Medusozoan Phylogeny and Character Evolution Clarified by New Large and Small Subunit rDNA Data and an Assessment of the Utility of Phylogenetic Mixture Models

Abstract

A newly compiled data set of nearly complete sequences of the large subunit of the nuclear ribosome (LSU or 28S) sampled from 31 diverse medusozoans greatly clarifies the phylogenetic history of Cnidaria. These data have substantial power to discern among many of the competing hypotheses of relationship derived from prior work. Moreover, LSU data provide strong support at key nodes that were equivocal based on other molecular markers. Combining LSU sequences with those of the small subunit of the nuclear ribosome (SSU or 18S), we present a detailed working hypothesis of medusozoan relationships and discuss character evolution within this diverse clade. Stauromedusae, comprising the benthic, so-called stalked jellyfish, appears to be the sister group of all other medusozoans, implying that the free-swimming medusa stage, the motor nerve net, and statocysts of ecto-endodermal origin are features derived within Medusozoa. Cubozoans, which have had uncertain phylogenetic affinities since the elucidation of their life cycles, form a clade-named Acraspeda-with the scyphozoan groups Coronatae, Rhizostomeae, and Semaeostomeae. The polyps of both cubozoans and hydrozoans appear to be secondarily simplified. Hydrozoa is comprised by two well-supported clades, Trachylina and Hydroidolina. The position of Limnomedusae within Trachylina indicates that the ancestral hydrozoan had a biphasic life cycle and that the medusa was formed via an entocodon. Recently hypothesized homologies between the entocodon and bilaterian mesoderm are therefore suspect. Laingiomedusae, which has often been viewed as a close ally of the trachyline group Narcomedusae, is instead shown to be unambiguously a member of Hydroidolina. The important model organisms of the Hydra species complex are part of a clade, Aplanulata, with other hydrozoans possessing direct development not involving a ciliated planula stage. Finally, applying phylogenetic mixture models to our data proved to be of little additional value over a more traditional phylogenetic approach involving explicit hypothesis testing and bootstrap analyses under multiple optimality criteria. [18S; 28S; Cubozoa; Hydrozoa; medusa; molecular systematics; polyp; Scyphozoa; Staurozoa.].

Comprehensive phylogenomic analyses resolve cnidarian relationships and the origins of key organismal traits

“…This former view is borne out by our results showing strong support for Staurozoa as the sister group to Cubozoa plus Scyphozoa (Figures 5, 7) and is also in agreement with the topology of Zapata et al (2015), which had only weak support. Earlier phylogenetic analyses of rDNA and morphology also supported the view that Staurozoa is a distinct clade from Scyphozoa and Cubozoa, but instead suggested that Staurozoa was the sister group to the remaining medusozoans (Collins, et al 2006b;Van Iten, et al 2006).…”

“…Cnidarian phylogeny has been a source of debate for decades, with nearly every possible sister group relationship proposed among the major lineages of Medusozoa ( Figure 1) and Anthozoa ( Figure 2) (Collins 2009;Collins, et al 2006b;Daly, et al 2007;Stampar, et al 2014). Whole mitochondrial phylogenomic analyses have supported paraphyletic Anthozoa and Scyphozoa (Kayal, et al 2013;Park, et al 2012), but subsequent work suggested that these findings were due to saturation bias (Pratlong, et al 2017).…”

“…Defining different cnidarian life history stages is often difficult because of the many variations and exceptions exhibited within the wide variety of taxa (Cartwright and Nawrocki 2010;Leclere, et al 2009;Marques and Collins 2004). Our definition of the medusa as a liberated, propulsive life history stage bearing gonads (Cartwright and Nawrocki 2010) requires that the solitary, benthic members of Staurozoa are scored as possessing a derived polyp rather than a degenerated medusa as suggested earlier (Collins, et al 2006b;Kayal, et al 2013;Thiel 1966;Uchida 1972;Werner 1973) and the stolon stage of Polypodium hydriforme is scored as neither a medusa nor a polyp (Evans, et al 2008).…”

“…Critically, prior to the present study, relatively little evidence has been Collins et al (2006) and Van Iten et al (2006); bottom from Zapata et al (2015). brought to bear on the phylogenetic position of Staurozoa, whether it be from morphology (Hyman 1940;Kiderlen 1937;Marques and Collins 2004;Van Iten 1992;Van Iten, et al 2006), a small number of genes (Collins 2002;Collins, et al 2006a), or sparse representation (in terms of both data and taxon sampling) in an otherwise, large phylogenomic study (Zapata, et al 2015).…”

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

“…Within Hydrozoa (Cnidaria), an ancient phylogenetic divergence appears to have given rise to two primary clades with extant representatives, Trachylina and Hydroidolina (Collins, 2002;Collins et al, 2006a). In terms of species richness, the vast majority of hydrozoan diversity is contained within Hydroidolina (¼Leptolina sensu Schuchert, 2007).…”