Abstract
Organisms face the fundamental ecological question of when to switch resources from growth to reproduction or allocate resources between the two. Social wasps, including Vespula species (the yellowjackets), must crucially decide to transition from colony growth to reproductive production before the onset of winter. The timing of this transition could be influenced by worker numbers and environmental factors that affect the fitness of the colony. Early initiation of reproductive production has the advantage that a few reproductives can emerge if the colony collapses prematurely. In contrast, once reproductive production begins, nest growth terminates and the increase of future reproductives should be limited. This study investigated the group decision-making process regarding when and under what circumstances Vespula shidai initiates its reproductive phase. During the early reproductive period, we estimated the number of workers and new queens that emerged from the meconia in the cells. Significantly, a positive correlation was observed between the number of workers and the production of new queens during the early reproductive period. To examine the benefits of early reproduction, we reared V. shidai colonies in a plastic greenhouse, allowed males and new queens to fly and mate freely, and allowed the queens to begin overwintering at their timing. In our experimental environment, new queens that emerged earlier in the reproductive period had a higher survival rate during overwintering and higher dry and fat weights in the following spring. The higher dry and fat weights of the queens suggested better survival during the founding phase of the nest.
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Data Abailability
We provided raw data on the survival time of queens of Vespula shidai during overwintering as supplementary material.
References
Barnes H, Blackstock J (1973) Estimation of lipids in marine animals and tissues: detailed investigation of the sulphophosphovanillin method for ‘total’ lipids. J Exp Mar Biol Ecol 12(1):103–118
Beekman M, Lingeman R, Kleijne FM, Sabelis MW (1998) Optimal timing of the production of sexuals in bumblebee colonies. Entomol Exp Appl 88:147–154
Bonckaert W, Van Zweden JS, D’Ettorre P, Billen J, Wenseleers T (2011) Colony stage and not facultative policing explains pattern of worker reproduction in the Saxon wasp. Mol Ecol 20:3455–3468
Cole LC (1954) The population consequences of life history phenomena. Q Rev Biol 29:103–137
Dobelmann J, Loope KJ, Wilson-Rankin E, Quinn O, Baty JW, Gruber MAM, Lester PJ (2017) Fitness in invasive social wasps: the role of variation in viral load, immune response and paternity in predicting nest size and reproductive output. Oikos 126:1208–1218
Duncan CD (1939) A contribution to the biology of North American vespine wasps. Stanf Univ Publs Biol Sci, California
Ejsmond A, Kozłowski J, Ejsmond MJ (2019) Probing of mortality by staying alive: the growth-reproduction trade-off in a spatially heterogenous environment. Funct Ecol 33:2327–2337. https://doi.org/10.1111/1365-2435.13442
Fucini D, Di Bona V, Mola F, Piccaluga C, Lerenzi MC (2009) Social wasps without workers: geographic variation of caste expression in the paper wasp Polistes biglumis. Insect Soc 56:347–358
Greene A (1984) Production schedules of vespine wasps: an empirical test of the bang-bang optimization model. J Kansas Entomol Soc 57:545–568
Greene A (1991) Dolichovespula and Vespula. In: Ross KG, Matthews RQ (eds.) The Social Biology of Wasps. Ithaca, NY: Comstock Publishing Associates, Cornell University Press. 263–305
Harris RJ, Beggs JR (1995) Variation in the quality of Vespula vulgaris (L.) queens (Hymenoptera: Vespidae) and its significance in wasp population dynamics. N Z J Zool 22:131–142
Heinze J, Tsuji K (1995) Ant reproductive strategies. Res Popul Ecol 37:135–149
Hoiss B, Krauss J, Potts SG, Roberts S, Steffan-Dewenter I (2012) Altitude acts as an environmental filter on phylogenetic composition, traits and diversity in bee communities. Proc R Soc B 279:4447–4456
Jaimes-Nino LM, Heinze J, Oettler J (2022) Late-life fitness gains and reproductive death in Cardiocondyla obscurior ants. Elife 11:e74695
Johnson EL, Cunningham TW, Marriner SM, Kovacs JL, Hunt BG, Bhakta DB, Goodisman MAD (2009) Resource allocation in a social wasp: effects of breeding system and life cycle on reproductive decisions. Mol Ecol 18:2908–2920
Kaspari M, Vargo EL (1995) Colony size as a buffer against seasonality: Bergmann’s rule in social insects. Am Nat 145(4):610–632
Keller L (1993) Queen number and sociality in insects. Oxford University Press, Oxford, United Kingdom
King D, Roughgarden J (1982) Graded allocation between vegetative and reproductive growth for annual plants in growing seasons of random length. Theor Popul Biol 22:1–16
Kocher SD, Pellissier L, Veller C, Purcell J, Nowak MA, Chapuisat M, Pierce NE (2014) Transitions in social complexity along elevational gradients reveal a combined impact of season length and development time on social evolution. Proc R Soc B 281:20140627
