Ctenophore relationships and their placement as the sister group to all other animals

Abstract

Ctenophora, comprising approximately 200 described species, is an important lineage for understanding metazoan evolution and is of great ecological and economic importance. Ctenophore diversity includes species with unique colloblasts used for prey capture, smooth and striated muscles, benthic and pelagic lifestyles, and locomotion with ciliated paddles or muscular propulsion. However, the ancestral states of traits are debated and relationships among many lineages are unresolved. Here, using 27 newly sequenced ctenophore transcriptomes, publicly available data and methods to control systematic error, we establish the placement of Ctenophora as the sister group to all other animals and refine the phylogenetic relationships within ctenophores. Molecular clock analyses suggest modern ctenophore diversity originated approximately 350 million years ago ± 88 million years, conflicting with previous hypotheses, which suggest it originated approximately 65 million years ago. We recover Euplokamis dunlapae-a species with striated muscles-as the sister lineage to other sampled ctenophores. Ancestral state reconstruction shows that the most recent common ancestor of extant ctenophores was pelagic, possessed tentacles, was bioluminescent and did not have separate sexes. Our results imply at least two transitions from a pelagic to benthic lifestyle within Ctenophora, suggesting that such transitions were more common in animal diversification than previously thought.

Fig. 1

Exemplar morphological forms of Ctenophora. a) Cydippid morphology (ovate body, long tentacles); photograph taken by James Townsend. b) Lobate morphology (reduced tentacles, large lobes). c) Beroida morphology (lacking tentacles and lobes). d) Platyctenida morphology (flattened, long tentacles). e) Cestida morphology (ribbon-like); photograph taken by Roberto Pillon and contrast adjusted in Adobe Photoshop.

Fig. 2

Relationships among metazoans inferred with the CAT-GTR substitution model and dataset Metazoa_Choano_RCFV_strict. All nodes have 100% PP. Inferred relationships among phyla are identical to those inferred with other models and datasets (Supplementary Figs. S1–S15; Supplementary Discussion). Scale bar in expected substitutions per site. Silhouette images downloaded from phylopic.org.

Fig. 3

Evolutionary relationships among Ctenophora and ancestral character state reconstruction of general body plan. Traditional orders labeled with colors matching corresponding body plan morphotype. Nodes are labelled with pie charts depicting posterior probability of character states. Phylogeny was inferred with dataset Ctenophore_RCFV_LB. Lines connect photographs of exemplars with species identity. Sponge and cnidarian outgroups that were used to root the tree were removed for illustrative purposes. Nodes have 100% BS or 1.00 PP support unless otherwise noted (BS/PP).

Fig. 4

Evolutionary relationships of Ctenophora and ancestral character state reconstruction of benthic vs. pelagic lifestyle. Nodes (and unique taxa) are labelled with pie charts depicting posterior probability of character states. Traditional orders are labeled. a) Phylogeny was inferred with dataset Ctenophore_RCFV_LB. Sponge and cnidarian outgroups that were used to root the tree were removed for illustrative purposes. Nodes have 100% BS or 1.00 PP support unless otherwise noted (BS/PP). b) Benthic Platyctenida, Ceoloplana astericola on a seastar. c) Pelagic Pleurobrachia bachei. d) Benthic Lobata, Lobatolampea tetragona.

Fig. 5

Evolutionary relationships of Ctenophora and ancestral sate reconstruction of primary feeding mode. Traditional orders are labeled. Nodes are labelled with posterior probability of character states. Phylogeny was inferred with dataset Ctenophore_RCFV_LB. Sponge and cnidarian outgroups that were used to root the tree were removed for illustrative purposes. Nodes have 100% BS or 1.00 PP support unless otherwise noted (BS/PP).