Racial mixing in South African honeybees: the effects of genotype mixing on reproductive traits of workers

Beekman, Madeleine; Allsopp, Michael H.; Holmes, Michael J.; Lim, Julianne; Noach-Pienaar, Lee-Ann; Wossler, Theresa C.; Oldroyd, Benjamin P.

doi:10.1007/s00265-012-1338-z

Cited by 11 publications

(10 citation statements)

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“…Our findings therefore support the hypothesis that Capensis fathers epigenetically modify certain genes in order to enhance the reproductive capacities of their female offspring. Our results support previous studies showing strong parent-of-origin effects for reproductive traits in honey bees in general and Capensis in particular (Beekman et al 2012;Oldroyd et al 2014;Galbraith et al 2016).…”

Section: Discussionsupporting

confidence: 92%

“…In reciprocal crosses between Africanised and European honey bee strains, worker offspring with Africanised fathers have significantly more ovarioles and increased patrigenene-biased gene expression than offspring with European fathers (Galbraith et al 2016). In reciprocal crosses between Capensis and a non-thelytokous subspecies, Apis mellifera scutellata (hereafter Scutellata), worker offspring with a Capensis father are heavier, more likely to possess a spermatheca (Beekman et al 2012), and have 30% more ovarioles (Oldroyd et al 2014). Thelytokouslyproduced diploid Capensis eggs possessing only a maternal genome have fewer hypermethylated genes than sexually-produced eggs with two contributing parental genomes (Remnant et al 2016).…”

Section: Introductionmentioning

confidence: 99%

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Paternal effects on Apis mellifera capensis worker ovary size

et al. 2017

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The kinship theory of genomic imprinting argues that conflicting reproductive interests between males and females can lead to epigenetic modifications to the genome, altering gene expression in offspring in a parent-oforigin specific manner. The phenomenon is well documented in mammals and angiosperms, while the evidence for imprinting in social insects is steadily increasing. Workers of the South African honey bee, Apis mellifera capensis (Capensis) produce fatherless female offspring via thelytokous parthenogenesis, whereas queens produce female eggs sexually. We examined differences in reproductive phenotype between thelytokously and sexually derived Capensis workers. Workers with a father had significantly more ovarioles than fatherless workers, suggesting that males may imprint genes to enhance the reproductive success of their worker offspring. Apis mellifera capensis / imprinting / genomic conflict / kinship theory Electronic supplementary material The online version of this article (

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Section: Discussionsupporting

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Paternal effects on Apis mellifera capensis worker ovary size

et al. 2017

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“…When Capensis queens were crossed with A. m. carnica males, thelytoky was expressed in offspring workers, but when crossed with A. m. ligustica males, offspring workers reproduced arrhenotokously (Ruttner, 1988), indicating an effect of sire independent of the genetic background of the queen. Similarly, aspects of honey bee defensiveness (Guzman-Novoa et al, 2005) and reproductive physiology (Jordan et al, 2008a;Linksvayer et al, 2009;Beekman et al, 2012;Oldroyd et al, 2014) are more strongly transmitted via males than via females. Honey bees have a fully functional DNA methylation system (Wang et al, 2006;Foret et al, 2009) and differential methylation depending on parent-of-origin could explain the observed effects of sire (Drewell et al, 2012;Drewell et al, 2014;Oldroyd et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Inheritance of thelytoky in the honey bee Apis mellifera capensis

Chapman

Beekman

Allsopp³

et al. 2015

Heredity

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Asexual reproduction via thelytokous parthenogenesis is widespread in the Hymenoptera, but its genetic underpinnings have been described only twice. In the wasp Lysiphlebus fabarum and the Cape honey bee Apis mellifera capensis the origin of thelytoky have each been traced to a single recessive locus. In the Cape honey bee it has been argued that thelytoky (th) controls the thelytoky phenotype and that a deletion of 9 bp in the flanking intron downstream of exon 5 (tae) of the gemini gene switches parthenogenesis from arrhenotoky to thelytoky. To further explore the mode of inheritance of thelytoky, we generated reciprocal backcrosses between thelytokous A. m. capensis and the arrhenotokous A. m. scutellata. Ten genetic markers were used to identify 108 thelytokously produced offspring and 225 arrhenotokously produced offspring from 14 colonies. Patterns of appearance of thelytokous parthenogenesis were inconsistent with a single locus, either th or tae, controlling thelytoky. We further show that the 9 bp deletion is present in the arrhenotokous A. m. scutellata population in South Africa, in A. m. intermissa in Morocco and in Africanized bees from Brazil and Texas, USA, where thelytoky has not been reported. Thus the 9 bp deletion cannot be the cause of thelytoky. Further, we found two novel tae alleles. One contains the previously described 9 bp deletion and an additional deletion of 7 bp nearby. The second carries a single base insertion with respect to the wild type. Our data are consistent with the putative th locus increasing reproductive capacity.

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“…In reality, a stable hybrid zone that neither subspecies is able to cross without human intervention (Beekman et al 2008) now separates the two populations. Hybrid or mixed colonies of Capensis and Scutellata are assumed to suffer from reduced fitness (Beekman et al 2008(Beekman et al , 2012, though evidence for this hypothesis is currently lacking. Scutellata drones and virgin queens may outcompete Capensis at mating leks.…”

Section: The Evolution Of Thelytoky In Capensismentioning

confidence: 99%

Thelytoky in the honey bee

Goudie

Oldroyd

2014

Apidologie

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Thelytoky, the asexual production of females, is rare in honey bees. However, it is ubiquitous in workers of the Cape honey bee Apis mellifera capensis. Thelytoky allows some workers to be reincarnated into the queen phenotype, and thereby selects for reproductive competition among workers. Thelytoky also acts as an exaptation for the emergence of reproductive parasites, the most extreme example of which is an entirely clonal 'cancerous' lineage of workers (the Clone) that lethally parasitises colonies of another subspecies Apis mellifera scutellata. The Clone is an enigma because thelytoky results in the accumulation of homozygosity at any loci that are free to recombine, yet the Clone retains considerable heterozygosity. The Clone pays a cost for its thelytoky: the selective removal of homozygous offspring at each generation. We propose that workers, queens and Clones have differing abilities to endure the costs and benefits of sex and asexuality, accounting for the heterogeneous distribution of reproductive strategies across the A. mellifera capensis population. We further suggest that multiple factors must fall into place for thelytoky to emerge as an effective reproductive strategy in a honey bee population, and that geographic isolation resulting in genetic drift and founder effects may have enabled thelytoky to emerge in A. mellifera capensis. Finally, we consider the honey bee in the broader context of haplodiploid Hymenoptera, and argue that constraints on the evolution of sex in non-haplodiploid taxa may make sexual reproduction an evolutionary 'one-way street'.

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Racial mixing in South African honeybees: the effects of genotype mixing on reproductive traits of workers

Cited by 11 publications

References 37 publications

Paternal effects on Apis mellifera capensis worker ovary size

Paternal effects on Apis mellifera capensis worker ovary size

Inheritance of thelytoky in the honey bee Apis mellifera capensis

Thelytoky in the honey bee

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