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Insights into the role of age and social interactions on the sexual attractiveness of queens in an eusocial bee, Melipona flavolineata (Apidae, Meliponini)

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Abstract

The attraction of sexual partners is a vital necessity among insects, and it involves conflict of interests and complex communication systems among male and female. In this study, we investigated the developing of sexual attractiveness in virgin queens (i.e., gynes) of Melipona flavolineata, an eusocial stingless bee. We followed the development of sexual attractiveness in 64 gynes, belonging to seven age classes (0, 3, 6, 9, 15, 18 days post-emergence), and we also evaluated the effect of different social interactions (such as competition between queens and interactions with workers) on the development of attractiveness in other 60 gynes. We used the number of males that tried to mate with a focal gyne as a representative variable of its sexual attractiveness. During the essays, each gyne was individually presented to 10 sexually mature males, and during 3 min, we counted the number of males that everted their genitalia in response to the presence of a gyne. Here, we show that M. flavolineata gynes are capable to (i) maintain their sexual attractiveness for long periods through adult life, (ii) they need a minimum social interaction to trigger the development of sexual attractiveness, and (iii) that gynes express this trait only within a social context. We conclude that the effective occurrence of matings is conditional on potential social interactions that gynes experienced before taking the nuptial flight, when they are still in the nest. These findings bring insights into the factors determining reproductive success in social insects.

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References

  • Alcock J (2001) Animal behavior: an evolutionary approach, 7th edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Amsalem E, Hefetz A (2010) The appeasement effect of sterility signaling in dominance contests among Bombus terrestris workers. Behav Ecol Sociobiol 64:1685–1694. doi:10.1007/s00265-010-0982-4

    Article  Google Scholar 

  • Bespalova I, Helms K (2014) Social selection and the evolution of a female weapon in queens of the ant Messor pergandei (Hymenoptera: Formicidae). Biol J Linn Soc 113:1011–1020

    Article  Google Scholar 

  • Camargo CA (1972) Mating of the social bee Melipona quadrifasciata under controlled conditions (Hymenoptera, Apidae). J Kansas Entomol Soc 45:520–523

    Google Scholar 

  • Châline N, Ratnieks FLW, Raine NE et al (2004) Non-lethal sampling of honey bee, Apis mellifera, DNA using wing tips. Apidologie 35:311–318. doi:10.1051/apido:2004015

    Article  Google Scholar 

  • da Silva DN, Zucchi R, Kerr W (1972) Biological and behavioural aspects of the reproduction in some species of Melipona (Hymenoptera, Apidae, Meliponinae). Anim Behav 20:123–132

    Article  PubMed  Google Scholar 

  • de Souza EA, Neves CA, Campos LA de O et al (2007) Effect of mating delay on the ovary of Melipona quadrifasciata anthidioides (Hymenoptera: Apidae) queens. Micron 38:471–477. doi:10.1016/j.micron.2006.08.005

    Article  PubMed  Google Scholar 

  • Emerson AE (1939) Populations of social insects. Ecol Monogr 9:287–300. doi:10.2307/1943230

    Article  Google Scholar 

  • Engels E, Engels W (1988) Age-dependent queen attractiveness for drones and mating in the stingless bee, Scaptotrigona postica. J Apic Res 27:3–8

    Article  Google Scholar 

  • Engels W, Engels E, Francke W (1997) Ontogeny of cephalic volatile patterns in queens and mating biology of the neotropical stingless bee, Scaptotrigona postica. Invertebr Reprod Dev 31:251–256. doi:10.1080/07924259.1997.9672583

    Article  CAS  Google Scholar 

  • van Engelsdorp D, Hayes J, Underwood RM, Pettis J (2008) A survey of honey bee colony losses in the U.S., fall 2007 to spring 2008. PLoS One 3:e4071. doi:10.1371/journal.pone.0004071

    Article  PubMed  Google Scholar 

  • Fewell JH, Page RE (1999) The emergence of division of labour in forced associations of normally solitary ant queens. Evol Ecol Res 1:537–548

    Google Scholar 

  • Fierro MM, Cruz-López L, Sánchez D et al (2011) Queen volatiles as a modulator of Tetragonisca angustula drone behavior. J Chem Ecol 37:1255–1262

    Article  CAS  PubMed  Google Scholar 

  • Foster KR, Seppä P, Ratnieks FLW, Thorén PA (1999) Low paternity in the hornet Vespa crabro indicates that multiple mating by queens is derived in vespine wasps. Behav Ecol Sociobiol 46:252–257. doi:10.1007/s002650050617

