Advertisement

Insectes Sociaux

, Volume 65, Issue 3, pp 483–492 | Cite as

Climatic variation across a latitudinal gradient affect phenology and group size, but not social complexity in small carpenter bees

  • S. P. Lawson
  • W. A. Shell
  • S. S. Lombard
  • S. M. Rehan
Research Article

Abstract

Greater social complexity at lower latitudes has been observed in a variety of arthropods from termites to spiders. Social behavior in the small carpenter bees, Ceratina, has been shown to vary widely both between species and across geographic range. Our goal was to determine how social plasticity of three populations of Ceratina species, C. calcarata and C. strenua, vary across a latitudinal gradient. The longer rearing season in the south did not result in two separate brood rearing periods, but instead increased brood production of a single brood with a higher female sex bias. The social structure of nests remained stable across both species’ ranges: mothers exhibit prolonged parental care and worker dwarf eldest daughters occur among populations and species. This is the first report of worker daughters in C. strenua. The ubiquity of worker daughter production in eastern North American Ceratina suggests that factors outside of climate underlie the early division of labor between the reproductive mother and worker dwarf eldest daughter.

Keywords

Social evolution Maternal investment Developmental plasticity Geographic distribution Ceratina 

Notes

Acknowledgements

We thank Cullen Franchino and Michael Mikát for assistance with nest collections in New Hampshire and Terry and Jackie Guilinger for help with nest collections in Missouri. This work was supported by National Science Foundation award numbers 1456296 to SMR, 1450271 to WAS, and 1523664 to SPL. This research was also supported by a Summer Undergraduate Research Fellowship from the Hamel Center for Undergraduate Research at University of New Hampshire to SSL. In addition, this work was made possible through funds from the University of New Hampshire, the New Hampshire Agricultural Experiment Station, and the Tuttle Foundation to SMR.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

40_2018_635_MOESM1_ESM.docx (32 kb)
Supplementary material 1 (DOCX 31 KB)

