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. 2013 Mar 6;280(1758):20122968.
doi: 10.1098/rspb.2012.2968. Print 2013 May 7.

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

Affiliations

Affiliation

  • 1 Department of Ecology and Evolution, University of Lausanne, Lausanne 1015, Switzerland.

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

Eyal Privman et al. Proc Biol Sci. .
. 2013 Mar 6;280(1758):20122968.
doi: 10.1098/rspb.2012.2968. Print 2013 May 7.

Affiliation

  • 1 Department of Ecology and Evolution, University of Lausanne, Lausanne 1015, Switzerland.

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.

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Figures

Figure 1.

Figure 1.

Gene tree of tra homologues…

Figure 1.

Gene tree of tra homologues in Hymenoptera. Stars indicate putative independent gene duplication…

Figure 1.
Gene tree of tra homologues in Hymenoptera. Stars indicate putative independent gene duplication events. Phylogeny was reconstructed using BAli-Phy from predicted protein sequences. Posterior probability support is indicated for each branch. Forward green arrows indicate significant acceleration of the evolutionary rate, and plus signs indicate significant evidence for positive diversifying selection. Backward blue arrow indicates significantly reduced rate (detailed results presented in tables 3 and 4). Species name abbreviations: nvit, Nasonia vitripennis; amel, Apis mellifera; acer, Apis cerana; ador, Apis dorsata; hsal, Harpegnathos saltator; lhum, Linepithema humile; cflo, Camponotus floridanus; pbar, Pogonomyrmex barbatus; sinv, Solenopsis invicta; aech, Acromyrmex echinatior; acep, Atta cephalotes. Gene name abbreviations: tra, transformer; fem, feminzer; csd, complementary sex determiner.
Figure 2.

Figure 2.

Evidence for recombination between tra

Figure 2.

Evidence for recombination between tra paralogues in ants from phylogenetic splits networks constructed…

Figure 2.
Evidence for recombination between tra paralogues in ants from phylogenetic splits networks constructed using SplitsTree for coding sequences from (a) the seven ant species and for (b) a narrowed dataset of the attine ants (Ac. echinatior and At. cephalotes) with S. invicta traA as an outgroup. Parallelogram branches represent alternative tree topologies corresponding to putative recombination events. Bootstrap support for two alternative topologies is indicated on the parallelogram. Species name abbreviations as in figure 1.
Figure 3.

Figure 3.

Pairwise identity plots calculated by…

Figure 3.

Pairwise identity plots calculated by RDP for the tra coding sequences from (

Figure 3.
Pairwise identity plots calculated by RDP for the tra coding sequences from (a) the two leaf cutter ant species At. cephalotes and Ac. echinatior and from (b) the two honeybee species Ap. mellifera (csd allele AY352276, fem AAS86667) and Ap. dorsata (csd allele EU100926). Shaded area indicates the putative recombinant region.
Figure 4.

Figure 4.

Recombination test statistics applied to

Figure 4.

Recombination test statistics applied to fem sequences and samples of csd alleles of

Figure 4.
Recombination test statistics applied to fem sequences and samples of csd alleles of Ap. mellifera, dorsata and cerana. (a) The number of samples that received a positive result for each test statistic. (b) The number of instances of inferred recombination events in these samples classified by test and species.

References

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