Complex early genes

Abstract

We use the pattern of intron conservation in 684 groups of orthologs from seven fully sequenced eukaryotic genomes to provide maximum likelihood estimates of the number of introns present in the same orthologs in various eukaryotic ancestors. We find: (i) intron density in the plant-animal ancestor was high, perhaps two-thirds that of humans and three times that of Drosophila; and (ii) intron density in the ancestral bilateran was also high, equaling that of humans and four times that of Drosophila. We further find that modern introns are generally very old, with two-thirds of modern bilateran introns dating to the ancestral bilateran and two-fifths of modern plant, animal, and fungus introns dating to the plant-animal ancestor. Intron losses outnumber gains over a large range of eukaryotic lineages. These results show that early eukaryotic gene structures were very complex, and that simplification, not embellishment, has dominated subsequent evolution.

Fig. 1.

A Dollo parsimony reconstruction of the data, for comparison with our results. D.mel, D. melanogaster; A.gam, A. gambiae; C.ele, C. elegans, H.sap, H. sapiens; S.pom, S. pombe; A.tha, A. thaliana; P.fal, P. falciparum.

Fig. 2.

Estimates of the numbers of introns in 684 genes for various eukaryotic ancestors. Numbers of introns for modern species are known, numbers for ancestors estimated. Large numbers give maximum likelihood estimates, small numbers confidence intervals (2 units of log-likelihood score). Groups 1 and 2 are the two descendant groups for each ancestor. Group 3 is then all species not in groups 1 or 2. o_1–3 columns give the maximum likelihood values. See Fig. 1 legend for abbreviations.

Fig. 3.

Estimates for the numbers of introns present in various eukaryotic ancestors, assuming alternative phylogenies. See Fig. 1 legend for abbreviations.