Abstract
Independent-founding paper wasps constitute a major group of primitively eusocial insects, and when caste-fate determination occurs in temperate species of these wasps, particularly regarding whether it occurs before or after emergence, remains unclear. No critical morphological differences occur between potential queens of the next generation (often called gynes) and workers in primitively eusocial insects. The gynes of temperate species are characterized by diapausing, and the nutrients available during the larval stage have often been believed to determine caste fate. Short days usually induce diapause in temperate nonsocial insects, although few investigations of the effects of day length on caste-fate determination in paper wasps have been conducted. By exposing individuals to different combinations of short and long days during the immature and adult stages, we show for the first time that short days during the adult stage (but not during the immature stage) facilitated caste-fate determination toward gynes in a paper wasp. Moreover, the decision to diapause partly depended on changes in the photoperiod during the pupal and adult stages. The size of the adult also affected caste-fate determination, with diapause more likely to occur in large adults, but this size effect did not occur when individuals were exposed to many short days during the pupal stage. In addition, all adults except for a small proportion of smaller individuals prepared for diapause under short days. These findings suggest that the photoperiod is a higher priority cue than adult size.
Similar content being viewed by others
References
Adkisson PL, Bell RA, Wellso SG (1963) Environmental factors controlling the induction of diapause in the pink bollworm, Pectinophora gossypiella (Saunders). J Insect Physiol 9(3):299–310. https://doi.org/10.1016/0022-1910(63)90107-0
Berens AJ, Hunt JH, Toth AL (2015) Nourishment level affects caste-related gene expression in Polistes wasps. BMC Genomics 16(1):235. https://doi.org/10.1186/s12864-015-1410-y
Bohm MK (1972) Effects of environment and juvenile hormone on ovaries of the wasp, Polistes metricus. J Insect Physiol 18(10):1875–1883. https://doi.org/10.1016/0022-1910(72)90158-8
Bourke AFG (1999) Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12(2):245–257. https://doi.org/10.1046/j.1420-9101.1999.00028.x
Cytel (2012) LogXact 10 user manual. Cytel Inc, Cambridge
Danks HV (1987) Insect dormancy: an ecological perspective. Monograph series no. 1. Biological survey of Canada, Ottawa
Dapporto L, Palagi E, Turillazzi S (2005) Sociality outside the nest: helpers in pre-hibernating clusters of Polistes dominulus. Ann Zool Fenn 42:135–139
Dapporto L, Petrocelli I, Turillazzi S (2011) Incipient morphological castes in Polistes gallicus (Vespidae, Hymenoptera). Zoomorphology 130(3):197–201. https://doi.org/10.1007/s00435-011-0130-3
Eickwort K (1969) Separation of the castes of Polistes exclamans and notes on its biology (Hym.: Vespidae). Insect Soc 16(1):67–72. https://doi.org/10.1007/BF02224464
Evans HE, West-Eberhard MJ (1970) The wasps. Univ of Michigan Press, Ann Arbor
Foster DR, Crowder LA (1980) Diapause of the pink bollworm, Pectinophora gossypiella (Saunders), related to dietary lipids. Comp Biochem Physiol B 65(4):723–726. https://doi.org/10.1016/0305-0491(80)90186-8
Haggard CM, Gamboa GJ (1980) Seasonal variation in body size and reproductive condition of a paper wasp, Polistes metricus (Hymenoptera: Vespidae). Can Entomol 112(03):239–248. https://doi.org/10.4039/Ent112239-3
Hahn DA, Denlinger DL (2011) Energetics of insect diapause. Annu Rev Entomol 56(1):103–121. https://doi.org/10.1146/annurev-ento-112408-085436
Hartfelder K, Emlen DJ (2012) Endocrine control of insect polyphenism. In: Gilbert LI (ed) Insect endocrinology. Academic Press, San Diego, pp 464–522. https://doi.org/10.1016/B978-0-12-384749-2.10011-1
Hunt JH (1991) Nourishment and the evolution of the social Vespidae. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell Univ Press, New York, pp 426–450
Hunt JH (2006) Evolution of castes in Polistes. Ann Zool Fenn 43:407–422
Hunt JH (2012) A conceptual model for the origin of worker behaviour and adaptation of eusociality. J Evol Biol 25(1):1–19. https://doi.org/10.1111/j.1420-9101.2011.02421.x
Hunt JH, Kensinger BJ, Kossuth JA, Henshaw MT, Norberg K, Wolschin F, Amdam GV (2007) A diapause pathway underlies the gyne phenotype Polistes wasps, revealing an evolutionary route to caste-containing insect societies. Proc Natl Acad Sci U S A 104(35):14020–14025. https://doi.org/10.1073/pnas.0705660104
Jeanne RL (2003) Social complexity in the Hymenoptera, with special attention to the wasps. In: Kikuchi T, Azuma N, Higashi S (eds) Genes, behaviors and evolution of social insects. Hokkaido Univ Press, Sapporo, pp 81–131
Jeanne RL, Suryanarayanan S (2011) A new model for caste development in social wasps. Comm Integr Biol 4(4):373–377. https://doi.org/10.4161/cib.15262
