Steven H. D. Haddock

Broad phylogenomic sampling improves resolution of the animal tree of life.

Long-held ideas regarding the evolutionary relationships among animals have recently been upended by sometimes controversial hypotheses based largely on insights from molecular data. These new hypotheses include a clade of moulting animals (Ecdysozoa) and the close relationship of the lophophorates to molluscs and annelids (Lophotrochozoa). Many relationships remain disputed, including those that are required to polarize key features of character evolution, and support for deep nodes is often low. Phylogenomic approaches, which use data from many genes, have shown promise for resolving deep animal relationships, but are hindered by a lack of data from many important groups. Here we report a total of 39.9 Mb of expressed sequence tags from 29 animals belonging to 21 phyla, including 11 phyla previously lacking genomic or expressed-sequence-tag data. Analysed in combination with existing sequences, our data reinforce several previously identified clades that split deeply in the animal tree (including Protostomia, Ecdysozoa and Lophotrochozoa), unambiguously resolve multiple long-standing issues for which there was strong conflicting support in earlier studies with less data (such as velvet worms rather than tardigrades as the sister group of arthropods), and provide molecular support for the monophyly of molluscs, a group long recognized by morphologists. In addition, we find strong support for several new hypotheses. These include a clade that unites annelids (including sipunculans and echiurans) with nemerteans, phoronids and brachiopods, molluscs as sister to that assemblage, and the placement of ctenophores as the earliest diverging extant multicellular animals. A single origin of spiral cleavage (with subsequent losses) is inferred from well-supported nodes. Many relationships between a stable subset of taxa find strong support, and a diminishing number of lineages remain recalcitrant to placement on the tree.

The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution

Introduction An understanding of ctenophore biology is critical for reconstructing events that occurred early in animal evolution. The phylogenetic relationship of ctenophores (comb jellies) to other animals has been a source of long-standing debate. Until recently, it was thought that Porifera (sponges) was the earliest diverging animal lineage, but recent reports have instead suggested Ctenophora as the earliest diverging animal lineage. Because ctenophores share some of the same complex cell types with bilaterians (such as neural and mesodermal cells), the phylogenetic position of ctenophores affects how we think about the early evolution of these cell types. The phylogenetic position of the ctenophore Mnemiopsis leidyi and its implications regarding the origin of mesodermal cell types. (A) Adult M. leidyi. (B) Summary of the relationships of the five main branches of animals and the outgroup Choanoflagellata

Recurrent jellyfish blooms are a consequence of global oscillations

A perceived recent increase in global jellyfish abundance has been portrayed as a symptom of degraded oceans. This perception is based primarily on a few case studies and anecdotal evidence, but a formal analysis of global temporal trends in jellyfish populations has been missing. Here, we analyze all available long-term datasets on changes in jellyfish abundance across multiple coastal stations, using linear and logistic mixed models and effect-size analysis to show that there is no robust evidence for a global increase in jellyfish. Although there has been a small linear increase in jellyfish since the 1970s, this trend was unsubstantiated by effect-size analysis that showed no difference in the proportion of increasing vs. decreasing jellyfish populations over all time periods examined. Rather, the strongest nonrandom trend indicated jellyfish populations undergo larger, worldwide oscillations with an approximate 20-y periodicity, including a rising phase during the 1990s that contributed to the perception of a global increase in jellyfish abundance. Sustained monitoring is required over the next decade to elucidate with statistical confidence whether the weak increasing linear trend in jellyfish after 1970 is an actual shift in the baseline or part of an oscillation. Irrespective of the nature of increase, given the potential damage posed by jellyfish blooms to fisheries, tourism, and other human industries, our findings foretell recurrent phases of rise and fall in jellyfish populations that society should be prepared to face.

Questioning the Rise of Gelatinous Zooplankton in the World's Oceans

During the past several decades, high numbers of gelatinous Zooplankton species have been reported in many estuarine and coastal ecosystems. Coupled with media-driven public perception, a paradigm has evolved in which the global ocean ecosystems are thought to he heading toward being dominated by “nuisance” jellyfish. We question this current paradigm by presenting a broad overview of gelatinous Zooplankton in a historical context to develop the hypothesis that population changes reflect the human-mediated alteration of global ocean ecosystems. To this end, we synthesize information related to the evolutionary context of contemporary gelatinous Zooplankton blooms, the human frame of reference for changes in gelatinous Zooplankton populations, and whether sufficient data are available to have established the paradigm. We conclude that the current paradigm in which it is believed that there has been a global increase in gelatinous Zooplankton is unsubstantiated, and we develop a strategy for addressing the critical questions about long-term, human-related changes in the sea as they relate to gelatinous Zooplankton blooms.

