Paternal effects on Apis mellifera capensis worker ovary size Rebecca J. Reid, Emily J. Remnant, Michael H. Allsopp, Madeleine Beekman, Benjamin P. Oldroyd To cite this version: Rebecca J. Reid, Emily J. Remnant, Michael H. Allsopp, Madeleine Beekman, Benjamin P. Oldroyd. Paternal effects on Apis mellifera capensis worker ovary size. Apidologie, 2017, 48 (5), pp.660-665. 10.1007/s13592-017-0510-x. hal-02973436 HAL Id: hal-02973436 https://hal.archives-ouvertes.fr/hal-02973436 Submitted on 21 Oct 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2017) 48:660–665 Original article * INRA, DIB and Springer-Verlag France, 2017 DOI: 10.1007/s13592-017-0510-x Paternal effects on Apis mellifera capensis worker ovary size 1 1 2 1 Rebecca J. REID , Emily J. REMNANT , Michael H. ALLSOPP , Madeleine BEEKMAN , 1 Benjamin P. OLDROYD 1Behaviour and Genetics of Social Insects Laboratory, Macleay Building A12, University of Sydney, Camperdown, New South Wales 2006, Australia 2Honey Bee Research Section, ARC-Plant Protection Research Institute, Private Bag X5017, Stellenbosch, South Africa Received 16 November 2016 – Revised 30 March 2017 – Accepted 13 April 2017 Abstract – 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-of- origin 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 1. INTRODUCTION his offspring can secure more resources from their mother at the expense of half-siblings, with which Kin selection theory normally assumes that the father shares no genes. In so doing, he in- matrigenes and patrigenes (genes inherited from creases his offsprings’ chances of survival, thus the mother and father, respectively) are equally maximizing the chance of future spread of his expressed in offspring (Queller 2003). Under nor- genes throughout the gene pool. Conversely, it is mal Mendelian inheritance, dominant traits are in the mother’s interest to ensure all her offspring expressed in offspring regardless of whether they are equally provided for, as she is equally related were inherited from the mother or the father. to each. The kinship theory of genomic imprinting However, differences in the level of investment (Haig 2000;Haig2004) argues that such intersex- in offspring by males and females can lead to ual genomic conflict can manifest as heritable intersexual conflict, wherein the expression of a epigenetic modifications to the genome that alter gene in one sex has a fitness cost if it is expressed gene expression in offspring in a parent-of-origin in the other sex. For instance, a father benefits if specific manner. The most well-known example of imprinting is the insulin-like growth factor II (IGF-II ) gene, Electronic supplementary material The online version of this article (doi:10.1007/s13592-017-0510-x) contains which is involved in foetal growth in mammals supplementary material, which is available to authorized (Haig and Graham 1991). Only the paternally users. inherited IGF-II allele is expressed and acts to Corresponding author: B. Oldroyd, increase foetal growth (DeChiara et al. 1990; [email protected] DeChiara et al. 1991). The maternal copy of the Manuscript Editor: Stan Schneider allele is epigenetically imprinted, or silenced Paternal effects on Apis mellifera capensis worker ovary size 661 (Rappolee et al. 1992). Conversely, the maternal Further, unlike a non-thelytokous honey bee col- copy of the IGF-II receptor (IGF-IIR )is ony, the queen and other workers are predicted to expressed, while the paternal copy is switched be largely indifferent to worker reproduction, as off. IGF-IIR appears to act as ‘sink’ for the IGF- queens are equally related to their daughters and II produced by the paternal genes, degrading their thelytokously produced granddaughters. IGF-II before it can act to increase foetal growth Workers too are equally related to the queen’s (Haig and Graham 1991). These two differentially offspring and the thelytokous offspring of their expressed genes demonstrate an evolutionary tug- sisters (Greeff 1996). As a consequence, worker of-war between males and females as each tries to reproduction occurs at a much higher frequency in gain the upper hand. Capensis colonies than in arrhenotokous honey The reproductive biology of the honey bee Apis bee subspecies, so much so that workers contrib- mellifera provides conditions that are perfect for ute significantly to the production of new queens the evolution of genomic imprinting (Queller (Jordan et al. 2008; Allsopp et al. 2010;Holmes 2003; Kronauer 2008; Drewell et al. 2012). Hon- et al. 2010;Moritzetal.2011). The reproductive ey bees are haplodiploid. In most honey bee sub- advantages of thelytoky, particularly queen pro- species, diploid female queens and workers arise duction, greatly enhance the likelihood of paternal via sexual reproduction and inherit a set of chro- imprinting evolving in this subspecies over other mosomes from both their mother and their father. honey bee subspecies (Oldroyd et al. 2014). Haploid male drones develop via arrhenotokous The increased reproductive advantage afforded parthenogenesis from an unfertilised egg, and thus by thelytokous reproduction appears to have en- inherit genetic material from only their mother. hanced certain reproductive traits in Capensis Honey bee queens are polyandrous, mating with workers. Although Capensis workers cannot 10–20 drones (Estoup et al. 1994; Palmer and mate, they often possess a spermatheca, the sperm Oldroyd 2000; Tarpy et al. 2004). Consider a focal storage organ usually found only in queens worker. Her mother has mated multiple times, and (Ruttner 1988). Queenless Capensis workers pro- none of the worker’s patrigenes are present in her duce queen-like pheromones that inhibit ovary half sisters. While workers are incapable of mat- activation in fellow workers (Moritz et al. 2000). ing (Oster and Wilson 1978), under certain cir- The most significant indicators of increased repro- cumstances, they can produce haploid male off- ductive capacity in honey bees are ovary size and spring via arrhenotoky (Bourke 1988). Thus, epi- activation (Makert et al. 2006). Honey bee ovaries genetic modifications to patrigenes that increase are comprised of multiple ovarioles, the tubes the chances of successful worker reproduction within which eggs are formed (Snodgrass 1956). should be selected for. In contrast, matrigenes Queens have between 180 and 200 ovarioles per should be modified to prevent worker reproduc- ovary (Snodgrass 1956). While the workers of tion, as the queen is more related to her own male most honey bee subspecies have between 3 and offspring than the offspring of daughters (Queller 5 ovarioles, Capensis usually have between 10 2003). and20(Ruttner1977; Allsopp et al. 2003; South Africa is home to a unique honey bee Goudie et al. 2012), indicating a shift towards a subspecies, A. m. capensis (hereafter, Capensis). more ‘queen-like’ physiology. Capensis differs from other subspecies in that The discovery that the honey bee possesses a unmated workers can produce diploid female off- fully functional methylation system (Wang et al. spring without mating via thelytokous partheno- 2006) suggested a mechanism by which honey genesis (Onions 1912; Goudie and Oldroyd bees might imprint their genes (Drewell et al. 2014). Thelytokous reproduction in Capensis has 2012). Subsequently, a number of behavioural, profound effects on the relatedness between colo- molecular and morphological of studies have pro- ny members. A Capensis worker that reproduces vided evidence for paternal imprinting in honey thelytokously is related to her offspring by unity, bees. Distinct DNA methylation patterns between and thus gains considerable fitness benefits from honey bee eggs and sperm are suggestive of reproduction if her offspring is raised as a queen. parent-specific imprinting (Drewell et al. 2014). 662 R.J. Reid et al. In reciprocal crosses between Africanised and reared through to pupation (Oldroyd et al. 2014). European honey bee strains, worker offspring However, the nurse colony did not rear eggs from with Africanised fathers have significantly more all sources; we were only able to obtain both ovarioles and increased patrigenene-biased gene queen-laid brood and worker-laid brood