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Apis Florea and Apis Cerana Workers Do Not Discriminate Between Queen-Laid and Worker-Laid Apis Mellifera Eggs Piyamas N

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Apis Florea and Apis Cerana Workers Do Not Discriminate Between Queen-Laid and Worker-Laid Apis Mellifera Eggs Piyamas N Apis florea and Apis cerana workers do not discriminate between queen-laid and worker-laid Apis mellifera eggs Piyamas N. Sopaladawan, Benjamin P. Oldroyd, Siriwat Wongsiri To cite this version: Piyamas N. Sopaladawan, Benjamin P. Oldroyd, Siriwat Wongsiri. Apis florea and Apis cerana workers do not discriminate between queen-laid and worker-laid Apis mellifera eggs. Apidologie, 2019, 50 (5), pp.681-688. 10.1007/s13592-019-00678-9. hal-02910740 HAL Id: hal-02910740 https://hal.archives-ouvertes.fr/hal-02910740 Submitted on 3 Aug 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 (2019) 50:681–688 Original Article * INRA, DIB and Springer-Verlag France SAS, part of Springer Nature, 2019 DOI: 10.1007/s13592-019-00678-9 Apis florea and Apis cerana workers do not discriminate between queen-laid and worker-laid Apis mellifera eggs 1 2 3 Piyamas N. SOPALADAWAN , Benjamin P. OLDROYD , Siriwat WONGSIRI 1Department of Biology, Faculty of Science, Mahasarakham University, Khamriang, Kantarawichai, Maha Sarakham 44150, Thailand 2Behaviour and Genetics of Social Insects Laboratory, Ecology and Evolution, University of Sydney, Macleay Building A12, Sydney, NSW 2006, Australia 3The Academy of Science, The Royal Society of Thailand, Dusit, Bangkok 10330, Thailand Received 14 November 2018 – Revised 17 May 2019 – Accepted 15 July 2019 Abstract – While honey bee workers have functional ovaries, worker reproduction is rare in colonies with a laying queen. An important mechanism by which functional worker sterility is enforced is worker policing—any behaviour of workers that prevents other workers from reproducing. In honey bees, policing workers identify worker-laid eggs and eat them. Policing workers apparently distinguish queen-laid eggs from eggs laid by workers using as yet unidentified chemical signals placed on eggs. These signals are conserved across evolutionary time because the Western hive bee Apis mellifera can distinguish queen- and worker-laid eggs of the phylogenetically distant dwarf honey bee Apis florea .HoweverA . mellifera cannot distinguish queen- and worker-laid eggs of the more closely related species Apis cerana .HereweshowthatA . cerana and A . florea workers do not distinguish queen-laid from worker-laid eggs of A . mellifera ,eventhoughA . cerana (but not A . florea ) tolerate A . mellifera eggs for extended periods. Apis florea / Apis cerana / Apis mellifera / worker policing / egg-marking signals 1. INTRODUCTION thread-like ovaries in which egg production is absent (Halling et al. 2001; Oldroyd et al. 2001a, In eusocial hymenopterans, the males are hap- b; Wattanachaiyingcharoen et al. 2002). In loid and arise from unfertilized eggs, whereas queenright colonies of the Western honey bee, females (queens and workers) are diploid and A . mellifera , only one worker in 10,000 has a arise from fertilized eggs (Dzierzon 1845; fully developed egg in her ovary (Ratnieks 1993), Crozier and Pamilo 1996). This means that in and workers produce less than 7% of the male- many species, unmated workers can lay eggs that destined eggs (Visscher 1996). Almost all worker- result in viable males (Bourke 1988). However, in laid eggs are promptly removed by worker polic- most species, workers with a queen rarely lay eggs ing (Ratnieks and Visscher 1989;Ratnieks1993). and reproduction is monopolized by mated ‘Worker policing’ is any behaviour of workers queens. For example, in honey bee (Apis )colo- that prevents other workers from producing sons, nies, the vast majority of honey bee workers have either by aggression toward reproductive workers or by the destruction of worker-laid eggs (Ratnieks 1988; Ratnieks and Visscher 1989; Ratnieks and Reeve 1992; Barron et al. 2001; Corresponding author: P. Sopaladawan, [email protected] Ratnieks and Wenseleers 2005). Worker policing Manuscript editor: David Tarpy likely evolves via two processes. First, in 682 P. N. Sopaladawan et al. polyandrous species, where workers are more re- (Ratnieks 1995; Oldroyd et al. 2002;Beekman lated to their queen’ssons(r= 0.25) than to the et al. 2004). The queen’s egg-marking signal ben- sons of their half-sisters (r = 0.125), workers are efits both the queen (sender) and police workers selected to prefer to rear their queen’ssonsrather (receiver) (Seeley 1985; Heinz and d’Ettorre than their half-sister’s sons (Hamilton 1964; 2009). The signal benefits the queen because it Ratnieks 1988). Second, colony efficiency can reinforces her reproductive hegemony. Police be compromised if a large proportion of workers workers benefit because the signal allows them are reproductive (Montague and Oldroyd 1998). to