    Article  Google Scholar 

  • Foster RL, Brunskill A, Verdirame D, O’Donnell S (2004) Reproductive physiology, dominance interactions, and division of labour among bumble bee workers. Physiol Entomol 29:327–334. doi:10.1111/j.0307-6962.2004.00388.x

    Article  Google Scholar 

  • Gans C (1987) The sensory world of animals. In: Hoage R (ed) Animal intelligence. Insights into the animal mind. Smithsonian Institution Press, Washington, pp 89–103

    Google Scholar 

  • Gilley DC, Tarpy DR (2005) Three mechanisms of queen elimination in swarming honey bee colonies. Apidologie 36:461–474. doi:10.1051/apido:2005033

    Article  Google Scholar 

  • Gilley DC, Tarpy DR, Land BB (2003) Effect of queen quality on interactions between workers and dueling queens in honeybee (Apis mellifera L.) colonies. Behav Ecol Sociobiol 55:190–196. doi:10.1007/s00265-003-0708-y

    Article  Google Scholar 

  • Grajales-Conesa J, Rojas JC, Guzman-Diaz M (2006) Cephalic and Dufour gland secretions of Scaptotrigona mexicana queens: chemical composition and biological activity. Apidologie 38:38–46. doi:10.1051/apido

    Article  Google Scholar 

  • Hartfelder K, Marker GR, Judice CC et al (2006) Physiological and genetic mechanisms underlying caste development, reproduction and division of labor in stingless bees. Apidologie 37:144–163

    Article  CAS  Google Scholar 

  • Human H, Brodschneider R, Dietemann V et al (2013) Miscellaneous standard methods for Apis mellifera research. J Apic Res 52:1–53. doi:10.3896/IBRA.1.52.4.10

    Article  Google Scholar 

  • Imperatriz-Fonseca VL, Zucchi R (1995) Virgin queens in stingless bee (Apidae, Meliponinae) colonies: a review. Apidologie 26:231–244

    Article  Google Scholar 

  • Imperatriz-Fonseca VL, Matos ET, Ferreira F, Velthuis HHW (1998) A case of multiple mating in stingless bees (Meliponinae). Insect Soc 45:231–233

    Article  Google Scholar 

  • Jarau S, Van Veen JW, Aguilar I, Ayasse M (2009) Virgin queen execution in the stingless bee Melipona beecheii: the sign stimulus for worker attacks. Apidologie 40:496–507. doi:10.1051/apido/2009022

    Article  Google Scholar 

  • Jarau S, van Veen JW, Aguilar I, Ayasse M (2010) A scientific note on virgin queen acceptance in stingless bees: evidence for the importance of queen aggression. Apidologie 41:38–39. doi:10.1051/apido/2009045

    Article  Google Scholar 

  • Kärcher MH, Menezes C, Alves DA et al (2013) Factors influencing survival duration and choice of virgin queens in the stingless bee Melipona quadrifasciata. Naturwissenschaften 100:571–580. doi:10.1007/s00114-013-1053-2

    Article  PubMed  Google Scholar 

  • Kerr WE (1950) Genetic determination of castes in the genus Melipona. Genetics 35(2):143–152

  • Koedam D, Aguilar Monge I, Sommeijer MJ (1995) Social interactions of gynes and their longevity in queenright colonies of Melipona favosa (Apidae: Meliponinae). Netherlands J Zool 45:480–494

    Article  Google Scholar 

  • Korb J, Heinze J (2004) Multilevel selection and social evolution of insect societies. Naturwissenschaften 91:291–304. doi:10.1007/s00114-004-0529-5

    Article  CAS  PubMed  Google Scholar 

  • Lebreton S, Trona F, Borrero-Echeverry F et al (2015) Feeding regulates sex pheromone attraction and courtship in Drosophila females. Sci Rep 5:13132. doi:10.1038/srep13132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin N, Michener CD (1972) Evolution of sociality in insects. Q Rev Biol 47:131–159

    Article  Google Scholar 

  • Michener C (2007) The bees of the world, 2nd edn. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • de Moraes BC, da Costa JMN, da Costa ACL, Costa MH (2005) Variação espacial e temporal da precipitação no Estado do Pará. Acta Amaz 35:207–214. doi:10.1590/S0044-59672005000200010

    Article  Google Scholar 

  • Pedro SRM (2014) The stingless bee fauna in Brazil (Hymenoptera: Apidae). Sociobiology 61:348–354. doi:10.13102/sociobiology.v61i4.348-354

    Article  Google Scholar 

  • Pettis JS, Rice N, Joselow K et al (2016) Colony failure linked to low sperm viability in honey bee (Apis mellifera) queens and an exploration of potential causative factors. PLoS One 11:e0147220. doi:10.1371/journal.pone.0147220

