Marine Metazoans Research Articles

Assessing patterns of metazoans in the global ocean using environmental DNA.

Documenting large-scale patterns of animals in the ocean and determining the drivers of these patterns is needed for conservation efforts given the unprecedented rates of change occurring within marine ecosystems. We used existing datasets from two global expeditions, Tara Oceans and Malaspina, that circumnavigated the oceans and sampled down to 4000 m to assess metazoans from environmental DNA (eDNA) extracted from seawater. We describe patterns of taxonomic richness within metazoan phyla and orders based on metabarcoding and infer the relative abundance of phyla using metagenome datasets, and relate these data to environmental variables. Arthropods had the greatest taxonomic richness of metazoan phyla at the surface, while cnidarians had the greatest richness in pelagic zones. Half of the marine metazoan eDNA from metagenome datasets was from arthropods, followed by cnidarians and nematodes. We found that mean surface temperature and primary productivity were positively related to metazoan taxonomic richness. Our findings concur with existing knowledge that temperature and primary productivity are important drivers of taxonomic richness for specific taxa at the ocean's surface, but these correlations are less evident in the deep ocean. Massive sequencing of eDNA can improve understanding of animal distributions, particularly for the deep ocean where sampling is challenging.

Navigating uncertainty in maximum body size in marine metazoans.

Body size is a fundamental biological trait shaping ecological interactions, evolutionary processes, and our understanding of the structure and dynamics of marine communities on a global scale. Accurately defining a species' body size, despite the ease of measurement, poses significant challenges due to varied methodologies, tool usage, and subjectivity among researchers, resulting in multiple, often discrepant size estimates. These discrepancies, stemming from diverse measurement approaches and inherent variability, could substantially impact the reliability and precision of ecological and evolutionary studies reliant on body size data across extensive species datasets. This study examines the variation in reported maximum body sizes across 69,570 individual measurements of maximum size, ranging from <0.2 μm to >45 m, for 27,271 species of marine metazoans. The research aims to investigate how reported maximum size variations within species relate to organism size, taxonomy, habitat, and the presence of skeletal structures. The investigation particularly focuses on understanding why discrepancies in maximum size estimates arise and their potential implications for broader ecological and evolutionary studies relying on body size data. Variation in reported maximum sizes is zero for 38% of species, and low for most species, although it exceeds two orders of magnitude for some species. The likelihood of zero variation in maximum size decreased with more measurements and increased in larger species, though this varied across phyla and habitats. Pelagic organisms consistently had low maximum size range values, while small species with unspecified habitats had the highest variation. Variations in maximum size within a species were notably smaller than interspecific variation at higher taxonomic levels. Significant variation in maximum size estimates exists within marine species, and partially explained by organism size, taxonomic group, and habitat. Variation in maximum size could be reduced by standardized measurement protocols and improved meta-data. Despite the variation, egregious errors in published maximum size measurements are rare, and their impact on comparative macroecological and macroevolutionary research is likely minimal.

Middle Ordovician climatic and oceanic destabilization in a slope-setting of the Yangtze platform, South China, and its role as a regional brake on the Ordovician radiations

