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Cited by 259Marine Invertebrate Physiology and EcologyGenomics and Phylogenetic StudiesProtist diversity and phylogeny

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Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits

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Kayal, Ehsan, Bentlage, Bastian, Sabrina Pankey, M., Ohdera, Aki H., Medina, Monica, Plachetzki, David C., Collins, Allen G., Ryan, Joseph F.·2018·BMC Evolutionary Biology
DOI 10.1186/s12862-018-1142-0PMC PMC5932825
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Abstract

The 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. Here 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. Cnidaria 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.

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Fig. 1 Exemplar staurozoans and competing phylogenetic hypotheses for the position of Stuarozoa within Medusozoa. a Haliclystus auricula. Credit: Marco Faasse; cropped. b Haliclystus “sanjuanensis”. Credit: Ron J. Larson. c Craterolophus convolvulus. Credit: Stauromedusae UK & David Fenwick; cropped. d Lucernaria quadricornis. Credit: Alexander Semenov. e Calvadosia cruxmelitensis Credit: Stauromedusae UK & David Fenwick; cropped. f Competing hypotheses for the phylogenetic position of Staurozoa within Medusozoa. Top from [25, 4] and Van Iten et al. [24]; bottom from Zapata et al. [10]
Fig. 1 Exemplar staurozoans and competing phylogenetic hypotheses for the position of Stuarozoa within Medusozoa. a Haliclystus auricula. Credit: Marco Faasse; cropped. b Haliclystus “sanjuanensis”. Credit: Ron J. Larson. c Craterolophus convolvulus. Credit: Stauromedusae UK & David Fenwick; cropped. d Lucernaria quadricornis. Credit: Alexander Semenov. e Calvadosia cruxmelitensis Credit: Stauromedusae UK & David Fenwick; cropped. f Competing hypotheses for the phylogenetic position of Staurozoa within Medusozoa. Top from [25, 4] and Van Iten et al. [24]; bottom from Zapata et al. [10]CC BY · PubMed Central
Fig. 2 Exemplar ceriantharians and octocorals and competing hypotheses for the position of Ceriantharia within Anthozoa. a Ceriantharian tube anemone adult. Credit: NOAA Okeanos Explorer Program, Galapagos Rift Expedition, 2011; cropped. b Ceriantharian tube anemone pelagic larva. Credit: A. G. Collins, Bonaire, 2016. c Octocorallian, the sea pansy, Renilla reniformis. Credit: J. Ryan. d Competing hypotheses for the phylogenetic position of Ceriantharia within Anthozoa. Top from Daly et al. [31, 32] and Zapata et al. [10]; bottom from Stampar et al. [6]
Fig. 2 Exemplar ceriantharians and octocorals and competing hypotheses for the position of Ceriantharia within Anthozoa. a Ceriantharian tube anemone adult. Credit: NOAA Okeanos Explorer Program, Galapagos Rift Expedition, 2011; cropped. b Ceriantharian tube anemone pelagic larva. Credit: A. G. Collins, Bonaire, 2016. c Octocorallian, the sea pansy, Renilla reniformis. Credit: J. Ryan. d Competing hypotheses for the phylogenetic position of Ceriantharia within Anthozoa. Top from Daly et al. [31, 32] and Zapata et al. [10]; bottom from Stampar et al. [6]CC BY · PubMed Central
Fig. 3 Relationship between sparse data representation and the retention of contaminated sequences in phylogenomic data matrices as illustrated by myxozoan species. We conducted BLAST similarity searches against a metazoan genome database for all myxozoan sequences present in both the AG_62tx and OF-PTP_62tx matrices. In addition, we noted how many myxozoan species were present in each partition. Myxozoans are internal parasites of teleost fishes and we noted significant contamination in transcriptome data from these host species. The Agalma pipeline produces a large, but sparse matrix as compared to OF-PTP (Fig. 4). In cases where contamination is common, as with myxozoan data, sparse data matrices have high numbers of partitions with single species represented per clade, which in turn are enriched for contaminant sequences. Partitions with greater than one species of myxozoan present have a lower potential to include contamination. The OF-PTP pipeline produces a denser data matrix, which makes it inherently less prone to selecting contaminants
Fig. 3 Relationship between sparse data representation and the retention of contaminated sequences in phylogenomic data matrices as illustrated by myxozoan species. We conducted BLAST similarity searches against a metazoan genome database for all myxozoan sequences present in both the AG_62tx and OF-PTP_62tx matrices. In addition, we noted how many myxozoan species were present in each partition. Myxozoans are internal parasites of teleost fishes and we noted significant contamination in transcriptome data from these host species. The Agalma pipeline produces a large, but sparse matrix as compared to OF-PTP (Fig. 4). In cases where contamination is common, as with myxozoan data, sparse data matrices have high numbers of partitions with single species represented per clade, which in turn are enriched for contaminant sequences. Partitions with greater than one species of myxozoan present have a lower potential to include contamination. The OF-PTP pipeline produces a denser data matrix, which makes it inherently less prone to selecting contaminantsCC BY · PubMed Central
Fig. 4 Comparisons of new and previously published phylogenomic datasets for Cnidaria reveal significant differences. a Histograms showing the distributions of alignment lengths for partitions included in the OF-PTP_62tx, AG_62tx and two previously published phylogenomic matrices [11, 10]. b The number of taxa plotted against the average taxon occupancy for each dataset. Size of each circle is based on number of partitions (see inset in a). p denotes preliminary datasets. c Venn diagram indicating the overlap in N. vectensis gene identities from partitions present in each dataset. The most similar datasets are AG_62tx and that from Zapata et al. [10], which are both based on Agalma [45]. d Composition, enrichment and depletion of GO terms associated with the cellular component category from the N. vectensis sequences present across partitions. Left, the composition of unique cellular component terms are shown as bar plots for each dataset. Only terms that are significantly enriched or depleted relative to their frequencies in the N. vectensis protein set in at least one dataset are shown. Right, the identities of each cellular component term and their enrichment or depletion for each dataset. Black = depleted. White = enriched. Grey = not significant. For b-c, datasets are color coded as in a
Fig. 4 Comparisons of new and previously published phylogenomic datasets for Cnidaria reveal significant differences. a Histograms showing the distributions of alignment lengths for partitions included in the OF-PTP_62tx, AG_62tx and two previously published phylogenomic matrices [11, 10]. b The number of taxa plotted against the average taxon occupancy for each dataset. Size of each circle is based on number of partitions (see inset in a). p denotes preliminary datasets. c Venn diagram indicating the overlap in N. vectensis gene identities from partitions present in each dataset. The most similar datasets are AG_62tx and that from Zapata et al. [10], which are both based on Agalma [45]. d Composition, enrichment and depletion of GO terms associated with the cellular component category from the N. vectensis sequences present across partitions. Left, the composition of unique cellular component terms are shown as bar plots for each dataset. Only terms that are significantly enriched or depleted relative to their frequencies in the N. vectensis protein set in at least one dataset are shown. Right, the identities of each cellular component term and their enrichment or depletion for each dataset. Black = depleted. White = enriched. Grey = not significant. For b-c, datasets are color coded as in aCC BY · PubMed Central
Fig. 5 ML and Bayesian analyses of the OF-PTP_75tx dataset confidently resolve cnidarian phylogeny and depict the three major lineages. Shown is the topology from ML analyses (Additional file 9). Nodes not present in the Bayesian analysis (Additional file 10) are collapsed to polytomies. All nodes receive maximum support in both analyses except where indicated as bootstraps and posterior probabilities. Circles at terminal tips indicate the number of data partitions present per taxon. Blue circles indicate data produced here, while orange circles indicate publically available data. All datasets are derived from RNA-seq data except when whole genome assemblies where used as indicated in Red
Fig. 5 ML and Bayesian analyses of the OF-PTP_75tx dataset confidently resolve cnidarian phylogeny and depict the three major lineages. Shown is the topology from ML analyses (Additional file 9). Nodes not present in the Bayesian analysis (Additional file 10) are collapsed to polytomies. All nodes receive maximum support in both analyses except where indicated as bootstraps and posterior probabilities. Circles at terminal tips indicate the number of data partitions present per taxon. Blue circles indicate data produced here, while orange circles indicate publically available data. All datasets are derived from RNA-seq data except when whole genome assemblies where used as indicated in RedCC BY · PubMed Central
Fig. 6 Studies of character evolution reveal a dynamic history of gain and loss for each trait examined. We conducted stochastic character mapping [53, 55] on our cnidarian ingroup topology (branch lengths not shown) for each character state included. Ancestral state reconstructions of each character at each node are shown as pie charts representing posterior probabilities. The color-coded presence or absence of each character is shown at Right. Our results suggest that the ancestral state of Cnidaria was a non-symbiotic, solitary polyp, however, other characters are equivocal at this node
Fig. 6 Studies of character evolution reveal a dynamic history of gain and loss for each trait examined. We conducted stochastic character mapping [53, 55] on our cnidarian ingroup topology (branch lengths not shown) for each character state included. Ancestral state reconstructions of each character at each node are shown as pie charts representing posterior probabilities. The color-coded presence or absence of each character is shown at Right. Our results suggest that the ancestral state of Cnidaria was a non-symbiotic, solitary polyp, however, other characters are equivocal at this nodeCC BY · PubMed Central
Fig. 7 Summary of results. Our working hypothesis for the topology of major cnidarian lineages based on the present study
Fig. 7 Summary of results. Our working hypothesis for the topology of major cnidarian lineages based on the present studyCC BY · PubMed Central

