Evolution and molecular phylogeny of Cibicides and Uvigerina (Rotaliida, Foraminifera)

Abstract

Foraminifers are a group of unicellular organisms present in all the oceans and seas, in fresh water and even in soil. An important number of foraminifers build a shell, often called a 'test' that can be preserved in the fossil record. These tests are extensively used in the field of paleoceanographic proxies, where the test morphology is the basis of foraminifer taxonomy. Formerly mainly familiar to paleontologists, biological research on foraminifers is increasing, partly in response to questions arising in the field of proxy research. It is, for instance, by no means clear how reliable the morphological species concept really is. This study focuses on two taxa widely used in proxy studies: Cibicides and Uvigerina, both classified under Rotaliida. Among the foraminifers bearing a shell, the Rotaliida represent the majority of hyaline calcareous benthic ones. Molecular studies based on the complete SSU rDNA (small subunit ribosomal DNA) show a partition of rotaliids in three main groups. Uvigerina belongs to the first group (also including Bolivina and the Cassidulinidae), whereas Cibicides belongs to the third group (with Bulimina, Stainforthia, Epistominella, Pullenia and Melonis). Phylogenetic analyses based on partial SSU sequences showed the monophyly of Cibicides and confirmed the existence of five morphospecies out of six (C. lobatulus, C. pachyderma, C. refulgens, C. ungerianus, C. wuellerstorfi). On the other hand, the occurrence of cryptic species was shown within two shallow-water species: C. lobatulus and C. refulgens.Of the numerous generic names used for cibicidids, many appear to be synonymous with Cibicides in view of the molecular results (e.g. Cibicidoides, Fontbotia, Heterolepa, Lobatula). Inferring their phylogeny from molecular and fossil data, cibicidids seem to have evolved first on the shelf and subsequently migrated to the deep sea during the Paleogene. In the middle Miocene, this process was apparently repeated, perhaps in response to paleoceanographic changes occurring at that time. Molecular studies of Uvigerina based on partial SSU sequences indicated the inclusion of Rectuvigerina and Trifarina species inside the genus Uvigerina. Moreover, two out of three previously morphologically defined groups: peregrina and semiornata were recognized in molecular phylogenies. Among the generic names used for uvigerinids, many have already been put in synonymy with Uvigerina, Trifarina or Rectuvigerina. It seems likely that Trifarina and Rectuvigerina are also synonyms of Uvigerina. Uvigerinids are preferentially deep sea species, but some are found in neritic environments or at the shelf break. The ornamentation is often used for specific distinction but seems to be strongly influenced by ecological and/or depth factors; Uvigerina peregrina is a good example with a wide morphological variability and a weak genetic diversity. The phylogenetic reconstruction based on molecular and fossil data shows that the studied uvigerinids either appeared during the Oligocene-early Miocene or during the Pliocene-Quaternary. This contrasts with the phylogeny of cibicidids where all studied species originated a long time ago (middle Miocene or Paleogene) and perhaps confirms a difference in the evolutionary rates that was already suspected on basis of the partial SSU phylogenies.