During the Middle Ordovician, the Great Ordovician Biodiversification Event (GOBE) saw an accelerated diversification pulse in the marine metazoan richness, which has been linked to the oceanic and climatic changes. Here we have examined a deep-water slope succession, Xijinhe section, in Lower Yangtze region by integrating sedimentological and geochemical methods. This study highlights that the climatic and oceanic destabilization might have substantially impacted the marine biodiversity during the Middle Ordovician in South China. Three phases are identified based on lithological and geochemical variations. During Phase I across the Early–Middle Ordovician transition (Floian–Dapingian), the TOC and abundances of redox sensitive elements (RSE) are relatively depleted, suggesting a suboxic-oxic environment in the slope area of Yangtze Sea. The continental chemical weathering intensity transits from stable to unstable in Phase I indicated by CIA (chemical index of alteration) that gradually fluctuate to lower values, potentially caused by the secular cooling. The slowly ameliorating climate and redox conditions advanced the biodiversification across the Early–Middle Ordovician transition. During the Phase II in the Darriwilian, the continental chemical weathering intensity continues to decrease and the concentrations of RSE start to rise. The values of Mn(%)*Co(ppm) become consistently lower than 0.4, and the bio-limited elements such as P, Ba, and Ni are substantially enriched correspondingly. This phenomenon implicates that a secular cooling climate would have resulted in oceanic destabilization by improving upwelling of deeper anoxic/euxinic and eutrophic water into epicontinental sea, potentially causing a deceleration in the biodiversification during the Darriwilian in South China. The Phase III across the Middle–Late Ordovician transition, witnesses the continuous decrease of CIA values and highest abundances of TOC and RSE though some minor fluctuations, indicating a possibly even more drastic oceanic destabilization relative to Phase II. Deeper anoxic/euxinic water continuously intruded and shoaled into the shelf area during the Phase III due to the enhanced upwelling. Consequently, the habitat of marine organisms in shallow water was contracted, and becoming harsher. Additionally, bio-limited elements such as P were released from anoxic sediments and recycle into the seawater during the Middle Ordovician, boosting primary productivity level and may further deplete oxygen in seawater. This unstable oceanic state during the Middle Ordovician, particularly Darriwilian, represented by high nutrients content in epi-continental sea and expanding anoxic/euxinic water, could be attributable for the deceleration of biodiversification in South China and potentially the spatially variable paces of biodiversification in different paleo-continents during the main phase of the GOBE.

Selection by differential survival among marine animals in the Phanerozoic

The Gaia hypothesis posits that the Earth and its biosphere function as a single self-stabilizing system, but a key challenge is explaining how this could have arisen through Darwinian evolution. One theory is that of “selection by differential survival,” in which a clade’s extinction probability decreases with age as it accumulates adaptations resisting environmental disturbances. While this is hard to assess during early Earth history, we can assess whether this process operated among marine animal genera throughout the Phanerozoic. To that end, we analyzed time ranges of 36,117 extinct animal genera using fossil occurrence data from the Paleobiology Database in order to calculate marine metazoan extinction age selectivity, extinction rates, and speciation rates over the Phanerozoic. We identify four signatures of selection by differential survival: lower extinction rates among older lineages, heritability and taxonomically nested propagation of extinction resistance, reduced age selectivity during rare environmental perturbations, and differential extinction rather than speciation as the primary driver of the phenomenon. Evidence for this process at lower taxonomic levels also implies its possibility for life as a whole – indeed, the possibility of Gaia.

Investigating pelagic biodiversity and gelatinous zooplankton communities in the rapidly changing European Arctic: An eDNA metabarcoding survey

AbstractFram Strait, the gateway between the Arctic and Atlantic Oceans, is undergoing major climate change‐induced physical and biological transformations. In particular, rapid warming and ongoing “Atlantification” are driving species range shifts and altering food web structures in the Arctic. Understanding and predicting the consequences of these processes on future ecosystems requires detailed assessments of local and pelagic biodiversity. Gelatinous zooplankton (GZP) is an important component of pelagic communities, and recent evidence indicates that such communities are undergoing major changes in the Fram Strait. However, as sampling GZP is challenging, they are regularly underestimated in biodiversity, distribution, and abundance. To overcome this and address existing ecological knowledge gaps, we investigated patterns of pelagic metazoan diversity in Fram Strait using environmental DNA (eDNA) metabarcoding of the cytochrome c oxidase I (COI) gene. We successfully detected a broad range of taxa from the marine metazoan and GZP communities across sampling locations and ocean depth zones. We demonstrate the vertical structuring of diversity and elucidate relationships between taxa and water mass indicators, such as salinity and temperature. Furthermore, when comparing eDNA data with net and video transect data for GZP at the same period and location, we found that eDNA uncovered a higher number of taxa, including several that were not detected by the other methods. This study is a contribution to the formation of baseline Arctic GZP biodiversity datasets, as well as future research on changing marine metazoan biodiversity and community composition.

