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Duplication and concerted evolution in a master sex determiner under balancing selection.

ABSTRACT: The transformer (tra) gene is a key regulator in the signalling hierarchy controlling all aspects of somatic sexual differentiation in Drosophila and other insects. Here, we show that six of the seven sequenced ants have two copies of tra. Surprisingly, the two paralogues are always more similar within species than among species. Comparative sequence analyses indicate that this pattern is owing to the ongoing concerted evolution after an ancestral duplication rather than independent duplications in each of the six species. In particular, there was strong support for inter-locus recombination between the paralogues of the ant Atta cephalotes. In the five species where the location of paralogues is known, they are adjacent to each other in four cases and separated by only few genes in the fifth case. Because there have been extensive genomic rearrangements in these lineages, this suggests selection acting to conserve their synteny. In three species, we also find a signature of positive selection in one of the paralogues. In three bee species where information is available, the tra gene is also duplicated, the copies are adjacent and in at least one species there was recombination between paralogues. These results suggest that concerted evolution plays an adaptive role in the evolution of this gene family.

SUBMITTER: Privman E

PROVIDER: S-EPMC3619454 | biostudies-literature | 2013 May

REPOSITORIES: biostudies-literature

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Duplication and concerted evolution in a master sex determiner under balancing selection.

Privman Eyal E Wurm Yannick Y Keller Laurent L

Proceedings. Biological sciences 20130306 1758

The transformer (tra) gene is a key regulator in the signalling hierarchy controlling all aspects of somatic sexual differentiation in Drosophila and other insects. Here, we show that six of the seven sequenced ants have two copies of tra. Surprisingly, the two paralogues are always more similar within species than among species. Comparative sequence analyses indicate that this pattern is owing to the ongoing concerted evolution after an ancestral duplication rather than independent duplications ...[more]

PMID: 23466984

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Project description:Recently diverged species typically have incomplete reproductive barriers, allowing introgression of genetic material from one species into the genomic background of the other. The role of natural selection in preventing or promoting introgression remains contentious. Because of genomic co-adaptation, some chromosomal fragments are expected to be selected against in the new background and resist introgression. In contrast, natural selection should favor introgression for alleles at genes evolving under multi-allelic balancing selection, such as the MHC in vertebrates, disease resistance, or self-incompatibility genes in plants. Here, we test the prediction that negative, frequency-dependent selection on alleles at the multi-allelic gene controlling pistil self-incompatibility specificity in two closely related species, Arabidopsis halleri and A. lyrata, caused introgression at this locus at a higher rate than the genomic background. Polymorphism at this gene is largely shared, and we have identified 18 pairs of S-alleles that are only slightly divergent between the two species. For these pairs of S-alleles, divergence at four-fold degenerate sites (K = 0.0193) is about four times lower than the genomic background (K = 0.0743). We demonstrate that this difference cannot be explained by differences in effective population size between the two types of loci. Rather, our data are most consistent with a five-fold increase of introgression rates for S-alleles as compared to the genomic background, making this study the first documented example of adaptive introgression facilitated by balancing selection. We suggest that this process plays an important role in the maintenance of high allelic diversity and divergence at the S-locus in flowering plant families. Because genes under balancing selection are expected to be among the last to stop introgressing, their comparison in closely related species provides a lower-bound estimate of the time since the species stopped forming fertile hybrids, thereby complementing the average portrait of divergence between species provided by genomic data.

Project description:BackgroundMolecular lock-and-key systems are common among reproductive proteins, yet their evolution remains a major puzzle in evolutionary biology. In the Brassicaceae, the genes encoding self-incompatibility have been identified, but technical challenges currently prevent detailed analyses of the molecular interaction between the male and female components. In the present study, we investigate sequence polymorphism in the female specificity determinant SRK of Arabidopsis halleri from throughout Europe. Using a comparative approach based on published SRK sequences in A. lyrata and Brassica, we track the signature of frequency-dependent selection acting on these genes at the codon level. Using simulations, we evaluate power and accuracy of our approach and estimate the proportion of codon sites involved in the molecular interaction.ResultsWe identified several members of the S-gene family, together with 22 putative S-haplotypes. Linkage to the S-locus and the presence of a kinase domain were formally demonstrated for four and six of these haplotypes, respectively, and sequence polymorphism was extremely high. Twenty-five codons showed signs of positive selection in at least one species, and clustered significantly (but not exclusively) within hypervariable regions. We checked that this clustering was not an artifact due to variation in evolution rate at synonymous sites. Simulations revealed that the analysis was highly accurate, thus providing a reliable set of candidates for future functional analyses, but with an overall power not higher than 60 %. Assuming similar power, we infer from our results that about 23% of all codons in the S-domain may actually be involved in recognition. Interestingly, while simulations demonstrated that this comparison remained reliable even at very high levels of divergence, codons identified in Brassica had higher posterior rates of non-synonymous to synonymous substitutions than codons identified in A. halleri or A. lyrata, possibly suggesting more intense selection in Brassica.ConclusionThe signature of balancing selection can be identified reliably at the codon level even in cases of very high sequence divergence, provided that a sufficiently large set of sequences are analyzed. Altogether, our results indicate that a large proportion of codons may be involved in recognition and confirm the particular importance of hypervariable regions. The more intense signature of positive selection detected in Brassica suggests that allelic diversification in this genus was very recent, possibly following a recent demographic bottleneck.

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Duplication and concerted evolution in a master sex determiner under balancing selection.

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Duplication and concerted evolution in a master sex determiner under balancing selection.

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