Phylogeny of Comatulidae (Echinodermata: Crinoidea: Comatulida): A new classification and an assessment of morphological characters for crinoid taxonomy

Highlights

• A molecular phylogeny for Comatulidae was inferred for 43 nominal species.

• Two of the subfamilies and two genera were paraphyletic and the taxonomy revised.

• Traditional taxonomic features were mainly convergent.

• Morphology of Comatulidae is in need of re-assessment.

Abstract

Comatulidae Fleming, 1828 (previously, and incorrectly, Comasteridae A.H. Clark, 1908a), is a group of feather star crinoids currently divided into four accepted subfamilies, 21 genera and approximately 95 nominal species. Comatulidae is the most commonly-encountered and species-rich crinoid group on shallow tropical coral reefs, particularly in the Indo-western Pacific region (IWP). We conducted a molecular phylogenetic analysis of the group with concatenated data from up to seven genes for 43 nominal species spanning 17 genera and all subfamilies. Basal nodes returned low support, but maximum likelihood, maximum parsimony, and Bayesian analyses were largely congruent, permitting an evaluation of current taxonomy and analysis of morphological character transformations. Two of the four current subfamilies were paraphyletic, whereas 15 of the 17 included genera returned as monophyletic. We provide a new classification with two subfamilies, Comatulinae and Comatellinae n. subfamily Summers, Messing, & Rouse, the former containing five tribes. We revised membership of analyzed genera to make them all clades and erected Anneissia n. gen. Summers, Messing, & Rouse. Transformation analyses for morphological features generally used in feather star classification (e.g., ray branching patterns, articulations) and those specifically for Comatulidae (e.g., comb pinnule form, mouth placement) were labile with considerable homoplasy. These traditional characters, in combination, allow for generic diagnoses, but in most cases we did not recover apomorphies for subfamilies, tribes, and genera. New morphological characters that will be informative for crinoid taxonomy and identification are still needed. DNA sequence data currently provides the most reliable method of identification to the species-level for many taxa of Comatulidae.

Introduction

Extant crinoids belong to Articulata, the only crinoid lineage of the four currently recognized to survive the end-Paleozoic extinction (Hess and Messing, 2011). Among extant articulates, over 80% of the ∼650 accepted species belong to order Comatulida (Rouse et al., 2013, Hemery et al., 2013), most members of which shed the postlarval stalk and take up a non-sessile existence as feather stars (Holland, 1991, Haig and Rouse, 2008). Contemporary taxonomy of extant crinoids dates chiefly from 1907 to 1909, when Clark, 1907a, Clark, 1908a, Clark, 1908b, Clark, 1909a, Clark, 1909b, Clark, 1909c described 75 genera and 17 family-level taxa, chiefly feather stars. Although a few families and genera have since been revised (e.g., Hoggett and Rowe, 1986, Rowe et al., 1986, White et al., 2001, Messing, 2001, Messing and White, 2001, Hess and Messing, 2011), Clark’s more than 100 publications, including a five-volume monograph (totaling more than 4100 pages) (Clark, 1915a, Clark, 1921a, Clark, 1931, Clark, 1941, Clark, 1947, Clark, 1950, Clark and Clark, 1967), remain the foundation for current morphologically-based classification of the group. However, recent molecular analyses spanning Articulata (Hemery et al., 2013, Rouse et al., 2013) have revealed serious taxonomic inadequacies and indicate that extensive revision is required.

Among feather stars, Comatulidae Fleming, 1828 (Fig. 1), includes approximately 95 accepted nominal species and dominates tropical reef crinoid faunas worldwide in terms of both species-richness and abundance (Messing, 2001). Although the name Comasteridae A.H. Clark (1908a), has been uniformly applied to this family for just over a century, we use here the family name Comatulidae Fleming (1828) and ‘comatulid’ with reference to Comatulidae, because the former is clearly a junior synonym and should not be used (see Appendix A). Comatulidae are distinguished from other feather stars by two easily recognized and arguably apomorphic features. (1) Several to many distal segments of at least a few proximal pinnules bear one or two blade- or knob-like projections that together form a comb-like structure. (2) In most genera and species, the mouth lies off-center or near the margin on the oral surface, or tegmen (Fig. 2). Previous molecular studies (Hemery et al., 2013, Rouse et al., 2013) recovered Comatulidae as monophyletic with strong support, but White et al. (2001) and Rouse et al. (2013) suggested paraphyly for subfamilies and some genera. Fossils attributed to this family date to the early Miocene (Simms et al., 1993). Rouse et al. (2013) suggested that it is likely a much older clade, or that it has a faster rate of molecular evolution than most other extant crinoid clades.

The most recent morphological classification places the species in 21 genera and four subfamilies (Hess and Messing, 2011, Messing, 2001): Comatulinae; Capillasterinae; Comasterinae; and Phanogeniinae. (Table 1 lists authorship for all taxa.) These subfamilies are distinguished chiefly by differences among patterns of articulation between proximal brachials (Fig. 3), whereas ray branching patterns, cirrus ornamentation, ossicle proportions, and, more recently, pinnule comb structure diagnose genera (Fig. 4). However, the current morphology-based classification suffers from a lack of consensus about character homologies (e.g., structure, derivation and placement of ligamentary articulations) (A.H. Clark, 1931, Hoggett and Rowe, 1986, Messing, 2001, Rowe et al., 1986). Identification is further confounded by substantial ontogenetic changes and morphological variation based on environmental conditions (e.g., mouth position, number of arms and cirri, and color variations (see Messing, 1998, Messing, 2001, Owen et al., 2009)).

In this paper, we re-assess the phylogeny, evaluate morphological characters, and revise the classification of Comatulidae accordingly. To this end, we sequenced DNA for part or all of seven genes (nuclear and mitochondrial) from 56 terminals (plus four outgroup species) representing 17 of the 21 accepted genera. These genes were concatenated and analyzed using maximum parsimony, maximum likelihood, and Bayesian methods. To assess morphological transformation, we mapped traits on the molecular phylogenetic results. We provide a revised classification of the subfamilies and three genera.