A universal tool for marine metazoan species identification: towards best practices in proteomic fingerprinting

Proteomic fingerprinting using MALDI-TOF mass spectrometry is a well-established tool for identifying microorganisms and has shown promising results for identification of animal species, particularly disease vectors and marine organisms. And thus can be a vital tool for biodiversity assessments in ecological studies. However, few studies have tested species identification across different orders and classes. In this study, we collected data from 1246 specimens and 198 species to test species identification in a diverse dataset. We also evaluated different specimen preparation and data processing approaches for machine learning and developed a workflow to optimize classification using random forest. Our results showed high success rates of over 90%, but we also found that the size of the reference library affects classification error. Additionally, we demonstrated the ability of the method to differentiate marine cryptic-species complexes and to distinguish sexes within species.

Scientific history, biogeography, and biological traits predict presence of cryptic or overlooked species.

Genetic data show that many nominal species are composed of more than one biological species, and thus contain cryptic species in the broad sense (including overlooked species). When ignored, cryptic species generate confusion which, beyond biodiversity or vulnerability underestimation, blurs our understanding of ecological and evolutionary processes and may impact the soundness of decisions in conservation or medicine. However, very few hypotheses have been tested about factors that predispose a taxon to contain cryptic or overlooked species. To fill this gap, we surveyed the literature on free-living marine metazoans and built two data sets, one of 187,603 nominal species and another of 83 classes or phyla, to test several hypotheses, correcting for sequence data availability, taxon size and phylogenetic relatedness. We found a strong effect of scientific history: the probability of a taxon containing cryptic species was highest for the earliest described species and varied among time periods potentially consistently with an influence of prevailing scientific theories. The probability of cryptic species being present was also increased for species with large distribution ranges. They were more frequent in the north polar and south polar zones, contradicting previous predictions of more cryptic species in the tropics, and supporting the hypothesis that many cryptic species diverged recently. The number of cryptic species varied among classes, with an excess in hydrozoans and polychaetes, and a deficit in actinopterygians, for example, but precise class ranking was relatively sensitive to the statistical model used. For all models, biological traits, rather than phylum, appeared responsible for the variation among classes: there were fewer cryptic species than expected in classes with hard skeletons (perhaps because they provide good characters for taxonomy) and image-forming vision (in which selection against heterospecific mating may enhance morphological divergence), and more in classes with internal fertilisation. We estimate that among marine free-living metazoans, several thousand additional cryptic species complexes could be identified as more sequence data become available. The factors identified as important for marine animal cryptic species are likely important for other biomes and taxa and should aid many areas in biology that rely on accurate species identification.

Complementary broad-range mitochondrial markers improve eDNA characterization of marine metazoan diversity

Complementary broad-range mitochondrial markers improve eDNA characterization of marine metazoan diversity

Capturing drifting species and molecules—Lessons learned from integrated approaches to assess marine metazoan diversity in highly dynamic waters

AbstractMarine community diversity surveys require a reliable assessment to estimate ecosystem functions and their dynamics. For these, non‐invasive environmental DNA (eDNA) metabarcoding is increasingly applied in zoological studies to complement or even replace traditional morphological identification methods. However, uncertainties remain about the accuracy of the diversity detected with eDNA to capture the actual diversity in the field. Here, we validate the reliability of eDNA metabarcoding in identifying metazoan biodiversity in highly dynamic marine waters of the North Sea. We analyzed biodiversity from water (eDNA) and zooplankton samples with cytochrome c oxidase subunit 1 (COI) and 18S rRNA (18S) metabarcoding at Helgoland Roads and validated the optimal molecular resolution by morphological and molecular zooplankton identification (metabarcoding) with the result of merely a few false‐negative detections. eDNA and zooplankton metabarcoding resolved 354 species from all major and in total 16 metazoan phyla. This molecular genetic species inventory overlapped by 95.9% (COI) and 81.9% (18S) with published inventories of local, morphologically identified species, among them neozoa and rediscovered species. Even though half of all species were detected by both eDNA and zooplankton metabarcoding, the methods differed significantly in their detected diversity. eDNA metabarcoding performed very well in cnidarians and annelids, whereas zooplankton metabarcoding identified higher numbers of fish and malacostraca. Species assemblages significantly differed between the individual sampling events and the cumulative number of identified species increased steadily over the sampling period and did not reach saturation. About a third of the species were detected only once while a core community of 22 species was identified continuously. Our study confirms eDNA metabarcoding to be a powerful tool to identify and analyze North Sea fauna in highly dynamic waters and we recommend investing in high sampling efforts by repetitive sampling and replication using at least 0.45 μm filters to increase filtration volume.

