Abstract

BackgroundThe phylogeny of Cnidaria has been a source of debate for decades, during which nearly all-possible relationships among the major lineages have been proposed. The ecological success of Cnidaria is predicated on several fascinating organismal innovations including stinging cells, symbiosis, colonial body plans and elaborate life histories. However, understanding the origins and subsequent diversification of these traits remains difficult due to persistent uncertainty surrounding the evolutionary relationships within Cnidaria. While recent phylogenomic studies have advanced our knowledge of the cnidarian tree of life, no analysis to date has included genome-scale data for each major cnidarian lineage.ResultsHere we describe a well-supported hypothesis for cnidarian phylogeny based on phylogenomic analyses of new and existing genome-scale data that includes representatives of all cnidarian classes. Our results are robust to alternative modes of phylogenetic estimation and phylogenomic dataset construction. We show that two popular phylogenomic matrix construction pipelines yield profoundly different datasets, both in the identities and in the functional classes of the loci they include, but resolve the same topology. We then leverage our phylogenetic resolution of Cnidaria to understand the character histories of several critical organismal traits. Ancestral state reconstruction analyses based on our phylogeny establish several notable organismal transitions in the evolutionary history of Cnidaria and depict the ancestral cnidarian as a solitary, non-symbiotic polyp that lacked a medusa stage. In addition, Bayes factor tests strongly suggest that symbiosis has evolved multiple times independently across the cnidarian radiation.ConclusionsCnidaria have experienced more than 600 million years of independent evolution and in the process generated an array of organismal innovations. Our results add significant clarification on the cnidarian tree of life and the histories of some of these innovations. Further, we confirm the existence of Acraspeda (staurozoans plus scyphozoans and cubozoans), thus reviving an evolutionary hypothesis put forward more than a century ago.

Highlights

  • The phylogeny of Cnidaria has been a source of debate for decades, during which most-possible relationships among the major lineages have been proposed

  • The ecological success of Cnidaria is predicated on several fascinating organismal innovations including stinging cells called cnidocytes, relationships with phototrophic endosymbiotic eukaryotes, colonial body plans and the metagenetic life cycle that includes medusa and polyp stages

  • Our findings suggested significant differences between the composition of datasets produced by OF-PTP, Agalma and those reported in recent phylogenomic analyses of Cnidaria [11, 10]

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Summary

Introduction

The phylogeny of Cnidaria has been a source of debate for decades, during which most-possible relationships among the major lineages have been proposed. Endocnidozoa is an entirely parasitic clade that includes about 2200 species of Myxozoa (minute endoparasites of invertebrates and vertebrates with complex life cycles) and the monotypic Polypodiozoa (a parasite that infects the eggs of sturgeon and paddlefish). It was not until after a long line of evidence that it became clear that Myxozoa was a clade within Cnidaria (reviewed in [2, 3]). The ecological success of Cnidaria is predicated on several fascinating organismal innovations including stinging cells called cnidocytes, relationships with phototrophic endosymbiotic eukaryotes, colonial body plans and the metagenetic life cycle that includes medusa (jellyfish) and polyp stages.

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