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Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Available online at www.sciencedirect.com Marine Micropaleontology 66 (2008) 233–246 www.elsevier.com/locate/marmicro Molecular phylogeny of Rotaliida (Foraminifera) based on complete small subunit rDNA sequences ⁎ Magali Schweizer a,b, , Jan Pawlowski c, Tanja J. Kouwenhoven a, Jackie Guiard c, Bert van der Zwaan a,d a Department of Earth Sciences, Utrecht University, The Netherlands b Geological Institute, ETH Zurich, Switzerland c Department of Zoology and Animal Biology, University of Geneva, Switzerland d Department of Biogeology, Radboud University Nijmegen, The Netherlands Received 18 May 2007; received in revised form 8 October 2007; accepted 9 October 2007 Abstract The traditional morphology-based classification of Rotaliida was recently challenged by molecular phylogenetic studies based on partial small subunit (SSU) rDNA sequences. These studies revealed some unexpected groupings of rotaliid genera. However, the support for the new clades was rather weak, mainly because of the limited length of the analysed fragment. In order to improve the resolution of the phylogeny of the rotaliids, 26 new complete SSU rDNA sequences have been obtained. Phylogenetic analyses of these data, together with seven sequences obtained previously, confirm with stronger statistical support the presence of three major clades among the Rotaliida. The first clade comprises members of the families Uvigerinidae, Cassidulinidae and Bolivinidae. The second clade includes all analysed Discorbidae, Rosalinidae, Planulinidae, Planorbulinidae, Rotaliidae, Elphidiidae, Nummulitidae and one of the Nonionidae. Finally, the third clade comprises the Cibicididae, Pseudoparreliidae, Oridorsalidae, Stainforthiidae, Buliminidae and part of the Nonionidae. The clades 1 and 3 are strongly supported by analyses of the complete SSU rDNA, while the monophyly of clade 2 is less certain, probably due to the rapid evolutionary rates of some lineages included in this clade. These results clearly contradict the classical separation of rotaliid foraminifera into two orders: Rotaliida and Buliminida. Relatively good agreement has been found between molecular data and the morphological definition of the families for which more than one genus was sequenced. However, larger taxon sampling will be necessary for a better definition of the three major clades. © 2007 Elsevier B.V. All rights reserved. Keywords: Benthic foraminifera; Rotaliida; Molecular phylogeny; Classification; SSU rDNA 1. Introduction the chemical composition of their fossil tests are exten- sively used as proxies for environmental changes in the Benthic foraminifera are important elements of the geological past (Van der Zwaan et al., 1999). Together meiofaunal community; their abundance data as well as with their potential use for monitoring recent environ- ments, this has led to an increasing interest in their ⁎ Corresponding author. Geological Institute, ETH Zurich, biological functioning. Since the second half of the last Switzerland. century research has focused on the use of foraminifera E-mail address: [email protected] (M. Schweizer). for environmental and pollution issues (e.g. Bandy et al., 0377-8398/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.marmicro.2007.10.003 Author's personal copy 234 M. Schweizer et al. / Marine Micropaleontology 66 (2008) 233–246 1964; Vénec-Peyré, 1981; Van der Zwaan and Jorissen, perforate foraminifera in the suborder Rotaliina which 1991; Alve, 1995; Mojtahid et al., 2006). Proxy re- included ten superfamilies (i.e. Nodosariacea, Bulimi- search, relevant to applications in the fossil record nacea, Discorbacea, Spirillinacea, Rotaliacea, Globiger- addresses, for instance, the response to environmental inacea, Orbitoidacea, Cassidulinacea, Carterinacea and factors such as organic carbon flux (e.g. Smart et al., Robertinacea) distinguished on the basis of the wall 1994; Murray, 2001; Ernst et al., 2005). The preserva- microstructure as well as coiling and aperture character- tion of foraminiferal tests is important in this type of istics. In 1981, Haynes retained the wall structure as the research (e.g. Berger, 1979; Mackensen and Douglas, primary basis of subdivision; however, more emphasis 1989; Murray, 1989), and so are the vital effects as- was given to the shape of the aperture. In his clas- sociated