Starvation decreases immunity and immune regulatory factor NF-κB in the starlet sea anemone Nematostella vectensis

Lack of proper nutrition has important consequences for the physiology of all organisms, and nutritional status can affect immunity, based on many studies in terrestrial animals. Here we show a positive correlation between nutrition and immunity in the sea anemone Nematostella vectensis. Gene expression profiling of adult anemones shows downregulation of genes involved in nutrient metabolism, cellular respiration, and immunity in starved animals. Starved adult anemones also have reduced protein levels and activity of immunity transcription factor NF-κB. Starved juvenile anemones have increased sensitivity to bacterial infection and also have lower NF-κB protein levels, as compared to fed controls. Weighted Gene Correlation Network Analysis (WGCNA) is used to identify significantly correlated gene networks that were downregulated with starvation. These experiments demonstrate a correlation between nutrition and immunity in an early diverged marine metazoan, and the results have implications for the survival of marine organisms as they encounter changing environments.

Development of two new sets of PCR primers for eDNA metabarcoding of brittle stars (Echinodermata, Ophiuroidea)

Brittle stars (class Ophiuroidea) are marine invertebrates comprising approximately 2,100 extant species, and are considered to constitute the most diverse taxon of the phylum Echinodermata. As a non-invasive method for monitoring biodiversity, we developed two new sets of PCR primers for metabarcoding environmental DNA (eDNA) from brittle stars. The new primer sets were designed to amplify 2 short regions of the mitochondrial 16S rRNA gene, comprising a conserved region (111–115 bp, 112 bp on average; named “16SOph1”) and a hyper-variable region (180–195 bp, 185 bp on average; named “16SOph2”) displaying interspecific variation. The performance of the primers was tested using eDNA obtained from two sources: a) rearing water of an 2.5 or 170 L aquarium tanks containing 15 brittle star species and b) from natural seawater collected around Misaki, the Pacific coast of central Japan, at depths ranging from shallow (2 m) to deep (&amp;gt; 200 m) sea. To build a reference library, we obtained 16S rRNA sequences of brittle star specimens collected from around Misaki and from similar depths in Japan, and sequences registered in International Nucleotide Sequence Database Collaboration. As a result of comparison of the obtained eDNA sequences with the reference library 37 (including cryptic species) and 26 brittle star species were detected with certain identities by 16SOph1 and 16SOph2 analyses, respectively. In shallow water, the number of species and reads other than the brittle stars detected with 16SOph1 was less than 10% of the total number. On the other hand, the number of brittle star species and reads detected with 16SOph2 was less than half of the total number, and the number of detected non-brittle star metazoan species ranged from 20 to 46 species across 6 to 8 phyla (only the reads at the “Tank” were less than 0.001%). The number of non-brittle star species and reads at 80 m was less than 10% with both of the primer sets. These findings suggest that 16SOph1 is specific to the brittle star and 16SOph2 is suitable for a variety of marine metazoans. It appears, however, that further optimization of primer sequences would still be necessary to avoid possible PCR dropouts from eDNA extracts. Moreover, a detailed elucidation of the brittle star fauna in the examined area, and the accurate identification of brittle star species in the current DNA databank is required.

