On the other hand, the radiation of Foraminifera probably occurred at 750– 850 Ma.
Although the first fossil Foraminifera appear only in the Early Cambrian, about 550 Ma
(Culver 1991; McIlroy et al. 2001), there is molecular evidence for a much earlier
radiation of non-fossilized lineages of naked or organic-walled, single-chambered
allogromiid Foraminifera that existed far before their skeletonized remnants were found
and identified in the fossil record (Pawlowski et al. 1999, 2002; unpublished data). Indeed,
the high genetic and morphological diversity of allogromiid Foraminifera suggests that
their diversification probably occurred in the Neoproterozoic.
In order to obtain a more precise estimate for the timing of this radiation, we used a
global phylogeny of Foraminifera based on partial SSU rRNA sequences (data not shown).
We first performed a relative rate test (Robinson-Rechavi and Huchon, 2000) in order to
exclude all sequences evolving significantly slower or faster than the others at a one per
cent level, so that we could approximate a global molecular clock on the dataset. Then we
calibrated the tree using the time of divergence of the first multi-chambered textulariid
Foraminifera, at 350 Ma (Ross and Ross, 1991). We calculated the mean rate of
substitution in the clade of textulariid and rotaliid Foraminifera and applied it to estimate
the time of radiation of all foraminiferan lineages. However, the position of the root in
foraminiferan phylogenies is quite arbitrary, because complete SSU rRNA sequences from
many single-chambered lineages are still missing. Furthermore, because of the lack of
fossil data for the allogromiid Foraminifera, we cannot exclude that the rates of
substitution in these lineages are globally higher than the rates of substitution in the
textulariid+rotaliid clade. So after testing different root positions we retain a proposed
interval of 750–850 Ma for the initial foraminiferan radiation.
Estimation of substitution ratesAccording to our calibration, duration of evolution of the foraminiferan stem-lineage can
be estimated to a maximum of 150–250 million years. Using the topology of Figure 6.1
and divergence times inferred from fossil and molecular data as discussed above, we
calculated that the rate of substitution in the most conserved regions of SSU rRNA genes
averaged at least 1.0 to 1.65 substitutions/1000 sites per 10^6 years during the stem-
lineage evolution of the Foraminifera. This rapid burst of the evolutionary rate was
followed by a return to a ‘normal’ value of about 0.03 substitutions/1000 sites per 10^6
years during the subsequent radiation of the different foraminiferan lineages. This value is
comparable with evolutionary rates calculated in other groups of Eukaryotes (see for
instance Sorhannus 1996).
A substantial slowdown of rates might even be observed in some lineages of
Foraminifera, for example in the clade of textulariids and rotaliids, the two groups where
the slowest rates of substitution were observed (Table 6.1). Conversely, secondary
accelerations occurred in some groups, especially planktonic taxa, as shown by their high
rates of substitution for ribosomal genes (Table 6.1). Most spectacular is the progressive
increase of the rates in the phylogenetic lineage leading to G. truncatulinoides (de Vargas et
al. 2001), as this species is less than six million years old.
114 JAN PAWLOWSKI AND CÉDRIC BERNEY