Phylogenetic analysis of phenotypic characters of Tunicata supports basal Appendicularia and monophyletic Ascidiacea.

Katrin Braun,Thomas Stach,Fanny Leubner

doi:10.1111/cla.12405

Abstract

With approximately 3000 marine species, Tunicata represents the most disparate subtaxon of Chordata. Molecular phylogenetic studies support Tunicata as sister taxon to Craniota, rendering it pivotal to understanding craniate evolution. Although successively more molecular data have become available to resolve internal tunicate phylogenetic relationships, phenotypic data have not been utilized consistently. Herein these shortcomings are addressed by cladistically analyzing 117 phenotypic characters for 49 tunicate species comprising all higher tunicate taxa, and five craniate and cephalochordate outgroup species. In addition, a combined analysis of the phenotypic characters with 18S rDNA-sequence data is performed in 32 OTUs. The analysis of the combined data is congruent with published molecular analyses. Successively up-weighting phenotypic characters indicates that phenotypic data contribute disproportionally more to the resulting phylogenetic hypothesis. The strict consensus tree from the analysis of the phenotypic characters as well as the single most parsimonious tree found in the analysis of the combined dataset recover monophyletic Appendicularia as sister taxon to the remaining tunicate taxa. Thus, both datasets support the hypothesis that the last common ancestor of Tunicata was free-living and that ascidian sessility is a derived trait within Tunicata. "Thaliacea" is found to be paraphyletic with Pyrosomatida as sister taxon to monophyletic Ascidiacea and the relationship between Doliolida and Salpida is unresolved in the analysis of morphological characters; however, the analysis of the combined data reconstructs Thaliacea as monophyletic nested within paraphyletic "Ascidiacea". Therefore, both datasets differ in the interpretation of the evolution of the complex holoplanktonic life history of thaliacean taxa. According to the phenotypic data, this evolution occurred in the plankton, whereas from the combined dataset a secondary transition into the plankton from a sessile ascidian is inferred. Besides these major differences, both analyses are in accord on many phylogenetic groupings, although both phylogenetic reconstructions invoke a high degree of homoplasy. In conclusion, this study represents the first serious attempt to utilize the potential phylogenetic information present in phenotypic characters to elucidate the inter-relationships of this diverse marine taxon in a consistent cladistic framework.

Highlights

Tunicata is a taxon that comprises approximately 3000 marine invertebrate species, including the brightly bioluminescent Pyrosomatida, the translucent Salpida with their heterogenic life cycle or the Appendicularia (= Larvacea) that are capable of producing a most delicate, yet at the same time complex, extracorporal structure often called a “house” (Shenkar and Swalla, 2011; Lemaire and Piette, 2015)
Statistical measures of nodal support are reported as Bremer support indices, jackknife values based on 100 replicates with 50% character deletion, and bootstrap percentages based on 100 replicates using the same search strategy as for the main analysis but with 200 replicates within each bootstrap replicate
These studies seemingly approach a more stable framework regarding some contentious points of tunicate phylogeny, it has been pointed out that phylogenetic analysis of tunicate DNA sequences is difficult due to generally increased mutation rates (Tsagkogeorga et al, 2010) and that phylogenetic information might not be as solid as suggested by statistical support values in published phylogenies (Stach, 2014)

Summary

Introduction

Tunicata is a taxon that comprises approximately 3000 marine invertebrate species, including the brightly bioluminescent Pyrosomatida, the translucent Salpida with their heterogenic life cycle or the Appendicularia (= Larvacea) that are capable of producing a most delicate, yet at the same time complex, extracorporal structure often called a “house” (Shenkar and Swalla, 2011; Lemaire and Piette, 2015). Wada, 1998; Swalla et al, 2000; Stach and Turbeville, 2002; Tsagkogeorga et al, 2009; see review in Giribet, 2018) Despite their limitations, these studies eventually converged on certain points: the planktonic Appendicularia is placed as sister taxon to the remaining Tunicata; the sessile seasquirts “Pyuridae”, traditionally considered to be a “family” within Stolidobranchiata, was recovered to be paraphyletic with Styelidae nested within “Pyuridae.” the number of molecular markers has increased considerably with two recently published studies that in parallel supported the phylogenies just outlined (Delsuc et al, 2018; Kocot et al, 2018), the number of species studied remains low considering the diversity found within Tunicata

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