Kovacs JL, Goodisman MAD (2012) Effects of size, shape, genotype, and mating status on queen overwintering survival in the social wasp Vespula maculifrons. Environ entomol 41(6):1612–1620
Loope KJ (2016) Matricide and queen sex allocation in a yellowjacket wasp. Sci Nat 103:57
Lopez-Osorio F, Perrard A, Pickett KM, Carpenter JM, Agnarsson I (2015) Phylogenetic tests reject Emery’s rule in the evolution of social parasitism in yellow jackets and hornets (Hymenoptera: Vespidae, Vespinae). R Soc Open Sci 2:150–159
Macevicz S, Oster G (1976) Modeling social insect populations II: optimal reproductive strategies in annual eusocial insect colonies. Behav Ecol Sociobiol 1:265–282
Matsuura M (1995) Social wasp of Japan in color. Hokkkaido University Press, Sappro, Japan
Matsuura M, Yamane S (1990) Biology of the vespine wasps. Springer, Berlin
Matsuzawa H, Shiozaki S (1962) On the seasonal prevalence of two species of flies, Musca domestica vicina MACQUART and Fannia canicularis L. in Kagawa Prefecture. Acad Rep Fac Agric Kagawa Univ 14:32–29
Mitesser O, Weissel N, Strohm E, Poethke HJ (2007) Optimal investment allocation in primitively eusocial bees: a balance model based on resource limitation of the queen. Insectes Soc 54:234–241
Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton, New Jersey
Perrin N, Sibly RM (1993) Dynamic-models of energy allocation and investment. Annu Rev Ecol Syst 24:379–410
Peters RS, Krogmann L, Mayer C, Donath A, Gunkel S, Meusemann K et al (2017) Evolutionary history of the hymenoptera. Curr Biol 27:1013–1018 (PMID:28343967)
R Core Team (2023). R: A language and environment for statistical computing (Version 4.3.1). R Foundation for Statistical Computing. https://www.R-project.org/
Richards MH, Packer L (1994) Trophic aspects of caste determination in Halictus ligatus, a primitively eusocial sweat bee. Behav Ecol Sociobiol 34:385–391
Saga T (2019) Evaluation of the productivity of social wasp colonies (Vespinae) and an introduction to the traditional Japanese vespula wasp hunting technique. J Visual Exp 151:e59044
Saga T, Kanai M, Shimada M, Okada Y (2017) Mutual intra- and interspecific social parasitism between parapatric sister species of Vespula wasps. Insect Soc 64:95–101
Saga T, Okuno M, Loope KJ, Tsuchida K, Ohbayashi K, Shimada M, Okada Y (2020) Polyandry and paternity affect disease resistance in eusocial wasps. Behav Ecol 31(5):1172–1179
Smith ML (2018) Queenless honey bees build infrastructure for direct reproduction until their new queen proves her worth. Evolution 72:2810–2817
Smith ML, Ostwald MM, Loftus JC, Seeley TD (2014) A critical number of workers in a honeybee colony triggers investment in reproduction. Naturwissenschaften 101:783–790
Smith ML, Loope KJ, Chuttong B, Dobelmann J, Makinson JC, Saga T et al (2023) Honey bees and social wasps reach convergent architectural solutions to nest-building problems. PLoS Biol 21(7):e3002211. https://doi.org/10.1371/journal.pbio.3002211
Spradbery JP (1973) Wasps: An Account of the Biology and Natural History of Solitary Social Wasps Sidgwick & Jackson, London
Van Itterbeeck J, Feng Y, Zhao M, Wang C, Tan K, Saga T, Nonaka K, Jung C (2021) Rearing techniques for hornets with emphasis on Vespa velutina (Hymenoptera: Vespidae): a review. J Asia Pac Entomol 24(2):103–117
Watanabe M (2021) Long-term observation of the numbers of overwintering flights of stink bugs in Toyama Prefecture IV. Seasonal fluctuation in overwintering flights of Halyomorpha halys and Menida disjecta. Pestology 36:59–65
Wenzel JW (2020) Nest Structure: Social Wasps. Encycl Soc Insects, 1–14
Wiernasz SC, Cole BJ (2003) Queen size mediates queen survival and colony fitness in harvester ants. Evolution 57:2179–2183
Acknowledgements
The authors would like to thank Tatsuo Aoki, Kazuharu Aoki, Tsutomu Kamata, Shuto Suzuki, Honami Kawabe, and Moe Takahashi for help in collections of wasps. We sincerely thank Dr. Ken-ichi Harano for teaching the measurement of fat content. We are very grateful to Drs. Kevin J. Loope, Yasuoki Takami, Christina Lorenzi (Associate Editor), and two anonymous reviewers for their valuable comments on previous versions of the manuscript. This study was supported in part by The Grant for High School Science Education by Takeda Science Foundation (2013, 2017, 2021), Academic Grants in Zoology by Fujiwara Natural History Foundation (2014 no.13), Scientific Research Grants by Nagano Society for The Promotion of Science (H28-3-9), The 55th and 58th Shimonaka Science Study Grant Contest by Shimonaka Memories Foundation (2016, 2019), Research Grant of Graduate School of Human Development and Environment, Kobe University, Hornet Fund by TAKEO Corporation, and The Dream Project by Come on UP, Ltd.
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Conceptualization and methodology: TS. Data collection: TS, MK. Data analysis: TS. Writing—original draft: TS. Writing—review and editing: TS, MK, MS, YO.
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Saga, T., Kanai, M., Shimada, M. et al. Adaptive significance of early reproduction in Vespula shidai social wasps. Insect. Soc. (2024). https://doi.org/10.1007/s00040-024-00953-8
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DOI: https://doi.org/10.1007/s00040-024-00953-8