Large-scale intron conservation and order-of-magnitude variation in intron loss/gain rates in apicomplexan evolution

Abstract

The age of modern introns and the evolutionary forces controlling intron loss and gain remain matters of much debate. In the case of the apicomplexan malaria parasite Plasmodium falciparum, previous studies have shown that while the positions of two thirds of P. falciparum introns are not shared with surveyed non-apicomplexans (leaving open the possibility that they were relatively recently gained), 99.1% are shared with Plasmodium yoelii, which diverged from P. falciparum at least 100 Mya. We show here that 60.6% of P. falciparum intron positions in conserved regions are shared with the distantly related apicomplexan Theileria parva, whereas only 18.2% of introns in the more intron-rich T. parva are shared with P. falciparum. Comparison of 3305 pairs of orthologous genes between T. parva and Theileria annulata showed that 7089/7111 (99.7%) introns in conserved regions are shared between species. These levels of conservation imply significant differences in rates of intron loss and gain through apicomplexan history. Because transposable elements (TEs) and/or (often TE-encoded) reverse transcriptase are implicated in models of intron loss and gain, the observed low rates of intron loss and gain in recent Plasmodium and Theileria evolution are consistent with the lack of known TE in those groups. We suggest that intron loss/gain in some eukaryotic lineages may be concentrated in relatively short episodes coincident with occasional TE invasions.

Figure 1.

Intron divergences between and within Theileria and Plasmodium species. Percentages of total intron positions in conserved regions that are species specific are given for the three apicomplexan comparisons. Times of divergence are from Escalante and Ayala (1995) (Theileria- Plasmodium divergence), from an assumption of P. yoelii–P. falciparum speciation at least as deep as host divergence, and based on an estimated d _S = 0.82 divergence between Theileria species, assuming a nucleotide substitution rate of 5 × 10^-9 (T. annulata–T. parva divergence).

Figure 2.

Estimated rates of intron loss and gain in three comparisons. The Plasmodium and Theileria traces give possible estimates of intron loss and gain for the P. falciparum–P. yoelii and T. parva–T. annulata comparisons, respectively, given the number of observed species-specific intron positions. The black traces give possible estimates derived from the T. parva–P. falciparum comparison, assuming either a divergence time of 350 Mya or 824 Mya. Estimates are derived as described in the text.