Judd TM, Magnus RM, Fasnacht MP (2010) A nutritional profile of the social wasp Polistes metricus: differences in nutrient levels between castes and changes within castes during the annual life cycle. J Insect Physiol 56(1):42–56. https://doi.org/10.1016/j.jinsphys.2009.09.002
Judd TM, Teal PEA, Hernandez EJ, Choudhury T, Hunt JH (2015) Quantitative differences in nourishment affect caste-related physiology and development in the paper wasp Polistes metricus. PLoS One 10(2):e0116199. https://doi.org/10.1371/journal.pone.0116199
Kelstrup HC, Hartfelder K, Esterhuizen N, Wossler TC (2017) Juvenile hormone titers, ovarian status and epicuticular hydrocarbons in gynes and workers of the paper wasp Belonogaster longitarsus. J Insect Physiol 98:83–92. https://doi.org/10.1016/j.jinsphys.2016.11.014
Kono Y (1979) Abnormal photoperiodic and phototactic reactions of the beetle, Epilachna vigintioctopunctata, reared on sliced potatoes. Appl Entomol Zool 14(2):185–192. https://doi.org/10.1303/aez.14.185
Kozyra KB, Baraniak E (2016) Causes of mortality of Polistes nimpha colonies. Insect Soc 63(3):481–482. https://doi.org/10.1007/s00040-016-0484-0
Michener CD (1974) The social behavior of the bees. Harvard Univ Press, Cambridge
O’Donnell S (1998) Reproductive caste determination in eusocial wasps (Hymenoptera: Vespidae). Annu Rev Entomol 43(1):323–346. https://doi.org/10.1146/annurev.ento.43.1.323
Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton Univ Press, Princeton
Petrocelli I, Turillazzi S (2013) The morphology of Van der Vecth’s organ as a tool to measure caste dimorphism in Polistes paper wasps: a comparative approach. J Zool Syst Evol Res 51:274–278
Queller DC (1996) The origin and maintenance of eusociality: the advantage of extended parental care. In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper wasps. Oxford University Press, Oxford, pp 218–234
Reeve HK (1991) Polistes. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell Univ Press, New York, pp 99–148
Reeve HK, Peters JM, Nonacs P, Starks PT (1998) Dispersal of first “workers” in social wasps: causes and implications of an alternative reproductive strategy. Proc Natl Acad Sci U S A 95(23):13737–13742. https://doi.org/10.1073/pnas.95.23.13737
Santos BF, Payne A, Pickett KM, Carpenter JM (2015) Phylogeny and historical biogeography of the paper wasp genus Polistes (Hymenoptera: Vespidae): implications for the overwintering hypothesis of social evolution. Cladistics 31(5):535–549. https://doi.org/10.1111/cla.12103
Saunders DS (1997) Under-sized larvae from short-day adults of the blow fly, Calliphora vicina, side-step the diapause programme. Physiol Entomol 22(3):249–255. https://doi.org/10.1111/j.1365-3032.1997.tb01165.x
Saunders DS (2002) Insect clocks, 3rd edn. Elsevier Science, Amsterdam
Smith CR, Toth AL, Suarez AV, Robinson GE (2008) Genetic and genomic analyses of the division of labour in insect societies. Nature Revs Gen 9(10):735–748. https://doi.org/10.1038/nrg2429
Solís CR, Strassmann JE (1990) Presence of brood affects caste differentiation in the social wasp, Polistes exclamans Viereck (Hymenoptera: Vespidae). Funct Ecol 4(4):531–541. https://doi.org/10.2307/2389321
Strassmann JE, Lee RE, Rojas RR, Baust JG (1984) Caste and sex differences in cold-hardiness in the social wasps, Polistes annularis and Polistes exclamans (Hymenoptera, Vespidae). Insect Soc 31(3):291–301. https://doi.org/10.1007/BF02223613
Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects. Oxford Univ Press, New York
Tibbetts EA (2007) Dispersal decisions and predispersal behavior in Polistes paper wasp ‘workers’. Behav Ecol Sociobiol 61(12):1877–1883. https://doi.org/10.1007/s00265-007-0427-x
Tibbetts EA, Levy S, Donajkowski K (2011) Reproductive plasticity in Polistes paper wasp workers and the evolutionary origins of sociality. J Insect Physiol 57(7):995–999. https://doi.org/10.1016/j.jinsphys.2011.04.016
Toth AL, Bilof KBJ, Henshaw MT, Hunt JH, Robinson GE (2009) Lipid stores, ovary development, and brain gene expression in Polistes metricus females. Insect Soc 56(1):77–84. https://doi.org/10.1007/s00040-008-1041-2
Wilson EO (1971) The insect societies. Harvard Univ Press, Cambridge
Yamane S (1996) Ecological factors influencing the colony cycle of Polistes wasps. In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper wasps. Oxford University Press, Oxford, pp 75–97
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Sven Thatje
Rights and permissions
About this article
Cite this article
Yoshimura, H., Yamada, Y.Y. Caste-fate determination primarily occurs after adult emergence in a primitively eusocial paper wasp: significance of the photoperiod during the adult stage. Sci Nat 105, 15 (2018). https://doi.org/10.1007/s00114-018-1541-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-018-1541-5