Abstract
Body size has frequently been discussed as related to reproductive success. Stingless bees show remarkable variation in body size among and within sexes and castes, but very little is known about the proximate causes and the consequences of such variation in these highly eusocial bees. In this study, we evaluated the effect of different amounts of food provided to the larvae on developmental time, body size, abdominal mass, and vitellogenin (Vg) hemolymph titers of gynes of the stingless bee Scaptotrigona pectoralis, a species with trophic caste determination. Our results provide empirical evidence of a significant effect of the quantity of larval food on the duration of development, body size, and traits of reproductive fitness. We discuss proximate causes that may explain gyne size variation in stingless bees. We see this as an initial step towards understanding the adaptive significance and ultimate causes of this phenomenon in highly eusocial bees.
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References
Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225. https://doi.org/10.1146/annurev-ento-112408-085356
Baptistella AR, Souza CCM, Santana WC, Soares AEE (2012) Techniques for the in vitro production of queens in stingless bees (Apidae, Meliponini). Sociobiology 59:297–310. https://doi.org/10.13102/sociobiology.v59i1.685
Boggs LC, Freeman K (2005) Larval food limitation in butterflies: effects on adult resource allocation and fitness. Oecologia 144:353–361. https://doi.org/10.1007/s00442-005-0076-6
Borsuk G, Ptaszyńska AA, Olszewski K, Domaciuk M, Krutmuang P, Paleolog J (2007) A new method for quick and easy hemolymph collection from Apidae adults. PLoS ONE 12:1–9. https://doi.org/10.1371/journal.pone.0170487
Bosch J, Vicens N (2006) Relationship between body size, provisioning rate, longevity and reproductive success in females of the solitary bee Osmia cornuta. Behav Ecol Sociobiol 60:26–33. https://doi.org/10.1007/s00265-005-0134-4
Buschini MLT, Campos LAO (1995) Caste determination in Trigona spinipes (Hymenoptera, Apidae): influence of the available food and juvenile hormone. Rev Bras Biol 55:121–129
Chan QWT, Foster JL (2008) Changes in protein expression during honey bee larval development. Genome Biol 9:R156. https://doi.org/10.1186/gb-2008-9-10-r156
Chinh TX, Grob GBJ, Meeuwsen FJAJ, Sommeijer MJ (2003) Patterns of male production in the stingless bee Melipona favosa (Apidae, Meliponini). Apidologie 34:161–170. https://doi.org/10.1051/apido:2003008
Chole H, Woodard SH, Bloch G (2019) Body size variation in bees: regulation, mechanisms, and relationship to social organization. Curr Opin Insect Sci 35:77–87. https://doi.org/10.1016/j.cois.2019.07.006
Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, Hughes KA, Robinson GE (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci U S A 104:7128–7133. https://doi.org/10.1073/pnas.0701909104
Davidowitz G, D’Amico LJ, Nijhout HF (2003) Critical weight in the development of insect body size. Evol Dev 5:188–197. https://doi.org/10.1046/j.1525-142x.2003.03026.x
De Souza DA, Kaftanoglu O, De Jong D, Page Jr. RE, Amdam GV, Wang Y (2018) Differences in the morphology, physiology and gene expression of honey bee queens and workers reared in vitro versus in situ. Biol Open 7:bio036616. Doi: https://doi.org/10.1242/bio.036616
De Souza DA, Hartfelder K, Tarpy DR (2019) Effects of larval age at grafting and juvenile hormone on morphometry and reproductive quality parameters of in vitro reared honey bees (Hymenoptera: Apidae). J Econ Entomol 112:2030–2039. https://doi.org/10.1093/jee/toz148
Dmitriew C, Rowe L (2011) The effects of larval nutrition on reproductive performance in a food-limited adult environment. PLoS ONE 30:e17399. https://doi.org/10.1371/journal.pone.0017399
Dos Santos CF, Souza Dos Santos PD, Blochtein B (2016) In vitro rearing of stingless bee queens and their acceptance rate into colonies. Apidologie 47:539–547. https://doi.org/10.1007/s13592-015-0398-2
Engels W (1974) Occurrence and significance of vitellogenin in female castes of social Hymenoptera. Am Zool 14:1229–1237
