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

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.

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

“…Furthermore, these primary signals seem to be rapidly evolving, as they derive from different origins such as from gene duplication or allelic variation (Bopp et al, 2014). Among closely related species like Apis and Bombus, gene duplication of fem occurred independently (Koch et al 2014) and likely led to different functions. Therefore, it is reasonable to argue that the evolution of A. florea and A. mellifera/A.…”

“…dorsata seems likely. The frequent and independent duplication of fem in Hymenopteran lineages (Geuverink and Beukeboom, 2014;Koch et al, 2014) (Bee10Genome consortium, Kapheim et al, 2015) seems to be a general phenomenon, which may be of broader relevance to better understand the evolution of sex determination pathways in other insect species.…”

“…Six amino acid residues associated with the fixation of nonsynonymous substitutions in the phylogenetic branch of csd prior to Apis species divergence gave rise to a predicted coiled-coil motif in the csd protein encoding proteinbinding properties (Lupas et al, 1991). In close sister lineages of corbiculate bees (for example, bumble and stingless bees), taking available genomic resources into account, no csd ortholog could be detected, indicating that the gene duplication of honey bee csd and fem occurred after the split of stingless, bumble and honey bees (~80 million years ago), but before honey bee divergence, as an independent event (Koch et al, 2014). Recent phylogenetic analyses of molecular and morphological data place the open-nesting dwarf honey bee, A. florea, as the most basal clade in the phylogeny of the genus Apis (Lo et al, 2010).…”

Evidence for involvement of atransformerparalogue in sex determination of the waspLeptopilina clavipes

“…). This matches a pattern observed in bumblebees and ants (Schmieder et al ., ; Privman et al ., ; Koch et al ., ). The tra homologue in honeybees ( Ap.…”

The transformer genes in the fig wasp Ceratosolen solmsi provide new evidence for duplications independent of complementary sex determination

“…Furthermore, previously reported data suggested that only CSD species have duplicated tra genes (Schmieder et al , ). Besides, studies of tra in the Chalcidoidea and Symphyta are few (Schmieder et al ., ; Privman et al ., ; Koch et al ., ).…”