Drifting with trilobites: The invasion of early post-embryonic trilobite stages to the pelagic realm

The Ordovician Radiation shaped Paleozoic marine ecosystems and led to an increase in the biodiversity of marine organisms. The onset of the Plankton Revolution in the late Cambrian is an important step within the Ordovician Radiation. During this revolution, various organisms invaded pelagic realms, which affected the marine trophic web through the introduction of phytoplankton, zooplankton, as well as plankton- and suspension-feeding animals. Trilobites, a main Paleozoic group of marine metazoans, played a major role during the Ordovician Radiation. Previous studies showed that some trilobites evolved planktic larvae during the Furongian and Early Ordovician. Herein, we quantify the appearance of trilobite planktic larvae by providing highly resolved Cambrian and Ordovician data on 144 trilobite species with well-known developmental sequences. We show that Cambrian trilobites were dominated by species and families with exclusively benthic early post-embryonic stages. On the contrary, Ordovician seas comprised a remarkable number of trilobites with one or more planktic stages. However, species and families with exclusively benthic early stages still constituted about half of the Ordovician trilobite diversity. The first trilobites with planktic larvae might have been present in the Miaolingian, but their earliest fossil record is from the mid-Furongian. The appearance of planktic forms was accentuated later in the Ordovician with many trilobite lineages adapting a multi-staged planktic mode of life – more than one developmental stage colonizing the water column during ontogeny. Between the Miaolingian and the Middle Ordovician, both species- and family-level data show a progressive increase in the number of taxa incorporating planktic larvae in their development, highlighting a gradual transition in the structure of marine ecosystems during the early Paleozoic.

Longitudinal expansion fitness of brachiopod genera controlled by the Wilson cycle

The brachiopods constitute one of the major components of the marine metazoan fossil record. On the other hand their apparent decline in importance in forming benthic communities through the Phanerozoic is one of the most striking macroevolutionary and macroecological patterns. Here we analyzed changes in average latitudinal and longitudinal ranges – indices for success of spatial expansion of brachiopod genera – during post-Cambrian Phanerozoic, and compared their fluctuation and scaling behaviour to the changes in continental fragmentation. The results revealed that latitudinal ranges on the longest time scales were highly constrained, while longitudinal ranges shown persistent decrease. The scale-by-scale correlation analysis of Haar fluctuations revealed that there is positive functional dependence of longitudinal ranges at the longest time scales with continental fragmentation. Moreover the ratio of average longitudinal to latitudinal ranges was positively correlated to the continental fragmentation at all time scales. The long term minima in longitudinal ranges and the least elongated shapes in E-W direction of geographic ranges were found during the maximal amalgamation of the Pangaea during Triassic and Jurassic. The failure for brachiopods to regain the dominance in marine biosphere after P-Tr extinction should be related to the tectonic restrictions on their longitudinal ranges during the maximally supercontinental conditions of the planet. Therefore, the pattern exemplified by brachiopods shows that the spatial expansion success (fitness) of a major clade at an eon time scale could be a direct consequence of the multi-scale tectonic reconfigurations.

Testing COI primers for ichthyoplankton metabarcoding and their capability to assess local mesozooplankton communities

DNA metabarcoding is particularly helpful for monitoring taxonomically complex communities and hard to identify morphologically, such as several zoo and ichthyoplankton, which contain eggs and larval stages of unknown species. However, the efficiency of metabarcoding in diversity recovery is dependent on the targeted genetic markers and primers employed. In this work, we compared the performance of three different primer pairs from cytochrome oxidase subunit I (COI) genetic marker in species detection from marine mesozooplankton samples and its potential to be implemented in biomonitoring programs. We employed the mlCOIintF/LoboR1 primer combination targeting marine metazoans, and two newly designed fish-specific primer cocktails for targeting the ichthyoplankton. Mesozooplankton samples were collected at 4 locations on the Portuguese coast – 1 in the northwest (Viana do Castelo) and 3 in the south (coastal lagoons of Ria de Alvor and Ria Formosa, and in the river Guadiana estuary). Bulk community DNA was extracted using a non-destructive protocol and amplicon libraries produced for the 3 primers combinations. After quality-filtering bioinformatic steps, we obtained 3.04 x 105 usable sequences, of which 76.26% were clustered into OTUs (operational taxonomic units) and 46.30% were identified at species level - corresponding to 103 taxa from 8 different metazoan Phyla. The most diverse classes were Malacostraca, Actinopterygii, and Copepoda. As expected, the generic primer pair for marine metazoa (mlCOIintF/LoboR1) retrieved a higher number of species (94) compared with the fish-specific primer cocktails (30). Nevertheless, 9 % of the total species were identified exclusively by the cocktails, of which 42% were fish. These results confirmed the potential of metabarcoding as a tool for profiling zooplankton communities and to assess ichthyoplankton diversity. Multiple primers pairs increased species detection from different taxonomic groups, being the protocol optimization for fish-specific primer cocktails, the next step for its implementation in fish stock assessments.