with incorporation into calcareous tests of sification, the superfamilies were raised to orders, and elements (e.g. Bentov and Erez, 2006) and stable iso- the Nodosariida, Robertinida, Buliminida and Globiger- topes (e.g. Schmiedl et al., 2004). In addition, research inida were separated from the Rotaliida. The Buliminida into the role of benthic foraminifera in biogeochemical comprised the hyaline perforate foraminifers with a cycling has recently resulted in the discovery that some toothplate and included the following superfamilies: species of foraminifera are able to perform complete Buliminacea, Bolivinitacea and Cassidulinacea, where- denitrification (Risgaard-Petersen et al., 2006)andin as the Rotaliida contained the Spirillinacea, Discorba- doing so could play an important, though as yet not cea, Asterigerinacea and Orbitoidacea (Haynes, 1981). quantified, role in the marine nitrogen cycle. In view of In their monumental work, Loeblich and Tappan foraminiferal evolution this raises the question whether (1988) defined supplementary suborders for the hyaline traits like nitrate reduction developed separately in perforate calcareous foraminifers in addition to their different clades, and when. Finally, cryptic speciation former classification (1964): Involutinina, Spirillinina, occurs in planktic (e.g., Darling et al., 2006) as well as in Carterinina, Silicoloculinina, Lagenina, Robertinina and benthic foraminifera (e.g. Hayward et al., 2002); Globigerinina. The suborder Rotaliina was divided into although in Uvigerina the opposite has been described 24 superfamilies; the criteria used were the number of recently (Schweizer et al., 2005). Either way, the use of chambers, the presence or absence of perforations, canals foraminifera as (paleo-) environmental proxies needs to and cavities in the test, and the aperture. In 1992, to solve be reconsidered. In view of these developments, phylo- some of the inconsistencies reported by Haynes (1981, genetic relationships between foraminifera, which were 1990), Loeblich and Tappan raised the foraminifera from previously predominantly based on morphology, need a an order to a class (the foraminiferal suborders were thus re-evaluation. given order status) and recognized the order Buliminida The order Rotaliida comprises calcareous hyaline Fursenko, 1958. In the most recent classification, Sen perforate species and represents one third of the extant, Gupta (2002) followed the classification of Loeblich and described genera of foraminifers (based on data from Tappan (1992) with slight modifications (Fig. 1). Decrouez, 1989). The taxon was introduced by Delage According to this view, Buliminida are distinguished and Hérouard in 1896 as the suborder Rotalidae from Rotaliida by the presence of a toothplate, a loop- (reference in Loeblich and Tappan, 1964). The hyaline shaped aperture and a high trochospiral coil. foraminifers were recognized earlier as a group by Since the mid-90s, the molecular approach has shed Williamson (1858), who was the first author to use the new light on foraminiferal phylogeny. The first molecular wall composition in foraminiferal classification (Cifelli results showed a clade combining the Textulariida and the and Richardson, 1990). However, this distinction was Rotaliida (Pawlowski et al., 1997; Pawlowski, 2000). not always adhered to in early classifications. For This mixed clade was explained either by a radiation example, Reuss (1861), Carpenter et al. (1862), Brady occurring in a relatively short time, or by slow rates of (1884), Rhumbler (1895) and Cushman (1922) placed evolution of both groups (Pawlowski et al., 1997, 2003). arenaceous textulariids and hyaline bolivinids (some- More recent analyses were able to separate the rotaliids times with buliminids and cassidulinids) within the and textulariids, albeit without strong statistical support same group; this was also the case in some more recent (Holzmann et al., 2003; Ertan et al., 2004; Bowser et al., publications (Hofker, 1951, 1956; Mikhalevich and 2006). Within the rotaliids, Holzmann et al. (2003) Debenay, 2001). examined the links between the Nummulitidae and seven The classifications of Cushman (1928) and Galloway other rotaliid families, Ertan et al. (2004) explored the (1933) separated the hyaline genera from other relationships of eleven genera of Rotallida, whereas foraminifera and placed them in several families. Schweizer et al. (2005)