Engels W, Imperatriz-Fonseca VL (1990) Caste development, reproductive strategies, and control of fertility in honey bees and stingless bees. In: Engels W (ed) Social Insects - an evolutionary approach to castes and reproduction. Springer, Berlin, pp 167–230
Guidugli KR, Nascimento AM, Amdam GV, Barchuk AR, Omholt S, Simões ZLP, Hartfelder K (2005) Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Lett 579:4961–4965. https://doi.org/10.1016/j.febslet.2005.07.085
Gutiérrez E, Ruiz D, Solís T, de May-Itzá W, J, Moo-Valle H, Quezada-Euán JJG, (2016) Does larval food affect cuticular profiles and recognition in eusocial bees? A test on Scaptotrigona gynes (Hymenoptera: Meliponini). Behav Ecol Sociobiol 70:781–789. https://doi.org/10.1007/s00265-016-2109-z
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1
Hartfelder K, Engels W (1989) The composition of larval food in stingless bees: evaluating nutricional balance by chemosystematic methods. Insectes Soc 36:1–14. https://doi.org/10.1007/BF02225876
Hartfelder K, Engels W (1992) Allometric and multivariate analysis of sex and caste polymorphism in the neotropical stingless bee, Scaptotrigona postica. Insectes Soc 39:251–266. https://doi.org/10.1007/BF01323946
Hartfelder K, Engels W (1998) Social insect polymorphism: Hormonal regulation of plasticity in development and reproduction in the honeybee. Curr Topics Dev Biol 40:45–77. https://doi.org/10.1016/s0070-2153(08)60364-6
Hartfelder K, Makert G, Judice C, Pereira G, Santana W, Dallacqua R, Bitondi M (2006) Physiological and genetic mechanisms underlying caste development, reproduction and division of labor in stingless bees. Apidologie 37:144–163. https://doi.org/10.1051/apido:2006013
Hartfelder K, Bitondi M, Brent C, Guidugli-Lazzarini K, Simões Z, Stabentheiner A, Tanaka E, Wang Y (2013) Standard methods for physiology and biochemistry research in Apis mellifera. J Apic Res 52(1). https://doi.org/https://doi.org/10.3896/IBRA.1.52.1.06
Hatjina F, Bieńkowska M, Charistos L, Chlebo R, Costa C et al (2014) A review of methods used in some European countries for assessing the quality of honey bee queens through their physical characters and the performance of their colonies. J Apic Res 53:337–363. https://doi.org/10.3896/IBRA.1.53.3.02
Haydak MH (1970) Honey bee nutrition. Annu Rev Entomol 15:143–156. https://doi.org/10.1146/annurev.en.15.010170.001043
Hurtado-Burillo M, May-Itzá W de J, Quezada-Euán JJG, De la Rúa P, Ruiz C (2017) Multilocus species delimitation in Mesoamerican Scaptotrigona stingless bees (Apidae: Meliponini) supports the existence of cryptic species. Syst Entomol 42:171-181. https://doi.org/https://doi.org/10.1111/syen.12201
Imperatriz-Fonseca VL, Cruz-Landim C, Silva de Moraes RLM (1997) Dwarf gynes in Nannotrigona testaceicornis (Apidae, Meliponinae, Trigonini), behaviour, exocrine gland morphology and reproductive status. Apidologie 28:113–122. https://doi.org/10.1051/apido:19970302
Johnson MD (1990) Female size and fecundity in the small carpenter bee, Ceratina calcarata (Robertson) (Hymenoptera: Anthophoridae). J Kansas Entomol Soc 63:414–419
Kahya Y, Genҫer HV, Woyke J (2008) Weight at emergence of honey bee (Apis mellifera caucasica) queens and its effect on live weights at the pre and post mating periods. J Apic Res 47:118–125. https://doi.org/10.1080/00218839.2008.11101437
Kramer BH, Schaible R (2013) Colony size explains the life span differences between queens and workers in eusocial Hymenoptera. Biol J Linn Soc 109:710–724. https://doi.org/10.1111/bij.12072
Lau P, Bryant V, Ellis JD, Huang Z-Y, Sullivan J, Schmehl DR et al (2019) Seasonal variation of pollen collected by honey bees (Apis mellifera) in developed areas across four regions in the United States. PLoS ONE 14:e0217294. https://doi.org/10.1371/journal.pone.0217294
Leather SR (1988) Size, reproductive potential and fecundity in insects: things aren’t as simple as they seem. Oikos 51:386–389. https://doi.org/10.2307/3565323
Leimar O, Hartfelder K, Laubichler MD, Page RE Jr (2012) Development and evolution of caste dimorphism in honeybees: a modeling approach. Ecol Evol 2:3098–3109. https://doi.org/10.1002/ece3.414
