning of biodiverse communities such as coral reefs and kelp forests. Given the quality of their fossil record, their remarkable morphological complexity and our thorough understanding of their development, echinoids provide unparalleled opportunities to explore evolutionary questions in deep-time, providing access to the developmental and morphological underpinnings of evolutionary innovation. These questions cannot be addressed without first resolving the phylogenetic relationships among living and extinct lineages. The goal of this dissertation is to advance our understanding of echinoid relationships and evolutionary history, as well as to explore more broadly the integration of phylogenomic, morphological and paleontological data in phylogenetic reconstruction and macroevolutionary inference.In Chapter 1, I report the results of the first phylogenomic analysis of echinoids based on the sequencing of 17 novel echinoid transcriptomes. Phylogenetic analyses of this data resolve the position of several clades—including the sand dollars—in disagreement with traditional morphological hypotheses. I demonstrate the presence of a strong phylogenetic signal for these novel resolutions, and explore scenarios to reconcile these findings with morphological evidence. In Chapter 7, I extend this approach with a more thorough taxon sampling, resulting in a robust topology with a near-complete sampling of major echinoid lineages. This effort reveals that apatopygids, a clade of three species with previously unclear affinities, represent the only living descendants of a once diverse Mesozoic clade. I also perform a thorough time calibration analysis, quantifying the relative effects of choosing among alternative models of molecular evolution, gene samples and clock priors. I introduce the concept of a chronospace and use it to reveal that only the last among the aforementioned choices affects significantly our understanding of echinoid diversification. Molecular clocks unambiguously support late Permian and late Cretaceous origins for crown group echinoids and sand dollars, respectively, implying long ghost ranges for both. Fossils have been shown to improve the accuracy of phylogenetic comparative methods, warranting their inclusion alongside extant terminals when exploring evolutionary processes across deep timescales. However, their impact on topological inference remains controversial. I explore this topic in Chapter 3 with the use of simulations, which show that morphological phylogenies are more accurate when fossil taxa are incorporated. I also show that tip-dated Bayesian inference, which takes stratigraphic information from fossils into account, outperforms uncalibrated methods. This approach is complemented in Chapter 2 with the analysis of empirical datasets, confirming that incorporating fossils reshapes phylogenies in a manner that is entirely distinct from increased sampling of extant taxa, a result largely attributable to the occurrence of distinctive character combinations among fossils. Even though phylogenomic and paleontological data are complementary resources for unraveling the relationships and divergence times of lineages, few studies have attempted to fully integrate them. Chapter 4 revisits the phylogeny of crown group Echinoidea using a total-evidence dating approach combining phylogenomic, morphological and stratigraphic information. To this end, I develop a method (genesortR) for subsampling molecular datasets that selects loci with high phylogenetic signal and low systematic biases. The results demonstrate that combining different data sources increases topological accuracy and helps resolve phylogenetic conflicts. Notably, I present a new hypothesis for the origin and early morphological evolution of the sand dollars and close allies. In Chapter 6, I compare the behavior of genesortR against alternative subsampling strategies across a sample of phylogenomic matrices. I find this method to systematically outperform random loci selection, unlike commonly-used approaches that target specific evolutionary rates or minimize sources of systematic error. I conclude that these methods should not be used indiscriminately, and that multivariate methods of phylogenomic subsampling should be favored. Finally, in Chapter 5, I explore the macroevolutionary dynamics of echinoid body size across 270 million years using data for more than 5,000 specimens in a phylogenetically explicit context. I also develop a method (extendedSurface) for parameterizing adaptive landscapes that overcomes issues with existing approaches and finds better fitting models. While echinoid body size has been largely constrained to evolve within a single adaptive peak, the disparity of the clade was generated by regime shifts driving the repeated evolution of miniaturized and gigantic forms. Most innovations occurred during the latter half of the Mesozoic, and were followed by a drastic slowdown in the aftermath of the Cretaceous-Paleogene mass extinction

Handbook of Marine Model Organisms in Experimental Biology

"The importance of molecular approaches for comparative biology and the rapid development of new molecular tools is unprecedented. The extraordinary molecular progress belies the need for understanding the development and basic biology of whole organisms. Vigorous international efforts to train the next-generation of experimental biologists must combine both levels – next generation molecular approaches and traditional organismal biology. This book provides cutting-edge chapters regarding the growing list of marine model organisms. Access to and practical advice on these model organisms have become aconditio sine qua non for a modern education of advanced undergraduate students, graduate students and postdocs working on marine model systems. Model organisms are not only tools they are also bridges between fields – from behavior, development and physiology to functional genomics. Key Features Offers deep insights into cutting-edge model system science Provides in-depth overviews of all prominent marine model organisms Illustrates challenging experimental approaches to model system research Serves as a reference book also for next-generation functional genomics applications Fills an urgent need for students Related Titles Jarret, R. L. & K. McCluskey, eds. The Biological Resources of Model Organisms (ISBN 978-1-1382-9461-5) Kim, S.-K. Healthcare Using Marine Organisms (ISBN 978-1-1382-9538-4) Mudher, A. & T. Newman, eds. Drosophila: A Toolbox for the Study of Neurodegenerative Disease (ISBN 978-0-4154-1185-1) Green, S. L. The Laboratory Xenopus sp. (ISBN 978-1-4200-9109-0)

EchinoDB, an application for comparative transcriptomics of deeply-sampled clades of echinoderms

BACKGROUND: One of our goals for the echinoderm tree of life project (http://echinotol.org) is to identify orthologs suitable for phylogenetic analysis from next-generation transcriptome data. The current dataset is the largest assembled for echinoderm phylogeny and transcriptomics. We used RNA-Seq to profile adult tissues from 42 echinoderm specimens from 24 orders and 37 families. In order to achieve sampling members of clades that span key evolutionary divergence, many of our exemplars were collected from deep and polar seas. DESCRIPTION: A small fraction of the transcriptome data we produced is being used for phylogenetic reconstruction. Thus to make a larger dataset available to researchers with a wide variety of interests, we made a web-based application, EchinoDB (http://echinodb.uncc.edu). EchinoDB is a repository of orthologous transcripts from echinoderms that is searchable via keywords and sequence similarity. CONCLUSIONS: From transcripts we identified 749,397 clusters of orthologous loci. We have developed the information technology to manage and search the loci their annotations with respect to the Sea Urchin (Strongylocentrotus purpuratus) genome. Several users have already taken advantage of these data for spin-off projects in developmental biology, gene family studies, and neuroscience. We hope others will search EchinoDB to discover datasets relevant to a variety of additional questions in comparative biology

Additional file 1: of EchinoDB, an application for comparative transcriptomics of deeply-sampled clades of echinoderms

Table of 42 echinoderm specimens used for RNA-seq data that are contained in http://echinodb.uncc.edu . The BJ number is an internal reference code. The voucher number represents where any residual tissues and metadata are stored. RAW indicates the number of raw reads produced by Illumina sequencing. Quality filter and adapter removal indicates the number of reads remaining following fastxtoolkit quality filter of Q score > 20 and removal of adapter regions. Percent reads remaining indicates the fraction of raw reads retained after quality filtering and adapter removal. Percentage Reads removed indicates the fraction of reads removed by quality filtering and adapter removal from the raw reads. Number of Amino Acid Sequences Participating in Orthologous Clusters indicates number of contigs for each species that participated in orthoclusters. Note that contigs may be partially overlapping and redundant. NCBI BioProject Accession number indicates where the contigs have been submitted to NCBI (note the orthoclusters only exist on http://echinodb.uncc.edu ). (XLSX 33 kb