Natural egg mass deposition by the Humboldt squid ( Dosidicus gigas ) in the Gulf of California and characteristics of hatchlings and paralarvae

The jumbo or Humboldt squid, Dosidicus gigas, is an important fisheries resource and a significant participant in regional ecologies as both predator and prey. It is the largest species in the oceanic squid family Ommastrephidae and has the largest known potential fecundity of any cephalopod, yet little is understood about its reproductive biology. We report the first discovery of a naturally deposited egg mass of Dosidicus gigas, as well as the first spawning of eggs in captivity. The egg mass was found in warm water (25‐278C) at a depth of 16 m and was far larger than the egg masses of any squid species previously reported. Eggs were embedded in a watery, gelatinous matrix and were individually surrounded by a unique envelope external to the chorion. This envelope was present in both wild and captive-spawned egg masses, but it was not present in artificially fertilized eggs. The wild egg mass appeared to be resistant to microbial infection, unlike the incomplete and damaged egg masses spawned in captivity, suggesting that the intact egg mass protects the eggs within. Chorion expansion was also more extensive in the wild egg mass. Hatchling behaviours included proboscis extension, chromatophore activity, and a range of swimming speeds that may allow them to exercise some control over their distribution in the wild.

A comparison across non-model animals suggests an optimal sequencing depth for de novo transcriptome assembly

BackgroundThe lack of genomic resources can present challenges for studies of non-model organisms. Transcriptome sequencing offers an attractive method to gather information about genes and gene expression without the need for a reference genome. However, it is unclear what sequencing depth is adequate to assemble the transcriptome de novo for these purposes.ResultsWe assembled transcriptomes of animals from six different phyla (Annelids, Arthropods, Chordates, Cnidarians, Ctenophores, and Molluscs) at regular increments of reads using Velvet/Oases and Trinity to determine how read count affects the assembly. This included an assembly of mouse heart reads because we could compare those against the reference genome that is available. We found qualitative differences in the assemblies of whole-animals versus tissues. With increasing reads, whole-animal assemblies show rapid increase of transcripts and discovery of conserved genes, while single-tissue assemblies show a slower discovery of conserved genes though the assembled transcripts were often longer. A deeper examination of the mouse assemblies shows that with more reads, assembly errors become more frequent but such errors can be mitigated with more stringent assembly parameters.ConclusionsThese assembly trends suggest that representative assemblies are generated with as few as 20 million reads for tissue samples and 30 million reads for whole-animals for RNA-level coverage. These depths provide a good balance between coverage and noise. Beyond 60 million reads, the discovery of new genes is low and sequencing errors of highly-expressed genes are likely to accumulate. Finally, siphonophores (polymorphic Cnidarians) are an exception and possibly require alternate assembly strategies.

Phylogenetics of Trachylina (Cnidaria: Hydrozoa) with new insights on the evolution of some problematical taxa

Some of the most interesting and enigmatic cnidarians are classified within the hydrozoan subclass Trachylina. Despite being relatively depauperate in species richness, the clade contains four taxa typically accorded ordinal status: Actinulida, Limnomedusae, Narcomedusae and Trachymedusae. We bring molecular data (mitochondrial 16S and nuclear small and large subunit ribosomal genes) to bear on the question of phylogenetic relationships within Trachylina. Surprisingly, we find that a diminutive polyp form, Microhydrula limopsicola (classified within Limnomedusae) is actually a previously unknown life stage of a species of Stauromedusae. Our data confirm that the interstitial form Halammohydra sp. (Actinulida) is derived from holopelagic direct developing ancestors, likely within the trachymedusan family Rhopalonematidae. Trachymedusae is shown to be diphyletic, suggesting that the polyp stage has been lost independently at least two times within trachyline evolution. Narcomedusae is supported as a monophyletic group likely also arising from trachymedusan ancestors. Finally, some data, albeit limited, suggest that some trachyline species names refer to cryptic species that have yet to be sorted taxonomically.

Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes

BackgroundCalcium-activated photoproteins are luciferase variants found in photocyte cells of bioluminescent jellyfish (Phylum Cnidaria) and comb jellies (Phylum Ctenophora). The complete genomic sequence from the ctenophore Mnemiopsis leidyi, a representative of the earliest branch of animals that emit light, provided an opportunity to examine the genome of an organism that uses this class of luciferase for bioluminescence and to look for genes involved in light reception. To determine when photoprotein genes first arose, we examined the genomic sequence from other early-branching taxa. We combined our genomic survey with gene trees, developmental expression patterns, and functional protein assays of photoproteins and opsins to provide a comprehensive view of light production and light reception in Mnemiopsis.ResultsThe Mnemiopsis genome has 10 full-length photoprotein genes situated within two genomic clusters with high sequence conservation that are maintained due to strong purifying selection and concerted evolution. Photoprotein-like genes were also identified in the genomes of the non-luminescent sponge Amphimedon queenslandica and the non-luminescent cnidarian Nematostella vectensis, and phylogenomic analysis demonstrated that photoprotein genes arose at the base of all animals. Photoprotein gene expression in Mnemiopsis embryos begins during gastrulation in migrating precursors to photocytes and persists throughout development in the canals where photocytes reside. We identified three putative opsin genes in the Mnemiopsis genome and show that they do not group with well-known bilaterian opsin subfamilies. Interestingly, photoprotein transcripts are co-expressed with two of the putative opsins in developing photocytes. Opsin expression is also seen in the apical sensory organ. We present evidence that one opsin functions as a photopigment in vitro, absorbing light at wavelengths that overlap with peak photoprotein light emission, raising the hypothesis that light production and light reception may be functionally connected in ctenophore photocytes. We also present genomic evidence of a complete ciliary phototransduction cascade in Mnemiopsis.ConclusionsThis study elucidates the genomic organization, evolutionary history, and developmental expression of photoprotein and opsin genes in the ctenophore Mnemiopsis leidyi, introduces a novel dual role for ctenophore photocytes in both bioluminescence and phototransduction, and raises the possibility that light production and light reception are linked in this early-branching non-bilaterian animal.

A golden age of gelata : past and future research on planktonic ctenophores and cnidarians

The study of the natural history of gelatinous zooplankton (‘gelata’) reached a high point at the end of the 19th century, when scientists first began to understand the phylogenetic and ecological links between cnidarians and ctenophores. Siphonophores, carefully figured in their entirety, and gauze-like lobate ctenophores too fragile to touch, were described by the dozens. In the ensuing years, focus on zooplankton shifted toward more ‘industrial’ goals such as quantitative sampling using plankton nets. While plankton scientists were busy summing tattered parts, they lost sight of the whole jellies themselves, and a crustaceocentric view of the ocean came to dominate. During this period, the most dramatic breakthroughs in cnidarian research came from laboratory studies of neurobiology, physiology, and development, particularly of certain model organisms. Now, at the turn of this century, we have the opportunity to bring gelata back into primacy. Submersibles and remotely operated vehicles allow us to study entire life histories of organisms that we did not even know existed. The tools of molecular biology allow us to answer questions about development, evolution, and phylogeny that had reached a stalemate. Even in the surface waters, where it might be thought that there is little left to learn, in situ observations have revealed unexpected interactions and hidden diversity. The critical roles that these organisms play in the health of the oceans, their position at the crux of many evolutionary debates, and the tools for biotechnology that they provide, have led to resurgent public appreciation and awareness. Although advanced tools do not necessitate good science, we have few excuses for failing to bring about another golden age of gelata.

Phylogenomic Analyses Support Traditional Relationships within Cnidaria

Cnidaria, the sister group to Bilateria, is a highly diverse group of animals in terms of morphology, lifecycles, ecology, and development. How this diversity originated and evolved is not well understood because phylogenetic relationships among major cnidarian lineages are unclear, and recent studies present contrasting phylogenetic hypotheses. Here, we use transcriptome data from 15 newly-sequenced species in combination with 26 publicly available genomes and transcriptomes to assess phylogenetic relationships among major cnidarian lineages. Phylogenetic analyses using different partition schemes and models of molecular evolution, as well as topology tests for alternative phylogenetic relationships, support the monophyly of Medusozoa, Anthozoa, Octocorallia, Hydrozoa, and a clade consisting of Staurozoa, Cubozoa, and Scyphozoa. Support for the monophyly of Hexacorallia is weak due to the equivocal position of Ceriantharia. Taken together, these results further resolve deep cnidarian relationships, largely support traditional phylogenetic views on relationships, and provide a historical framework for studying the evolutionary processes involved in one of the most ancient animal radiations.