    Article  PubMed  PubMed Central  Google Scholar 

  • Ryan MJ (1997) Sexual selection and mate choice. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell Publishing, Oxford, pp 179–202

    Google Scholar 

  • Siegel SC, Castellan NJ Jr (1988) Nonparametric statistics for the behavioural sciences, 2nd edn. McGraw-Hill, New York

    Google Scholar 

  • Sommeijer MJ, Bruijn LLM, Meeuwsen JAJ, Slaa J (2003) Reproductive behaviour of stingless bees: nest departures of non-accepted gynes and nuptial flights in Melipona favosa (Hymenoptera: Apidae, Meliponini). Entomol Ber 63:7–13

    Google Scholar 

  • Tarpy DR, Gilley DC, Seeley TD (2004) Levels of selection in a social insect: a review of conflict and cooperation during honey bee (Apis mellifera) queen replacement. Behav Ecol Sociobiol 55:513–523. doi:10.1007/s00265-003-0738-5

    Article  Google Scholar 

  • Tautz J (2008) The buzz about bees: biology of a superorganism. Springer Science & Business Media

  • Van Veen JW, Sommeijer MJ, Monge IA (1999) Behavioural development and abdomen inflation of gynes and newly mated queens of Melipona beecheii (Apidae, Meliponinae). Insect Soc 46:361–365

    Article  Google Scholar 

  • Velthuis HHW, Vries HD, Imperatriz-Fonseca VL (2006) The polygyny of Melipona bicolor: scramble competition among queens. Apidologie 37:222–239

    Article  Google Scholar 

  • Venturieri GC, de Raiol VFO, Pereira CAB (2003) Avaliação da introdução da criação racional de Melipona fasciculata (Apidae: Meliponina), entre os agricultores familiares de Bragança - PA, Brasil. Biota Neotrop 3:1–7. doi:10.1590/S1676-06032003000200003

    Article  Google Scholar 

  • Wenseleers T, Ratnieks FLW (2004) Tragedy of the commons in Melipona bees. Proc R Soc London B 271:S310–S312. doi:10.1098/rsbl.2003.0159

    Article  Google Scholar 

  • Wenseleers T, Hart AG, Ratnieks FLW, Quezada-Euán JJG (2004) Queen execution and caste conflict in the stingless bee Melipona beecheii. Ethology 110:725–736

    Article  Google Scholar 

  • Wilson EO (1971) The insect societies. Harvard University Press, Cambridge

    Google Scholar 

  • Zar J (1999) Biostatistical Analysis, 4th edn. Pearson Education India

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Acknowledgements

We thank MSc. Ana Carolina Martins de Queiroz, MSc. Kamila Leão Leão, and MSc. Epifânia Emanuela de Macêdo Rocha for assistance during the experiments. We also thank Dr. Ayrton Vollet Neto for providing critical reading of early drafts of the manuscript, Dr. Alistair Campbell for linguistic advice, and the anonymous referees for the valuable comments which really improved this manuscript.

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Authors and Affiliations

  1. Laboratório de Biologia e Ecologia de Abelhas, Instituto de Ciências Biológicas, Universidade Federal do Pará, Rua Augusto Corrêa 01, Campus Básico, Belém, Pará, 66075-110, Brazil

    Jamille Costa Veiga & Felipe Andrés León Contrera

  2. Laboratório de Botânica, Embrapa Amazônia Oriental, Travessa Enéas Pinheiro, s/n; PO. 18, Belém, Pará, 66095-100, Brazil

    Cristiano Menezes

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  1. Jamille Costa Veiga
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  3. Felipe Andrés León Contrera
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Correspondence to Jamille Costa Veiga.

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Funding

This study was funded by CNPq (479710/2011-2, 400435/2014-4) and FAPESPA (ICAAF 30/2011). JCV was funded by CAPES (CAPES/EMBRAPA 15/2014).

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The authors declare that they have no conflict of interest.

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Communicated by: Sven Thatje

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(DOCX 2312 kb).

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Behaviors performed by dominant Melipona flavolineata gynes (Hymenoptera, Apidae, Meliponini): the video starts by presenting a dominant gyne, which is not attacked. In sequence, we show a non-dominant gyne, killed by workers and thrown in the nest’s garbage area. We also show the behaviors related to dominance-subordination mechanism, with emphasis on the interactions with workers. (MP4 100,331 kb).

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Veiga, J.C., Menezes, C. & Contrera, F.A.L. Insights into the role of age and social interactions on the sexual attractiveness of queens in an eusocial bee, Melipona flavolineata (Apidae, Meliponini). Sci Nat 104, 31 (2017). https://doi.org/10.1007/s00114-017-1450-z

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  • DOI: https://doi.org/10.1007/s00114-017-1450-z

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