Heterogeneity of the substitution rates in foraminiferan
rRNA genesAnalyses of partial SSU rDNA sequences show important differences in the evolutionary
rates between major taxonomic groups of Foraminifera (Pawlowski et al. 1997). Results of
a re-analysis of previously published data (Pawlowski et al. 1997; de Vargas and Pawlowski
1998), with additional pairs of benthic and planktonic foraminiferan genera and species,
and using an enhanced alignment comprising 620 unambiguously aligned positions, are
summarized in Table 6.1.
Pairwise-distance rates were calculated using distances corrected according to
Kimura’s two-parameter model of substitutions; however, as all pairs of species are
closely related, very similar results were obtained using the more complex GTR model of
substitutions, taking into account a proportion of invariant sites and a gamma distribution
of the rates of substitution across sites, with an alpha distribution shape parameter
calculated from the dataset (data not shown). The values obtained are slightly different
from those previously published. Observed discrepancies may be explained by the fact
that calculation of rates of substitution depends directly on the choice of sites used in the
analyses. In this study, we used a slightly larger number of sites in order to avoid very small
numbers of differences between the slowest evolving lineages. However, the differences
between the values presented here (Table 6.1) and previously published data are smaller
than 50 per cent and the ratios between substitution rates of different lineages remain
similar.
In the Foraminifera, the slowest rates of substitution (0.02–0.1 substitutions/1000
sites per 10^6 years) are observed in the clade of textulariids and rotaliids, two groups that
are characterized by multi-chambered tests, having agglutinated (Textulariida) or
calcareous, perforate (Rotaliida) walls. Miliolids, a group of multi-chambered
Foraminifera with calcareous, porcellaneous tests, exhibit rates that are five to 10 times
higher than in the textulariids and rotaliids. But the most rapid substitution rates are
observed in planktonic species; these rates are more than 100 times faster than in the most
slowly evolving benthic lineages (Table 6.1).
Such variations contrast sharply with values calculated in other eukaryotes. Friedrich
and Tautz (1997) showed the fast-evolving Diptera to have only two- to four-fold higher
rates of substitution than other holometabolous insects for LSU and SSU rRNA genes.
Similarly, Smith et al. (1992) reported statistically significant differences in evolutionary
rates between different lineages of echinoids, based on LSU rRNA data. But again, the
rate difference between lineages did not exceed a three-fold magnitude. More important
differences can be observed in protein-coding genes. Li et al. (1987) estimated
substitution rates in rodents to be four to 10 times higher than those in higher primates,
and two to four times higher than those in artiodactyls. Exceptionally high variations (up
to 138 per cent for non-synonymous substitutions) were observed by Bousquet et al.
(1992) in rbcL sequences of seed plants, which nevertheless remain small compared with
those in the Foraminifera.
The rates seem to be much more uniform within some foraminiferan lineages,
suggesting the existence of local molecular clocks. In the large porcellaneous Foraminifera
of the superfamily Soritacea (Miliolida), the rates of SSU rRNA evolution vary from 0.25–
0.5 substitutions/1000 sites per 10^6 years, with a mean value of 0.34 substitutions/1000
EVOLUTION IN THE STEM-LINEAGE OF FORAMINIFERA 111