Exceptionally high levels of recombination across the honey bee genome

Beye, Martin; Gattermeier, Irene; Hasselmann, Martin; Gempe, Tanja; Schioett, Morten; Baines, John F.; Schlipalius, David I.; Mougel, Florence; Emore, Christine; Rueppell, Olav; Sirviö, Anu; Guzmán-Novoa, Ernesto; Hunt, Greg J.; Solignac, Michel; Page, Robert E.

doi:10.1101/gr.5680406

Cited by 177 publications

(227 citation statements)

References 44 publications

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“…This analysis demonstrates that the socially advanced honeybee A. mellifera and the ants studied to date (all of which are socially advanced) are characterized by unusually high recombination densities. For the honeybee, Beye et al (2006) have shown that this high recombination density is a genome-wide phenomenon, although there is large local variation. The authors particularly showed that whereas there are weak positive correlations with GC-content and repetitive DNA, recombination densities are not influenced by chromosome size.…”

Section: Discussionmentioning

confidence: 99%

Variation in genomic recombination rates among animal taxa and the case of social insects

2007

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Meiotic recombination is almost universal among sexually reproducing organisms. Because the process leads to the destruction of successful parental allele combinations and the creation of novel, untested genotypes for offspring, the evolutionary forces responsible for the origin and maintenance of this counter-intuitive process are still enigmatic. Here, we have used newly available genetic data to compare genome-wide recombination rates in a report on recombination rates among different taxa. In particular, we find that among the higher eukaryotes exceptionally high rates are found in social Hymenoptera. The high rates are compatible with current hypotheses suggesting that sociality in insects strongly selects for increased genotypic diversity in worker offspring to either meet the demands of a sophisticated caste system or to mitigate against the effects of parasitism. Our findings might stimulate more detailed research for the comparative study of recombination frequencies in taxa with different life histories or ecological settings and so help to understand the causes for the evolution and maintenance of this puzzling process.

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Section: Discussionmentioning

confidence: 99%

Variation in genomic recombination rates among animal taxa and the case of social insects

2007

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“…Watterson's estimator of the population mutation rate per base (θ w ) in African bees was 0.79%, whereas native European subspecies had lower levels of variation (average θ w values of 0.30% and 0.33% for the C and M groups, respectively), and Middle-Eastern subspecies were intermediate (average θ w value of 0.47%; Table 1 and Supplementary Note), in concordance with previous studies based on a few loci 16 . We also note an extremely fast decay of linkage disequilibrium (LD) with physical distance, which reflects the high recombination rate in honeybees 18 (~50% reduction in the r 2 linkage statistic with only 500 bp; Supplementary Fig. 4).…”

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confidence: 81%

A worldwide survey of genome sequence variation provides insight into the evolutionary history of the honeybee Apis mellifera

et al. 2014

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“…Specifically, for each chromosome, we created a function relating recombination distance to physical distance using a least squares fit of a six-term polynomial of physical distance to recombination distance; R 2 . 0.99 for all chromosomes (Beye et al 2006;Solignac et al 2007). After estimating QTL position, QTL allele frequencies were estimated and used to estimate QTL substitution effects, a i , for each mapping population (following Dekkers 2000; Wang et al 2007).…”

Section: Methodsmentioning

confidence: 99%

The Genetic Basis of Transgressive Ovary Size in Honeybee Workers

et al. 2009

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Ovarioles are the functional unit of the female insect reproductive organs and the number of ovarioles per ovary strongly influences egg-laying rate and fecundity. Social evolution in the honeybee (Apis mellifera) has resulted in queens with 200-360 total ovarioles and workers with usually 20 or less. In addition, variation in ovariole number among workers relates to worker sensory tuning, foraging behavior, and the ability to lay unfertilized male-destined eggs. To study the genetic architecture of worker ovariole number, we performed a series of crosses between Africanized and European bees that differ in worker ovariole number. Unexpectedly, these crosses produced transgressive worker phenotypes with extreme ovariole numbers that were sensitive to the social environment. We used a new selective pooled DNA interval mapping approach with two Africanized backcrosses to identify quantitative trait loci (QTL) underlying the transgressive ovary phenotype. We identified one QTL on chromosome 11 and found some evidence for another QTL on chromosome 2. Both QTL regions contain plausible functional candidate genes. The ovariole number of foragers was correlated with the sugar concentration of collected nectar, supporting previous studies showing a link between worker physiology and foraging behavior. We discuss how the phenotype of extreme worker ovariole numbers and the underlying genetic factors we identified could be linked to the development of queen traits.T HE number of ovariole filaments per ovary is an important female reproductive character that affects fecundity across insect taxa (Richard et al. 2005;Makert et al. 2006). Social insect lineages have evolved a strong dimorphism in ovariole number between reproductive and nonreproductive castes. For example, while most families of bees consistently have 6 total ovarioles, and most species in the family Apidae have 8, the highly social species in the genus Apis (the honeybees) have queens that can have .360 total ovarioles and workers that often have ,10 (Winston 1987;Michener 2003). This queen-worker dimorphism is of primary importance because it translates into differential reproductive potential that defines the social roles of these female castes (Winston 1987) and classifies social species in general (Sherman et al. 1995). Furthermore, ovary size (i.e., ovariole number) is the most sensitive indicator of caste-specific development in honeybees (Dedej et al. 1998). The extreme increase in ovariole number for queen honeybees enables high egg-laying rates (.1500 per day) and is apparently a result of selection for increased colony reproduction (growth and fission by swarming) (Seeley 1997). Honeybee queens are thus highly specialized for egg laying, similar to queens of several other social insect taxa, such as army ants or higher termites (Hö lldobler and Wilson 1990). Honeybee workers in contrast, do not normally reproduce but perform all other essential activities including foraging for nectar, pollen, and water; caring for brood; and building, main...

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Exceptionally high levels of recombination across the honey bee genome

Cited by 177 publications

References 44 publications

Variation in genomic recombination rates among animal taxa and the case of social insects

Variation in genomic recombination rates among animal taxa and the case of social insects

A worldwide survey of genome sequence variation provides insight into the evolutionary history of the honeybee Apis mellifera

The Genetic Basis of Transgressive Ovary Size in Honeybee Workers

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