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Metadata

Authors
Kayal, E., Bentlage, B., Sabrina Pankey, M., Ohdera, A. H., Medina, M., Plachetzki, D. C., Collins, A. G., & Ryan, J. F.
Affiliations
  • Smithsonian Institution (US)
  • Pennsylvania State University (US)
  • University of New Hampshire (US)
  • University of Florida (US)
Corresponding author
  • Plachetzki, David C.
  • Ryan, Joseph F.
ORCID
Venue
BMC Evolutionary Biology
Publisher
Springer Science and Business Media LLC
Published
2018-04-13
Volume
18
Issue
1
Pages
68
ISSN
1471-2148 (ISSN-L)
DOI
10.1186/s12862-018-1142-0
PMC
PMC5932825
OpenAlex
W2807223659
Cited by
255
References
104
Citations by year
2026: 15 · 2025: 28 · 2024: 35 · 2023: 37 · 2022: 28 · 2021: 40 · 2020: 40 · 2019: 28 · 2018: 4
FWCI
20.61
Type
journal article
Language
en
Open access
Licence
Locations
  • BMC Evolutionary Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • HAL (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • NOAA Institutional Repository (submittedVersion)
Funders
  • Smithsonian Institution
  • Directorate for Biological Sciences (OIA-1457769)
  • National Institute of Food and Agriculture (Hatch Project 00654)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
Keywords
genome-scale data, ancestral state reconstruction, symbiosis evolution, nematocysts, Scyphozoa, cubozoans

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