Tracing back the nascence of a new sex-determination pathway to the ancestor of bees and ants

Schmieder, Sandra; Colinet, Dominique; Poirié, Marylène

doi:10.1038/ncomms1898

Cited by 60 publications

(77 citation statements)

References 33 publications

(46 reference statements)

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“…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].…”

Section: Duplications Of Transformermentioning

confidence: 99%

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

Geuverink

Beukeboom²

2013

Sex Dev

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Sex determination in insects is characterized by a gene cascade that is conserved at the bottom but contains diverse primary signals at the top. The bottom master switch gene doublesex is found in all insects. Its upstream regulator transformer is present in the orders Hymenoptera, Coleoptera and Diptera, but has thus far not been found in Lepidoptera and in the basal lineages of Diptera. transformer is presumed to be ancestral to the holometabolous insects based on its shared domains and conserved features of autoregulation and sex-specific splicing. We interpret that its absence in basal lineages of Diptera and its order-specific conserved domains indicate multiple independent losses or recruitments into the sex determination cascade. Duplications of transformer are found in derived families within the Hymenoptera, characterized by their complementary sex determination mechanism. As duplications are not found in any other insect order, they appear linked to the haplodiploid reproduction of the Hymenoptera. Further phylogenetic analyses combined with functional studies are needed to understand the evolutionary history of the transformer gene among insects.

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Section: Duplications Of Transformermentioning

confidence: 99%

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

Geuverink

Beukeboom²

2013

Sex Dev

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“…In all three Apis species, support is given for a common target of balancing selection in csd, the potential specifying domain (PSD) located in exons 6 and 7, based on high average diversity at synonymous (π S ) and nonsynonymous (π N ) sites (Hasselmann et al, 2008b). For A. florea and other Hymenoptera (for example, bumble bees), genome predictions have been used to describe fem and its orthologs (Schmieder et al, 2012). A putative csd ortholog has been reported in A. florea, showing exceptionally high-nucleotide diversity exceeding those described for any other Apis (Liu et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Similar but not the same: insights into the evolutionary history of paralogous sex-determining genes of the dwarf honey bee Apis florea

2015

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Studying the fate of duplicated genes provides informative insight into the evolutionary plasticity of biological pathways to which they belong. In the paralogous sex-determining genes complementary sex determiner (csd) and feminizer (fem) of honey bee species (genus Apis), only heterozygous csd initiates female development. Here, the full-length coding sequences of the genes csd and fem of the phylogenetically basal dwarf honey bee Apis florea are characterized. Compared with other Apis species, remarkable evolutionary changes in the formation and localization of a protein-interacting (coiled-coil) motif and in the amino acids coding for the csd characteristic hypervariable region (HVR) are observed. Furthermore, functionally different csd alleles were isolated as genomic fragments from a random population sample. In the predicted potential specifying domain (PSD), a high ratio of π N /π S = 1.6 indicated positive selection, whereas signs of balancing selection, commonly found in other Apis species, are missing. Low nucleotide diversity on synonymous and genome-wide, non-coding sites as well as site frequency analyses indicated a strong impact of genetic drift in A. florea, likely linked to its biology. Along the evolutionary trajectory of 30 million years of csd evolution, episodic diversifying selection seems to have acted differently among distinct Apis branches. Consistently low amino-acid differences within the PSD among pairs of functional heterozygous csd alleles indicate that the HVR is the most important region for determining allele specificity. We propose that in the early history of the lineage-specific fem duplication giving rise to csd in Apis, A. florea csd stands as a remarkable example for the plasticity of initial sex-determining signals.

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“…There were three important differences between our analyses and those done by Schmieder et al [59]. First, we used a superior Bayesian method for joint alignment and phylogeny reconstruction (BALI-PHY) to minimize artefacts owing to alignment errors.…”

Section: Discussionmentioning

confidence: 99%

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

2013

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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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Tracing back the nascence of a new sex-determination pathway to the ancestor of bees and ants

Cited by 60 publications

References 33 publications

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

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

Similar but not the same: insights into the evolutionary history of paralogous sex-determining genes of the dwarf honey bee Apis florea

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

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