ENVIRONMENTAL DNA IN AN OCEAN OF CHANGE: STATUS, CHALLENGES AND PROSPECTS

Environmental DNA (eDNA) studies have burgeoned over the last two decades and the application of eDNA has increased exponentially since 2010, albeit at a slower pace in the marine system. We provide a literature overview on marine metazoan eDNA studies and assess recent achievements in answering questions related to species distributions, biodiversity and biomass. We investigate which are the better studied taxonomic groups, geographic regions and the genetic markers used. We evaluate the use of eDNA for addressing ecological and environmental issues through food web, ecotoxicological, surveillance and management studies. Based on this state of the art, we highlight exciting prospects of eDNA for marine time series, population genetic studies, the use of natural sampler DNA, and eDNA data for building trophic networks and ecosystem models. We discuss the current limitations, in terms of marker choice and incompleteness of reference databases. We also present recent advances using experiments and modeling to better understand persistence, decay and dispersal of eDNA in coastal and oceanic systems. Finally, we explore promising avenues for marine eDNA research, including autonomous or passive eDNA sampling, as well as the combined applications of eDNA with different surveillance methods and further molecular advances.&#x0D; Keywords: environmental DNA, DNA metabarcoding, marine metazoa, biodiversity, population genetics, natural sampler DNA, diet analysis.

Mitochondrial Genome of Nonmodel Marine Metazoans by Next-Generation Sequencing (NGS).

Mitochondrial genomes (mtgenome) represent an important source of information for addressing fundamental evolutionary, phylogeographic, systematic, and ecological questions in marine organisms. In the last two decades the advent of high-throughput next-generation sequencing (NGS) has provided an unprecedented possibility to access large amount of genomic data and, as such, there has been a rapid growth in mtgenome resources and studies. In particular, NGS strategies represent a great advantage for investigating nonmodel marine organisms for which no or limited genomic resources are available. Here, we describe a routinely used standardized protocol to obtain mtgenome of nonmodel marine organisms by NGS. The protocol is composed of five main steps, including DNA extraction, DNA fragmentation, library preparation, high-throughput sequencing, and bioinformatic analyses. Each of the first three steps is followed by size/quality and concentration validations. The advantages of the described protocol rely on the assumption that no a priori information on mtgenome of the studied organism is needed and on its versatility as researchers may choose several kits for DNA extraction and library preparation and adopt different methods for DNA fragmentation depending on their needs, experience, and suppliers.

Geologic controls on phytoplankton elemental composition.

Planktonic organic matter forms the base of the marine food web, and its nutrient content (C:N:Porg) governs material and energy fluxes in the ocean. Over Earth history, C:N:Porg had a crucial role in marine metazoan evolution and global biogeochemical dynamics, but the geologic history of C:N:Porg is unknown, and it is often regarded constant at the "Redfield" ratio of ∼106:16:1. We calculated C:N:Porg through Phanerozoic time by including nutrient- and temperature-dependent C:N:Porg parameterizations in a model of the long-timescale biogeochemical cycles. We infer a decrease from high Paleozoic C:Porg and N:Porg to present-day ratios, which stems from a decrease in the global average temperature and an increase in seawater phosphate availability. These changes in the phytoplankton's growth environment were driven by various Phanerozoic events: specifically, the middle to late Paleozoic expansion of land plants and the Triassic breakup of the supercontinent Pangaea, which increased continental weatherability and the fluxes of weathering-derived phosphate to the oceans. The resulting increase in the nutrient content of planktonic organic matter likely impacted the evolution of marine fauna and global biogeochemistry.

