The evolution of early Foraminifera

Abstract

Fossil Foraminifera appear in the Early Cambrian, at about the same time as the first skeletonized metazoans. However, due to the inadequate preservation of early unilocular (single-chambered) foraminiferal tests and difficulties in their identification, the evolution of early foraminifers is poorly understood. By using molecular data from a wide range of extant naked and testate unilocular species, we demonstrate that a large radiation of nonfossilized unilocular Foraminifera preceded the diversification of multilocular lineages during the Carboniferous. Within this radiation, similar test morphologies and wall types developed several times independently. Our findings indicate that the early Foraminifera were an important component of Neoproterozoic protistan community, whose ecological complexity was probably much higher than has been generally accepted.

Fig. 1.

Phylogenetic relationships among early Foraminifera inferred from partial small subunit rRNA gene sequences. The various types of test are highlighted with different colors. Among multilocular foraminiferans, the Rotaliida are marked in green, whereas the Textulariida are marked in dark green. The tree was calibrated according to the fossil radiation of multilocular Foraminifera (350 Ma). The time ranges for the initial radiation of unilocular species, as well as the radiation leading to the divergence of multilocular species, are indicated. The topology shown was obtained with the ML method, by using the F84 substitution model. Because the exact position of the root remains unresolved, the tree is drawn with a basal trichotomy. However, the placement of the root does not influence the general topology of the tree and has little influence on the tree calibration. The bootstrap support values for the main lineages in ML and NJ analyses are indicated at internal nodes. The presented tree does not differ markedly from that obtained with ML analysis performed by using the GTR substitution model, taking into account a proportion of invariant sites and a gamma-shaped distribution of rates of substitution among sites, with eight rate categories. The only differences relate to the relative branching order of the unilocular lineages and, most particularly, to the position of the monogeneric groups (Nemogullmia, Reticulomyxa, Tinogullmia, and Vanhoeffenella).

Fig. 2.

Phylogenetic relationships among 55 Foraminifera inferred from partial small subunit rDNA sequences, including representatives of all groups shown in Fig. 1, as well as 3 members of the genus Ammodiscus, 7 members of the order Miliolida, and 2 members of the order Spirillinida. Because of the high divergence of the SSU rDNA sequences in the three latter groups, 500 unambiguously aligned positions were kept in phylogenetic analyses for this dataset. The topology shown was obtained with the ML method by using the F84 substitution model. Because the exact position of the root is yet unclear, the tree is drawn with a basal trichotomy. Representatives of the genus Ammodiscus and the orders Miliolida and Spirillinida form a clearly monophyletic group, but their placement as a sister group to Psammosphaera sp. is not supported. Due to the reduced number of analyzed positions, the resolution among the other groups of Foraminifera is weaker than in Fig. 1. The bootstrap support values >80% for NJ and ML analyses are indicated at internal nodes.

Fig. 3.

Time scale of early foraminiferal evolution based on combined molecular and fossil data, highlighting the development of reticulopodia at the origin of the group, and the independent development of a multilocular test in the lineages leading to Textulariida + Rotaliida and Spirillinida + Miliolida. Only the taxonomic groups for which molecular data exist are illustrated. The height of each rectangle is proportional to the number of recognized families in the clade, or to the number of different genetic lineages in the case of Monothalamida. Stars indicate the fossil appearance of some unilocular lineages.