Lisboa LCO, Serrão JC, Cruz-Landim C, Campos LAO (2005) Effect of larval food amount on ovariole development in queens of Trigona spinipes (Hymenoptera, Apinae). Anat Histol Embryol 34:179–184. https://doi.org/10.1111/j.1439-0264.2005.00591.x
Medina RG, Fairbairn DJ, Bustillos A, Moo-Valle H, Medina S, Quezada-Euán JJG (2016) Variable patterns of intraspecific sexual size dimorphism and allometry in three species of eusocial corbiculate bees. Insectes Soc 63:493–500. https://doi.org/10.1007/s00040-016-0491-1
Menezes C, Bonetti AM, Amaral IMR, Kerr WE (2007) Larval feeding of Melipona (Hymenoptera, Apidae): study of individual brood cells. Bioscience J 1:70–75
Menezes C, Vollet-Neto A, Imperatriz-Fonseca VL (2013) An advance in the in vitro rearing of stingless bee queens. Apidologie 44:491–500. https://doi.org/10.1007/s13592-013-0197-6
Mirth CK, Riddiford LM (2007) Size assessment and growth control: how adult size is determined in insects. BioEssays 29:344–355. https://doi.org/10.1002/bies.20552
Moo-Valle H, Quezada-Euán JJG, Wenseleers T (2001) The effect of food reserves on the production of sexual offspring in the stingless bee Melipona beecheii (Apidae, Meliponini). Insectes Soc 48:398–403. https://doi.org/10.1007/PL00001797
Moo-Valle H, Quezada-Euán JJG, Canto-Martín J, González- Acereto JA (2004) Caste ontogeny and the distribution of reproductive cells on the combs of Melipona beecheii (Apidae: Meliponini). Apidologie 35:587–594. https://doi.org/10.1051/apido:2004054
Moritz B, Crailsheim K (1987) Physiology of protein digestion in the midgut of the honeybee (Apis mellifera L.). J Insect Physiol 33:923–931. https://doi.org/10.1016/0022-1910(87)90004-7
Nijhout HJ, Riddiford LM, Mirth CK, Shingleton AW, Suzuki Y, Callier V (2014) The developmental control of size in insects. Wiley Interdiscip Rev Dev Biol 3:113–134. https://doi.org/10.1002/wdev.124
Nilsen KA, Ihle KE, Frederick K, Fondrk MK, Smedal B, Hartfelder K, Amdam GV (2011) Insulin-like peptide genes in honey bee fat body respond differently to manipulation of social behavioral physiology. J Exp Biol 214:1488–1497. https://doi.org/10.1242/jeb.050393
Oliveira VTP, Cruz-Landim C (2006) Histological and ultrastructural aspects of the fat body in virgin and physogastric queens of Melipona quadrifasciata anthidioides Lepeletier, 1836 (Hymenoptera, Apidae, Meliponini). Braz J Morphol Sci 23:385–392
Pereira RA, Morais MM, Nascimento FS, Bego LR (2009) Intrinsic colony conditions affect the provisioning and oviposition process in the stingless bee Melipona scutellaris. Genet Mol Res 8:725–729. https://doi.org/10.4238/vol8-2kerr034
Quezada-Euán JJG (2018) Stingless bees of Mexico: the biology, management and conservation of an ancient heritage. Springer, New York
Quezada-Euán JJG, López-Velasco A, Pérez-Balam J, Moo-Valle H, Velazquez-Madrazo A, Paxton RJ (2011) Body size differs in workers produced across time and is associated with variation in the quantity and composition of larval food in Nannotrigona perilampoides (Hymenoptera, Meliponini). Insectes Soc 58:31–38. https://doi.org/10.1007/s00040-010-0113-2
Quezada-Euán JJG, Sanabria-Urbán S, Smith C, Cueva del Castillo R (2019) Patterns of sexual size dimorphism in stingless bees: testing Rensch’s rule and potential causes in highly eusocial bees (Hymenoptera: Apidae, Meliponini). Ecol Evol 9:2688–2698. https://doi.org/10.1002/ece3.4935
Radmacher S, Strohm E (2009) Factors affecting offspring body size in the solitary bee Osmia bicornis (Hymenoptera, Megachilidae). Apidologie 41:169–177. https://doi.org/10.1051/apido/2009064
Ramalho M, Imperatriz-Fonseca VL, Giannini TC (1998) Within-colony size variation of foragers and pollen load capacity in the stingless bee Melipona quadrifasciata anthidioides Lepeletier (Apidae, Hymenoptera). Apidologie 29:221–228. https://doi.org/10.1051/apido:19980302
Ribeiro MF, Imperatriz-Fonseca VL, Santos-Filho PS (2003) Exceptional high queen production in the Brazilian stingless bee Plebeia remota. Stud Neotrop Fauna E 38:111–114. https://doi.org/10.1076/snfe.38.2.111.15925
Ribeiro MdF, Wenseleers T, Filho PdSS, Alves DdA (2006) Miniature queens in stingless bees: Basic facts and evolutionary hypotheses. Apidologie 37:191–206. https://doi.org/10.1051/apido:2006023
