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Evolution of the complementary sex-determination gene of honey bees: balancing selection and trans-species polymorphisms.

ABSTRACT: The mechanism of sex determination varies substantively among evolutionary lineages. One important mode of genetic sex determination is haplodiploidy, which is used by approximately 20% of all animal species, including >200,000 species of the entire insect order Hymenoptera. In the honey bee Apis mellifera, a hymenopteran model organism, females are heterozygous at the csd (complementary sex determination) locus, whereas males are hemizygous (from unfertilized eggs). Fertilized homozygotes develop into sterile males that are eaten before maturity. Because homozygotes have zero fitness and because common alleles are more likely than rare ones to form homozygotes, csd should be subject to strong overdominant selection and negative frequency-dependent selection. Under these selective forces, together known as balancing selection, csd is expected to exhibit a high degree of intraspecific polymorphism, with long-lived alleles that may be even older than the species. Here we sequence the csd genes as well as randomly selected neutral genomic regions from individuals of three closely related species, A. mellifera, Apis cerana, and Apis dorsata. The polymorphic level is approximately seven times higher in csd than in the neutral regions. Gene genealogies reveal trans-species polymorphisms at csd but not at any neutral regions. Consistent with the prediction of rare-allele advantage, nonsynonymous mutations are found to be positively selected in csd only in early stages after their appearances. Surprisingly, three different hypervariable repetitive regions in csd are present in the three species, suggesting variable mechanisms underlying allelic specificities. Our results provide a definitive demonstration of balancing selection acting at the honey bee csd gene, offer insights into the molecular determinants of csd allelic specificities, and help avoid homozygosity in bee breeding.

SUBMITTER: Cho S

PROVIDER: S-EPMC1626638 | biostudies-literature | 2006 Nov

REPOSITORIES: biostudies-literature

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Evolution of the complementary sex-determination gene of honey bees: balancing selection and trans-species polymorphisms.

Cho Soochin S Huang Zachary Y ZY Green Daniel R DR Smith Deborah R DR Zhang Jianzhi J

Genome research 20061025 11

The mechanism of sex determination varies substantively among evolutionary lineages. One important mode of genetic sex determination is haplodiploidy, which is used by approximately 20% of all animal species, including >200,000 species of the entire insect order Hymenoptera. In the honey bee Apis mellifera, a hymenopteran model organism, females are heterozygous at the csd (complementary sex determination) locus, whereas males are hemizygous (from unfertilized eggs). Fertilized homozygotes devel ...[more]

PMID: 17065615

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Project description:Sex determination mechanisms play a central role in life-history characteristics, affecting mating systems, sex ratios, inbreeding tolerance, etc. Downstream components of sex determination pathways are highly conserved, but upstream components evolve rapidly. Evolutionary dynamics of sex determination remain poorly understood, particularly because mechanisms appear so diverse. Here we investigate the origins and evolution of complementary sex determination (CSD) in ants and bees. The honey bee has a well-characterized CSD locus, containing tandemly arranged homologs of the transformer gene [complementary sex determiner (csd) and feminizer (fem)]. Such tandem paralogs appear frequently in aculeate hymenopteran genomes. However, only comparative genomic, but not functional, data support a broader role for csd/fem in sex determination, and whether species other than the honey bee use this pathway remains controversial. Here we used a backcross to test whether csd/fem acts as a CSD locus in an ant (Vollenhovia emeryi). After sequencing and assembling the genome, we computed a linkage map, and conducted a quantitative trait locus (QTL) analysis of diploid male production using 68 diploid males and 171 workers. We found two QTLs on separate linkage groups (CsdQTL1 and CsdQTL2) that jointly explained 98.0% of the phenotypic variance. CsdQTL1 included two tandem transformer homologs. These data support the prediction that the same CSD mechanism has indeed been conserved for over 100 million years. CsdQTL2 had no similarity to CsdQTL1 and included a 236-kb region with no obvious CSD gene candidates, making it impossible to conclusively characterize it using our data. The sequence of this locus was conserved in at least one other ant genome that diverged >75 million years ago. By applying QTL analysis to ants for the first time, we support the hypothesis that elements of hymenopteran CSD are ancient, but also show that more remains to be learned about the diversity of CSD mechanisms.

