The phylogeny of closely related species as revealed by the genealogy of a speciation gene, Odysseus

Abstract

Molecular differentiation between races or closely related species is often incongruent with the reproductive divergence of the taxa of interest. Shared ancient polymorphism and/or introgression during secondary contact may be responsible for the incongruence. At loci contributing to speciation, these two complications should be minimized (1, 2); hence, their variation may more faithfully reflect the history of the species' reproductive differentiation. In this study, we analyzed DNA polymorphism at the Odysseus (OdsH) locus of hybrid sterility between Drosophila mauritiana and Drosophila simulans and were able to verify such a prediction. Interestingly, DNA variation only a short distance away (1.8 kb) appears not to be influenced by the forces that shape the recent evolution of the OdsH coding region. This locus thus may represent a test case of inferring phylogeny of very closely related species.

Figure 1

Contrasting gene genealogies at two types of loci. Speciation occurred first between species 3 and the ancestor of species 1 and 2, and then between the latter species. Gene flow across species boundaries diminished with time. (a) “Speciation loci.” Each favorable mutation (marked with an *) drives the spread of a single lineage, excluding other lineages (ending with a tick). This would result in the purge of shared ancient polymorphisms. In addition, any lineage introgressed from the other species (arrow) is quickly eliminated because of the incompatibility with the new genetic background. Monophyly by species and a clear species phylogeny are observed. (b) “Other loci.” Ancient polymorphism and introgression during secondary contact (arrow) lead to mixed genealogies between species. Dashed branches denote lineages lost because of genetic drift. Note that species 2 and 3 appear most closely related.

Figure 2

Schematic drawing of the genomic region of OdsH. Exons are shown as solid boxes. Line segments A and B denote the regions sequenced in this study.

Figure 3

Genealogies of region A or B (as shown in Fig. 2) among the four sibling species of Drosophila, as inferred by the maximum parsimony method (paup, version 3.1.1). Variation at other loci published so far exhibits genealogies similar to that of B (see text). Branch length is proportional to the inferred number of changes, which are given along the major branches. The short terminal branches often represent 0 changes. Adjacent nodes whose bootstrapping value is lower than 50% are compressed into a single node. The bootstrapping values of the four interspecific nodes are of special interest. In A, they are all 100%, as shown, but in B, two are less than 50% and are compressed into a star phylogeny. Arrow indicates the root. L, Number of nucleotides analyzed.