Molecular Phylogenetics of the Siphonophora (Cnidaria), with Implications for the Evolution of Functional Specialization

Abstract

Siphonophores are a group of pelagic colonial hydrozoans (Cnidaria) that have long been of general interest because of the division of labor between the polyps and medusae that make up these "superorganisms." These polyps and medusae are each homologous to free living animals but are generated by an incomplete asexual budding process that leaves them physiologically integrated. They are functionally specialized for different tasks and are precisely organized within each colony. The number of functional types of polyps and medusae varies across taxa, and different authors have used this character to construct phylogenies polarized in opposite directions, depending on whether they thought siphonophore evolution proceeded by a reduction or an increase in functional specialization. We have collected taxa across all major groups of siphonophores, many of which are found exclusively in the deep sea, using remotely operated underwater vehicles (ROVs) and by SCUBA diving from ships in the open ocean. We have used 52 siphonophores and four outgroup taxa to estimate the siphonophore phylogeny with molecular data from the nuclear small subunit ribosomal RNA gene (18S) and the mitochondrial large subunit ribosomal RNA gene (16S). Parsimony reconstructions indicate that functionally specialized polyps and medusae have been gained and lost across the phylogeny. Maximum likelihood and Bayesian analyses of morphological data suggest that the transition rate for decreased functional specialization is greater than the transition rate for increased functional specialization for three out of the four investigated categories of polyps and medusae. The present analysis also bears on several long-standing questions about siphonophore systematics. It indicates that the cystonects are sister to all other siphonophores, a group that we call the Codonophora. We also find that the Calycophorae are nested within the Physonectae, and that the Brachystelia, a historically recognized grouping of short-stemmed taxa, are polyphyletic. [Cnidaria; colonial animals; deep sea; division of labor; functional specialization; Hydrozoa; phylogenetics; Siphonophores.].

Phylogenetics of Hydroidolina (Hydrozoa: Cnidaria)

“…We did not however find support for Codonophora (sensu Dunn et al, 2005). Our ML analysis placed the cystonect Physalia as the sister taxon to Calycophorae (Figure 1), not as the earliest diverging member of siphonophores (Collins 2002;Dunn et al, 2005). The MP analysis also recovered a probable paraphyletic Physonectae, but unlike the ML analyses, Physalia was nested within Calycophorae (Figure 2).…”

“…Collins (2002) placed the cystonect Physalia as sister to the other included siphonophores and suggested that Physonectae may be paraphyletic with respect to the Calycophorae. A later study (Dunn et al, 2005), that considered additional taxa and two genes (18S and 16S) found that cystonects form a monophyletic group that is sister to the remaining siphonophores and the paraphyly of Physonectae was recovered with significant support. Dunn et al (2005) erected the name Codonophora to refer to the clade comprising taxa assigned to Physonectae and Calycophorae (i.e.…”

“…A later study (Dunn et al, 2005), that considered additional taxa and two genes (18S and 16S) found that cystonects form a monophyletic group that is sister to the remaining siphonophores and the paraphyly of Physonectae was recovered with significant support. Dunn et al (2005) erected the name Codonophora to refer to the clade comprising taxa assigned to Physonectae and Calycophorae (i.e. the clade that is sister to Cystonectae).…”

“…For example, phylogenetic analyses have shown that Hydrozoa comprises two well-supported, reciprocally monophyletic clades, Trachylina and Hydroidolina (Marques & Collins, 2004;Marques, 2001a;Collins, 2002;Collins et al, 2006;Van Iten et al, 2006). Siphonophorae is a clade (Collins, 2002;Dunn et al, 2005), but its phylogenetic position within Hydroidolina is uncertain (Collins, 2002;Collins et al, 2006). Similarly, there is strong support for the monophyly of Leptothecata Leclère et al, 2007), but no well-supported hypotheses have emerged regarding its relationship with other hydroidolinans.…”

“…In addition, with exception to studies on Kirchenpaueriidae (Peña Cantero & Marques, 1999), Corynidae (Collins et al, 2005), Siphonophorae (Dunn et al, 2005), Tubulariidae (Marques & Migotto, 2001), Campanulariidae (Govindarajan et al, 2006), HebellidaeLafoeidae and Plumularioidea (Leclère et al, 2006), relationships within component hydroidolinan groups have not been studied within a detailed phylogenetic framework. In an effort to further clarify relationships within Hydroidolina, we greatly augmented the published molecular dataset of hydroidolinan taxa using three molecular markers, the nuclear large (28S) and small (18S) subunit rDNAs and the mitochondrial large subunit rDNA (16S).…”