Abstract
The primary signal of sex determination in the honeybee, the complementary sex determiner (csd) gene, evolved from a gene duplication event from an ancestral copy of the fem gene. Recently, other paralogs of the fem gene have been identified in several ant and bumblebee genomes. This discovery and the close phylogenetic relationship of the paralogous gene sequences led to the hypothesis of a single ancestry of the csd genetic system of complementary sex determination in the Hymenopteran insects, in which the fem and csd gene copies evolved as a unit in concert with the mutual transfers of sequences (concerted evolution). Here, we show that the paralogous gene copies evolved repeatedly through independent gene duplication events in the honeybee, bumblebee, and ant lineage. We detected no sequence tracts that would indicate a DNA transfer between the fem and the fem1/csd genes between different ant and bee species. Instead, we found tracts of duplication events in other genomic locations, suggesting that gene duplication was a frequent event in the evolution of these genes. These and other evidences suggest that the fem1/csd gene originated repeatedly through gene duplications in the bumblebee, honeybee, and ant lineages in the last 100 million years. Signatures of concerted evolution were not detectable, implicating that the gene tree based on neutral synonymous sites represents the phylogenetic relationships and origins of the fem and fem1/csd genes. Our results further imply that the fem1 and csd gene in bumblebees, honeybees, and ants are not orthologs, because they originated independently from the fem gene. Hence, the widely shared and conserved complementary sex determination mechanism in Hymenopteran insects is controlled by different genes and molecular processes. These findings highlight the limits of comparative genomics and emphasize the requirement to study gene functions in different species and major hymenopteran lineages.
Highlights
Complementary sex determination, in which the heterozygous genotype at a certain locus determines femaleness, is widely shared in hymenopteran insects and has a deep ancestry [1,2]
To find further support for either the repeated gene duplication model or the concerted evolution model, we followed the evolutionary trajectory of substitutions that led to amino acid changes in the ancestral sequences of the most recent common ancestor (MRCA) of bees and ants (Fig. 2a)
Our study presents several lines of evidence that support the repeated gene duplication model, but reject the concerted evolution model in which the low divergence of paralogs resulted from homogenization
Summary
Complementary sex determination, in which the heterozygous genotype at a certain locus determines femaleness, is widely shared in hymenopteran insects and has a deep ancestry [1,2]. The underlying gene complementary sex determiner (csd) has been identified in the western honeybee (Apis mellifera) by positional cloning and knockdown studies [3,4]. Csd proteins derived from the heterozygous csd genotype induce the female sex pathway by directing the female splicing of the primary transcripts of the fem gene [4,5]. The resulting female mRNAs subsequently encode the functional Fem proteins. Csd proteins derived from the hemizygous or homozygous genotypes are not required for sex determination. The male splicing of the fem transcripts results by default. More than 14 csd alleles have been identified in local honeybee populations, which show an average of 3% pairwise difference in their entire amino acid encoding sequence [6,7]
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