Phylogenetic Relationships and Evolutionary Patterns of the Order Collodaria (Radiolaria)

Yoshiyuki Ishitani,Colomban De Vargas,Fabrice Not,Kozo Takahashi,Yurika Ujiié,Jonathan H Badger

doi:10.1371/journal.pone.0035775

Abstract

Collodaria are the only group of Radiolaria that has a colonial lifestyle. This group is potentially the most important plankton in the oligotrophic ocean because of its large biomass and the high primary productivity associated with the numerous symbionts inside a cell or colony. The evolution of Collodaria could thus be related to the changes in paleo-productivity that have affected organic carbon fixation in the oligotrophic ocean. However, the fossil record of Collodaria is insufficient to trace their abundance through geological time, because most collodarians do not have silicified shells. Recently, molecular phylogeny based on nuclear small sub-unit ribosomal DNA (SSU rDNA) confirmed Collodaria to be one of five orders of Radiolaria, though the relationship among collodarians is still unresolved because of inadequate taxonomic sampling. Our phylogenetic analysis has revealed four novel collodarian sequences, on the basis of which collodarians can be divided into four clades that correspond to taxonomic grouping at the family level: Thalassicollidae, Collozoidae, Collosphaeridae, and Collophidae. Comparison of the results of our phylogenetic analyses with the morphological characteristics of each collodarian family suggests that the first ancestral collodarians had a solitary lifestyle and left no silica deposits. The timing of events estimated from molecular divergence calculations indicates that naked collodarian lineages first appeared around 45.6 million years (Ma) ago, coincident with the diversification of diatoms in the pelagic oceans. Colonial collodarians appeared after the formation of the present ocean circulation system and the development of oligotrophic conditions in the equatorial Pacific (ca. 33.4 Ma ago). The divergence of colonial collodarians probably caused a shift in the efficiency of primary production during this period.

Highlights

Radiolaria are classified in the Rhizaria super group together with Foraminifera, Endomyxa, and Filosa [1]
In our discussion we have examined the co-evolution of collodarian lineages and the development of the oligotrophic oceans throughout the Cenozoic Era
SSU rDNA phylogeny We confirmed that all 19 collodarian SSU rDNA sequences were associated with the single monophyletic clade of Collodaria in the radiolarian phylogeny (Fig S1)

Summary

Introduction

Radiolaria are classified in the Rhizaria super group together with Foraminifera, Endomyxa, and Filosa [1]. On the basis of a combination of morphological and molecular phylogenetic analyses, the Radiolaria have been assigned to five distinct orders: Spumellaria, Acantharia, Taxopodida, Nassellaria, and Collodaria [3]. Collodaria have unique morphological and ecological features among Radiolaria, because this order includes species with colonial lifestyles and without silicification (i.e., naked). On the basis of these features, Collodaria have been classified into three families: Thalassicollidae, Collosphaeridae, and Collozoidae [2]. Morphological characterization of the siliceous skeletons divides the Collozoidae and Collosphaeridae on the basis of whether the cells possess siliceous spines or an irregular latticed shell, respectively [2]. The other shell-bearing radiolarian orders (Spumellaria, Nassellaria, and Acantharia) are generally classified on the basis of the structure of the inner shell, which is located inside the endoplasm [8]. Some studies have tried to approach collodarian taxonomy on the basis of cell structure characteristics [10,11], these studies have been examined in few taxa and are insufficient to classify all collodarians

Methods

Results

Conclusion