Geologic controls on phytoplankton elemental composition

Planktonic organic matter forms the base of the marine food web, and its nutrient content (C:N:Porg) governs material and energy fluxes in the ocean. Over Earth history, C:N:Porg had a crucial role in marine metazoan evolution and global biogeochemical dynamics, but the geologic history of C:N:Porg is unknown, and it is often regarded constant at the "Redfield" ratio of ∼106:16:1. We calculated C:N:Porg through Phanerozoic time by including nutrient- and temperature-dependent C:N:Porg parameterizations in a model of the long-timescale biogeochemical cycles. We infer a decrease from high Paleozoic C:Porg and N:Porg to present-day ratios, which stems from a decrease in the global average temperature and an increase in seawater phosphate availability. These changes in the phytoplankton's growth environment were driven by various Phanerozoic events: specifically, the middle to late Paleozoic expansion of land plants and the Triassic breakup of the supercontinent Pangaea, which increased continental weatherability and the fluxes of weathering-derived phosphate to the oceans. The resulting increase in the nutrient content of planktonic organic matter likely impacted the evolution of marine fauna and global biogeochemistry.

Phanerozoic parasitism and marine metazoan diversity: dilution versus amplification.

Growing evidence suggests that biodiversity mediates parasite prevalence. We have compiled the first global database on occurrences and prevalence of marine parasitism throughout the Phanerozoic and assess the relationship with biodiversity to test if there is support for amplification or dilution of parasitism at the macroevolutionary scale. Median prevalence values by era are 5% for the Paleozoic, 4% for the Mesozoic, and a significant increase to 10% for the Cenozoic. We calculated period-level shareholder quorum sub-sampled (SQS) estimates of mean sampled diversity, three-timer (3T) origination rates, and 3T extinction rates for the most abundant host clades in the Paleobiology Database to compare to both occurrences of parasitism and the more informative parasite prevalence values. Generalized linear models (GLMs) of parasite occurrences and SQS diversity measures support both the amplification (all taxa pooled, crinoids and blastoids, and molluscs) and dilution hypotheses (arthropods, cnidarians, and bivalves). GLMs of prevalence and SQS diversity measures support the amplification hypothesis (all taxa pooled and molluscs). Though likely scale-dependent, parasitism has increased through the Phanerozoic and clear patterns primarily support the amplification of parasitism with biodiversity in the history of life.This article is part of the theme issue ‘Infectious disease macroecology: parasite diversity and dynamics across the globe’.

A synthesis tree of the Copepoda: integrating phylogenetic and taxonomic data reveals multiple origins of parasitism.

The Copepoda is a clade of pancrustaceans containing 14,485 species that are extremely varied in their morphology and lifestyle. Not only do copepods dominate marine plankton and sediment communities and make up a sizeable component of the freshwater plankton, but over 6,000 species are symbiotically associated with every major phylum of marine metazoans, mostly as parasites. Unfortunately, our understanding of copepod evolutionary relationships is relatively limited in part because of their extremely divergent morphology, sparse taxon sampling in molecular phylogenetic analyses, a reliance on only a handful of molecular markers, and little taxonomic overlap between phylogenetic studies. Here, a synthesis tree method is used to integrate published phylogenies into a more comprehensive tree of copepods by leveraging phylogenetic and taxonomic data. A literature review in this study finds fewer than 500 species of copepods have been sampled in molecular phylogenetic studies. Using the Open Tree of Life platform, those taxa that have been sampled in previous phylogenetic studies are grafted together and combined with the underlying copepod taxonomic hierarchy from the Open Tree of Life Taxonomy to make a synthesis phylogeny of all copepod species. Taxon sampling with respect to molecular phylogenetic analyses is reviewed for all orders of copepods and shows only 3% of copepod species have been sampled in phylogenetic studies. The resulting synthesis phylogeny reveals copepods have transitioned to a parasitic lifestyle on at least 14 occasions. We examine the underlying phylogenetic, taxonomic, and natural history data supporting these transitions to parasitism; review the species diversity of each parasitic clade; and identify key areas for further phylogenetic investigation.