Evolution of anthozoan polyp retraction mechanisms: convergent functional morphology and evolutionary allometry of the marginal musculature in order Zoanthidea (Cnidaria: Anthozoa: Hexacorallia)

Abstract

BackgroundRetraction is among the most important basic behaviors of anthozoan Cnidaria polyps and is achieved through the coordinated contraction of at least six different muscle groups. Across the Anthozoa, these muscles range from unrecognizable atrophies to massive hypertrophies, producing a wide diversity of retraction abilities and functional morphologies. The marginal musculature is often the single largest component of the retraction mechanism and is composed of a diversity of muscular, attachment, and structural features. Although the arrangements of these features have defined the higher taxonomy of Zoanthidea for more than 100 years, a decade of inferring phylogenies from nucleotide sequences has demonstrated fundamental misconceptions of their evolution.ResultsHere we expand the diversity of known marginal muscle forms from two to at least ten basic states and reconstruct the evolution of its functional morphology across the most comprehensive molecular phylogeny available. We demonstrate that the evolution of these forms follows a series of transitions that are much more complex than previously hypothesized and converge on similar forms multiple times. Evolution of the marginal musculature and its attachment and support structures are partially scaled according to variation in polyp and muscle size, but also vary through evolutionary allometry.ConclusionsAlthough the retraction mechanisms are diverse and their evolutionary histories complex, their morphologies are largely reflective of the evolutionary relationships among Zoanthidea higher taxa and may offer a key feature for integrative systematics. The convergence on similar forms across multiple linages of Zoanthidea mirrors the evolution of the marginal musculature in another anthozoan order (Actiniaria). The marginal musculature varies through evolutionary allometry of functional morphologies in response to requirements for additional force and resistance, and the specific ecological and symbiotic functions of individual taxa.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0406-1) contains supplementary material, which is available to authorized users.

Three new species and the molecular phylogeny of Antipathozoanthus from the Indo-Pacific Ocean (Anthozoa, Hexacorallia, Zoantharia)

“…Macrocinemic zoantharians with cteniform endodermal muscle or endo-meso transitional sphincter muscle (Swain et al 2015). Substrate consists of either antipatharians or coral carbonate (reef).…”

“…Internal morphology : Cteniform endodermal arrangement marginal muscle sensu Swain et al (2015) in longitudinal section (Fig. 4).…”

“…While many taxonomic and molecular studies focusing on the family Parazoanthidae have been conducted using various genetic markers (e.g., Sinniger et al 2005, 2010; Reimer et al 2008; Montenegro et al 2015), little research has been conducted focusing on the phylogenetic relations within different parazoanthid genera, except for studies examining Bergia, Parazoanthus , and Umimayanthus , which are all associated with sponges (Sinniger et al 2005; Montenegro et al 2015, 2016; Carreiro-Silva et al 2017). There is a need for more phylogenetic studies focusing on increasing the numbers of species examined within each of the genera of Parazoanthidae in order to better understand the evolutionary history of substrate specificity and other traits within the family Parazoanthidae (Swain et al 2015, 2016). …”

The order Zoantharia Rafinesque, 1815 (Cnidaria, Anthozoa: Hexacorallia): supraspecific classification and nomenclature

“…This taxon was originally defined as “Zoanthaires à arrangement mésentérique de type brachycnémique et à sphincter endodermique” (Herberts 1972: 137). However, recent work has further divided zoantharian sphincter muscles into ten different basic types; that of Neozoanthidae is discontiguous endodermal (Swain et al 2015). Thus, the above diagnosis has been slightly modified from that of Herberts’ (1972).…”

“…However, recent molecular phylogenetic examination of zoantharians, combined with a reassessment of their taxonomy and diagnostic characters, has led to the group becoming somewhat ordered (Reimer et al 2007a, 2008a, Reimer and Fujii 2010, Sinniger et al 2010a, 2013, Fujii and Reimer 2011, 2013, Swain and Swain 2014; Swain et al 2015), setting an example for the reorganization of other anthozoan groups. This follows in the footsteps of the database Biogeoinformatics of Hexacorallia (Fautin and Buddemeier 2008), which was established as a repository for taxonomic and nomenclatural information on the Hexacorallia (see also Fautin 2016).…”