raise more-related QL eggs and fewer, less- In species where policing is highly effective, the related, WL eggs. benefits of egg laying are much diminished for A clear prediction of inter-animal signaling workers, and they are likely to evolve reproduc- theory is that if signals are honest and benefit both tive ‘acquiescence’. Where acquiescence has sender and receiver, then the signal should be evolved, workers with a queen rarely (and in some stable over evolutionary time (Hefetz and species never) produce eggs (Wenseleers et al. Katzav-Gozansky 2004;Nanorketal.2007b; 2004a, b; Wenseleers and Ratnieks 2006). Jäger 2008). In contrast, if a signal benefits only Even though worker acquiescence (sterility) one party, or if a party can benefit by mimicking may have evolved because it benefits the collective the signal, the signal may change over evolution- workers, individual workers are still more related to ary time as the receiver changes its response to the their own eggs than to queen-laid (hereafter QL) or signal to its own advantage, possibly by ignoring worker-laid (hereafter WL) eggs (Ratnieks 1988). it (Hefetz and Katzav-Gozansky 2004; Jäger Therefore, there is an evolutionary tension between 2008). In this circumstance, the sender may alter the optimal behaviour for the individual and the its signal, so that it can be recognized as genuine. optimal behaviour of the collective workers We have previously shown that colonies of A . (Wenseleers et al. 2004a, b; Ratnieks et al. 2006). mellifera can distinguish QL from WL eggs of the Indeed,eveninaspecieslikeA . mellifera where red dwarf honey bee, Apis florea , but cannot worker acquiescence is almost complete, some distinguish between QL and WL eggs of the Asian workers successfully produce offspring during hive bee, Apis cerana (Nanork et al. 2007b). A . swarming periods (Woyciechowski and mellifera and A . cerana diverged less than 3 mya Kuszewska 2012;Holmesetal.2013; Kuszewska (Arias and Sheppard 2005), whereas the diver- et al. 2018). It is also possible to artificially select gence of A . florea from the A . mellifera -A . for high levels of worker reproduction (Oldroyd cerana clade is much more ancient (Arias and and Osborne 1999) and low levels of policing Sheppard 2005; Raffiudin and Crozier 2007;Lo (Oldroyd et al. 2001a, b). et al. 2010), about 6–10 mya (Engel 1998;Engel The underlying genetic and phenotypic plastic- 1999). This suggests that an ‘episode of revolu- ity in worker sterility means that workers can po- tion’ (Wenseleers et al. 2004a, b) has occurred in tentially evolve resistance to policing, leading to A . cerana (Nanork et al. 2007b)inwhich,A . ‘episodes of worker revolution’ (Wenseleers et al. cerana workers evolved to mimic the queen’s 2004a, b). During these episodes, a species endures egg-marking signal, forcing a change in the queen a period when the efficiency of policing declines, egg-marking signal. That means that whereas the workers contribute a significant proportion of the queen’s egg-marking signal is similar in A . male offspring of a colony, and the species suffers mellifera and A . florea , it has diverged between the ergonomic costs of increased intra-colony con- A . mellifera and A . cerana , despite their more flict and reduced ergonomic efficiency. recent co-ancestry. Police workers discriminate queen-laid (QL) Here we present the reverse experiment of eggs from worker-laid (WL) eggs using unidenti- Nanork et al. (2007b) to investigate the relative fied signals present on eggs (Katzav-Gozansky abilities of A . florea and A . cerana to discrimi- et al. 1997; 2001; Barron et al. 2001; Martin nate QL and WL eggs of A . mellifera . We pre- et al. 2002, 2005). This signal is most likely a dicted that A . florea would retain some ability to queen-derived pheromone placed on eggs distinguish QL and WL eggs of A . mellifera , Apis florea and Apis cerana workers do not discriminate between queen-laid... 683 whereas A . cerana would be less able or unable suspended underneath each colony in the po- to distinguish QL and WL eggs of A . mellifera . sition of natural drone comb. Before the ex- Note that both A . florea (Halling et al. 2001)and periment, we hung each test comb next to a A . cerana (Oldroyd et al. 2001a)policeWLeggs queenright discriminator colony so that the of their own species, while retaining QL eggs. bees cleaned and polished it. 2. MATERIALS AND METHODS A . cerana Four colonies were wild-caught from Samut Songkhram, transferred to artificial boxes, 2.1. Sources of eggs and left to establish their nests at the natal site for 2 weeks (Nanork et al. 2007a, b). We transported Four colonies of A . mellifera were transferred the four queenright A . cerana colonies to the to a coconut plantation in Damnoen Saduak, coconut plantation in Ratchaburi and left them Ratchaburi Province, Thailand. The colonies were there for a week prior to performing experiment.
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