Project description:BackgroundWith the completion of a single nucleotide polymorphism (SNP) chip for honey bees, the technical basis of genomic selection is laid. However, for its application in practice, methods to estimate genomic breeding values need to be adapted to the specificities of the genetics and breeding infrastructure of this species. Drone-producing queens (DPQ) are used for mating control, and usually, they head non-phenotyped colonies that will be placed on mating stations. Breeding queens (BQ) head colonies that are intended to be phenotyped and used to produce new queens. Our aim was to evaluate different breeding program designs for the initiation of genomic selection in honey bees.MethodsStochastic simulations were conducted to evaluate the quality of the estimated breeding values. We developed a variation of the genomic relationship matrix to include genotypes of DPQ and tested different sizes of the reference population. The results were used to estimate genetic gain in the initial selection cycle of a genomic breeding program. This program was run over six years, and different numbers of genotyped queens per year were considered. Resources could be allocated to increase the reference population, or to perform genomic preselection of BQ and/or DPQ.ResultsIncluding the genotypes of 5000 phenotyped BQ increased the accuracy of predictions of breeding values by up to 173%, depending on the size of the reference population and the trait considered. To initiate a breeding program, genotyping a minimum number of 1000 queens per year is required. In this case, genetic gain was highest when genomic preselection of DPQ was coupled with the genotyping of 10-20% of the phenotyped BQ. For maximum genetic gain per used genotype, more than 2500 genotyped queens per year and preselection of all BQ and DPQ are required.ConclusionsThis study shows that the first priority in a breeding program is to genotype phenotyped BQ to obtain a sufficiently large reference population, which allows successful genomic preselection of queens. To maximize genetic gain, DPQ should be preselected, and their genotypes included in the genomic relationship matrix. We suggest, that the developed methods for genomic prediction are suitable for implementation in genomic honey bee breeding programs.

Project description:BACKGROUND:Managed, feral and wild populations of European honey bee subspecies, Apis mellifera, are currently facing severe colony losses globally. There is consensus that the ectoparasitic mite Varroa destructor, that switched hosts from the Eastern honey bee Apis cerana to the Western honey bee A. mellifera, is a key factor driving these losses. For >20 years, breeding efforts have not produced European honey bee colonies that can survive infestations without the need for mite control. However, at least three populations of European honey bees have developed this ability by means of natural selection and have been surviving for >10 years without mite treatments. Reduced mite reproductive success has been suggested as a key factor explaining this natural survival. Here, we report a managed A. mellifera population in Norway, that has been naturally surviving consistent V. destructor infestations for >17 years. METHODS:Surviving colonies and local susceptible controls were evaluated for mite infestation levels, mite reproductive success and two potential mechanisms explaining colony survival: grooming of adult worker bees and Varroa Sensitive Hygiene (VSH): adult workers specifically detecting and removing mite-infested brood. RESULTS:Mite infestation levels were significantly lower in surviving colonies and mite reproductive success was reduced by 30% when compared to the controls. No significant differences were found between surviving and control colonies for either grooming or VSH. DISCUSSION:Our data confirm that reduced mite reproductive success seems to be a key factor for natural survival of infested A. mellifera colonies. However, neither grooming nor VSH seem to explain colony survival. Instead, other behaviors of the adult bees seem to be sufficient to hinder mite reproductive success, because brood for this experiment was taken from susceptible donor colonies only. To mitigate the global impact of V. destructor, we suggest learning more from nature, i.e., identifying the obviously efficient mechanisms favored by natural selection.

Dataset Information

Evolution of the complementary sex-determination gene of honey bees: balancing selection and trans-species polymorphisms.

Publications

Evolution of the complementary sex-determination gene of honey bees: balancing selection and trans-species polymorphisms.

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