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.

Independent Evolutionary Origin of fem Paralogous Genes and Complementary Sex Determination in Hymenopteran Insects

“…We included the same coding nucleotide sequences as in a previous study [13], comprised of 36 csd and 1 fem A. mellifera , 16 csd and 1 fem Apis cerana csd , 19 csd and 1 fem Apis dorsata sequence and a fem B. terrestris sequence as an outgroup reference.…”

“…The authors suggested that (i) alternative tree topologies of the nucleotide sequences [13] and (ii) putative gene conversion tracts [11], [13] are evidence for concerted evolution. Schmieder et al identified gene conversion tracts in the genomic sequences of the paralogs.…”

Phylogenetic Distribution and Evolutionary Dynamics of the Sex Determination Genes doublesex and transformer in Insects

“…The Apis genus belongs to the Aculeata, consisting of bees, vespoid wasps and ants, which is considered a derived lineage within the Hymenoptera. Two recent reports [Schmieder et al, 2012;Privman et al, 2013] found a similar duplication of transformer in 2 bumblebees and 6 out of 7 sequenced ant species (listed in table 1 ), all belonging to the Aculeata. The presence of transformer paralogs in these aculeate species is explained by a single duplication event after which the genes evolved through concerted evolution [Schmieder et al, 2012;Privman et al, 2013].…”

“…Two recent reports [Schmieder et al, 2012;Privman et al, 2013] found a similar duplication of transformer in 2 bumblebees and 6 out of 7 sequenced ant species (listed in table 1 ), all belonging to the Aculeata. The presence of transformer paralogs in these aculeate species is explained by a single duplication event after which the genes evolved through concerted evolution [Schmieder et al, 2012;Privman et al, 2013]. This places the duplication of transformer/feminizer leading to the csd gene before the appearance of the Aculeata lineages, around 120 million years ago [Schmieder et al, 2012].…”

“…The paralog would then need to contain a hypervariable region as in the A. mellifera csd gene, or at least a high variety of alleles. However, within the Aculeata, 2 of the thus far examined species appear to lack a duplication of transformer : the leaf-cutting ant Acromyrmex echinatior [Nygaard et al, 2011;Schmieder et al, 2012;Privman et al, 2013], which is known to produce high levels of diploid males, and the solitary bee Megachile rotundata ( table 1 ). No duplications have yet been found outside the Aculeata, but the availability of databases in Hymenoptera is strongly skewed towards eusocial derived species.…”