Ribeiro MF, Santos-Filho PS, Imperatriz-Fonseca VL (2006) Size variation and egg laying performance in Plebeia remota queens (Hymenoptera, Apidae, Meliponini). Apidologie 37:653–664. https://doi.org/10.1051/apido:2006046
Sakagami SF (1982) Stingless bees. In: Hermann HR (ed) Social Insects, Vol. III, Academic Press, London, pp. 361–423
Salmela H, Amdam GV, Freitak D (2015) Transfer of immunity from mother to offspring is mediated via egg-yolk protein vitellogenin. PLoS Pathog 11:1–12
Salmela H, Stark T, Stucki D, Fuchs S, Freitak D, Dey A, Kent CF, Zayed A et al (2016) Ancient duplications have led to functional divergence of vitellogenin-like genes potentially involved in inflammation and oxidative stress in honey bees. Genome Biol Evol 8:495–506
Seehuus S-C, Norberg K, Gimsa U et al (2006) Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc Natl Acad Sci USA 103:962–967
Shi YY, Huang ZY, Zeng ZJ, Wang ZL, Wu XB et al (2011) Diet and cell size both affect queen-worker differentiation through DNA methylation in honey bees (Apis mellifera, Apidae). PLoS ONE 6:e18808. https://doi.org/10.1371/journal.pone.0018808
Slansky F Jr, Scriber JM (1985) Food consumption and utilization. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 4. Pergamon Press, Oxford, pp 87–163
Slater GP, Yocum GD, Bowsher JH (2020) Diet quantity influences caste determination in honeybees (Apis mellifera). Proc R Soc B 287:20200614. https://doi.org/10.1098/rspb.2020.0614
Sommeijer MJ, De Bruijn LLM, Van de Guchte C (1985) The social food flow within the colony of a stingless bee, Melipona favosa (F.). Behaviour 92:39–58
Tarpy DR, Gilley DC (2004) Group decision making during queen production in colonies of highly eusocial bees. Apidologie 35:207–216. https://doi.org/10.1051/apido:2004008
Teder T (2014) Sexual size dimorphism requires a corresponding sex difference in development time: a meta-analysis in insects. Funct Ecol 28:479–486. https://doi.org/10.1111/1365-2435.12172
van Veen JW (2000) Cell provisioning and oviposition in Melipona beecheii (Apidae, Meliponinae), with a note on caste determination. Apidologie 31:411–419. https://doi.org/10.1051/apido:2000131
Veiga JC, Menezes C, Venturieri G, Contrera FAL (2013) The bigger the smaller: relationship between body size and food stores in the stingless bee Melipona flavolineata. Apidologie 44:324–333. https://doi.org/10.1007/s13592-012-0183-4
Velthuis HHW, Cortopassi-Laurino M, Pereboom Z, Imperatriz-Fonseca VL (2003) Speciation, development, and the conservative egg of the stingless bee genus Melipona. Proc Exp Appl Entomol 14:53–57
Wenseleers T, Hart AG, Ratnieks FLW, Quezada-Euan JJG (2004) Queen execution and caste conflict in the stingless bee Melipona beecheii. Ethology 110:725–736. https://doi.org/10.1111/j.1439-0310.2004.01008.x
Wenseleers T, Ratnieks FLW, Ribeiro MF, Alves DA, Imperatriz-Fonseca VL (2005) Working-class royalty: bees beat the caste system. Biol Lett 1:125–128. https://doi.org/10.1098/rsbl.2004.0281
West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York
Wu X, Zhou L, Zou C, Zeng Z (2018) Effects of queen cell size and caging days of mother queen on rearing young honey bee queens Apis mellifera L. J Apic Sci 62:215–222. https://doi.org/10.2478/jas-2018-0025
Acknowledgments
We thank two anonymous reviewers and Professor Miriam Richards for their valuable comments to improve our manuscript. The article is part of AM thesis for which she received a CONACyT grant. CONACyT project 291333 “Manejo sustentable de polinizadores” supported this investigation. Many thanks to Biol. Teresita Solis for help in lab work and data collection.
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Morales, A., Hartfelder, K., Medina-Peralta, S. et al. Larval food provisions affect developmental time, body size and vitellogenin titers of Scaptotrigona pectoralis gynes (Hymenoptera: Meliponini). Insect. Soc. 68, 93–100 (2021). https://doi.org/10.1007/s00040-020-00801-5
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DOI: https://doi.org/10.1007/s00040-020-00801-5