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The high rate of sequence divergence in nuclear ribosomal RNA (rRNA) expansion segments offers a unique opportunity to study the importance of natural selection in their evolution. To this end, we polymerase chain reaction amplified and cloned a 589-nt fragment of the 18S rRNA gene containing expansion segments 43/e1 and 43/e4 from six individual Daphnia obtusa from four populations. We screened 2,588 clones using single-stranded conformation polymorphism analysis and identified 103 unique haplotype sequences. We detected two pairs of indel sites in segment 43/e4 that complement each other when the secondary structure of the linear sequence is formed. Seven of the 12 observed combinations of length variants at these four sites (haplotypes) are shared between individuals from different populations, which may suggest that some of the length variation was present in their common ancestor. Haplotypes with uncompensated indels were only observed at low frequencies, while compensated indel haplotypes were found at a wide range of frequencies, supporting the hypothesis that the energetic stability of expansion segments is a trait under natural selection. In addition, there was strong linkage disequilibrium between the four complementary indel sites, particularly those that pair with one another in the secondary structure. Despite selection against unpaired bulges at these four indel sites, some nucleotides that form unpaired bulges are highly conserved in segment 43/e4, indicating that they are under a different selective constraint, possibly due to their role in higher level structural interactions.

Selection on the Structural Stability of a Ribosomal RNA Expansion Segment in Daphnia obtusa