References

  1. Abrams PA, Leimar O, Nylin S et al (1996) The effect of flexible growth rates on optimal sizes and development times in a seasonal environment. Am Nat 147:381–395CrossRefGoogle Scholar
  2. Addo-Bediako A, Chown SL, Gaston KJ (2002) Metabolic cold adaptation in insects: a large-scale perspective. Funct Ecol 16:332–338CrossRefGoogle Scholar
  3. Agnarsson I (2006) A revision of the New World eximius lineage of Anelosimus (Araneae, Theridiidae) and a phylogenetic analysis using worldwide exemplars. Zool. J Linn Soc 146:453–493CrossRefGoogle Scholar
  4. Aviles L (1997) Causes and consequences of cooperation and permanent sociality in spiders. In: Choe JC, Crespi B (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 476–498CrossRefGoogle Scholar
  5. Aviles L, Agnarsson I, Salazar PA, Purcell J et al (2007) Altitudinal patterns of spider sociality and the biology of a new midelevation social Anelosimus speices in Ecuador. Am Nat 170:783–792CrossRefPubMedGoogle Scholar
  6. Bergmann C (1847) About the relationships between heat conservation and body size of animals. Goettinger Studien 3:595–708Google Scholar
  7. Bradshaw WE, Holzapfel CM (2007) Evolution of animal photoperiodism. Annu Rev Ecol Evol Syst 38:1–25CrossRefGoogle Scholar
  8. Chandler L (1975) Eusociality in Ceratina calcarata Robertson. Proc Indiana Acad Sci 84:283–284Google Scholar
  9. Conover DO, Duffy TA, Hice LA (2009) The covariance between genetic and environmental influences across ecological gradients. reassessing the evolutionary significance of countergradient and cogradient variation. Ann NY Acad Sci 1168:100–129CrossRefPubMedGoogle Scholar
  10. Corbet PS (2003) A positive correlation between photoperiod and development rate in summer species of Odonata could help to make emergence date appropriate to latitude: a testable hypothesis. J Entomol Soc B Columbia 100:3–17Google Scholar
  11. Cronin AL, Schwarz MP (1999a) The lifecycle and social behaviour of Exoneura robusta (Hymenoptera: Apidae): habitat influences opportunities for sib rearing in a primitively social bee. Ann Entomol Soc Am 92:707–716CrossRefGoogle Scholar
  12. Cronin AL, Schwarz MP (1999b) Latitudinal variation in the social behaviour of allodapine bees (Hymenoptera: Apidae). Can J Zool 77:857–864CrossRefGoogle Scholar
  13. Cronin AL (2001) Social flexibility in a primitively social allodapine bee (Hymenoptera; Apidae): results of a translocation experiment. Oikos 94:337–343CrossRefGoogle Scholar
  14. Cronin AL, Hirata M (2003) Social polymorphism in the sweat bee Lasioglossum (Evylaeus) baleicum (Hymenoptera; Halictidae) in Hokkaido, northern Japan. Insect Soc 50:379–386CrossRefGoogle Scholar
  15. Danforth B, Eickwort C (1997) The evolution of social behavior in the augochlorine sweat bees (Hymenoptera: Halictidae) based on a phylogenetic analysis of the genera. In: Choe JC, Crespi B (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 270–292CrossRefGoogle Scholar
  16. Davison PJ, Field J (2017) Season length, body size and social polymorphism: size clines but not saw tooth clines in sweat bees. Ecol Entomol 42:768–776CrossRefGoogle Scholar
  17. Davison P, Field J (2018) Limited social plasticity in the socially polymorphic sweat bee Lasioglossum calceatum. Behav Ecol Sociobiol 72:56CrossRefPubMedPubMedCentralGoogle Scholar
  18. Eickwort GC, Eickwort JM, Gordon J, Eickwort MA, Wcislo WT (1996) Solitary behaviour in a high-altitude population of the social sweat bee Halictus rubicundus (Hymenoptera: Halictidae). Behav Ecol Sociobiol 38:227–233CrossRefGoogle Scholar
  19. Field J, Paxton RJ, Soro A, Bridge C (2010) Cryptic plasticity underlies a major evolutionary transition. Curr Biol 20:2028–2031CrossRefPubMedGoogle Scholar
  20. Gaston K, Blackburn T (1996) Range size-body size relationships: evidence of scale dependence. Oikos 75:479–485CrossRefGoogle Scholar
  21. Gaston K, Gauld I, Hanson P (1996) The size and composition of the hymenopteran fauna of Costa Rica. J Biogeor 23:105–113CrossRefGoogle Scholar
  22. Grothaus R (1962) The biology of the species of Ceratina (Hymenoptera, Xylocopidae) in Indiana. Masters thesis, Department of Biology, Purdue University, West Lafayette, Indiana, USAGoogle Scholar
  23. Gullan PJ, Cranston PS (2010) The insects: an outline of entomology, 4th edn. Wiley-Blackwell, HobokenGoogle Scholar
  24. Hirata M, Higashi S (2008) Degree-day accumulation controlling allopatric and sympatric variations in the sociality of sweat bees, Lasioglossum (Evylaeus) baleicum (Hymenoptera. Halictidae). Behav Ecol Sociobiol 62:1239–1247CrossRefGoogle Scholar
  25. Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity of ectotherm performance. Trends Ecol Evol 4:131–135CrossRefPubMedGoogle Scholar
  26. Hunt JH, Amdam GV (2005) Bivoltinism as an antecedent to eusociality in the paper wasp genus. Polistes Science 308:264–267PubMedGoogle Scholar
  27. Jeanne RI (1991) The swarm founding Polistinae. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, Ithaca, pp 191–231Google Scholar
  28. Johnson M (1988) The relationship of provision weight to adult weight and sex ratio in the solitary bee, Ceratina calcarata. Ecol Entomol 13:165–170CrossRefGoogle Scholar
  29. Kaspari M, Vargo E (1995) Colony size as a buffer against seasonality: Bergmann’s rule in social insects. Am Nat 145:610–632CrossRefGoogle Scholar
  30. Kaspari M, Ward PS, Yuan M (2004) Energy gradients and the geographic distribution of local ant diversity. Oecologia 140:407–413CrossRefPubMedGoogle Scholar
  31. Kim J, Thorp R (2001) Maternal investment and size-number trade-off in a bee, Megachile apicalis, in seasonal environments. Oecologia 126:451–456CrossRefPubMedGoogle Scholar
  32. Kislow C (1976) The comparative biology of two species of small carpenter bees, Ceratina strenua Smith F. and Ceratina calcarata Robertson. PhD thesis, Department of Biology, University of Georgia, Athens, Georgia, USAGoogle Scholar
  33. Knies JL, Kingsolver JG, Burch CL (2009) Hotter is better and broader: thermal sensitivity of fitness in a population of bacteriophages. Am Nat 173:419–430CrossRefPubMedGoogle Scholar
  34. Lawson SP, Ciaccio KN, Rehan SM (2016) Maternal manipulation of pollen provisions affects worker production in a small carpenter bee. Behav Ecol Sociobiol 70:1891CrossRefGoogle Scholar
  35. Masaki S (1972) Climatic adaptation and photoperiodic response in the band-legged ground cricket. Evol 26:587–600CrossRefGoogle Scholar
  36. Michener C (1985) From solitary to eusocial: need there be a series of intervening species? Fortschritte der Zoologie 31:293–305Google Scholar
  37. Mikat M, Franchino C, Rehan SM (2017) Sociodemographic variation in foraging behavior and the adaptive significance of worker production in the facultatively social small carpenter bee, Ceratina calcarata. Behav Ecol Sociobiol 71:135CrossRefGoogle Scholar
  38. Minckley R, Wcislo WT, Yanega D et al (1994) Behavior and phenology of a specialist bee (Dieunomia) and sunflower (Helianthus) pollen availability. Ecology 75:1406–1419CrossRefGoogle Scholar
  39. Mousseau TA, Roff DA (1989) Adaptation to seasonality in a cricket: patterns of phenotypic and genotypic variation in body size and diapause expression along a cline in season length. Evol 43:1483–1496CrossRefGoogle Scholar
  40. Mueller UG (1996) Life history and social evolution of the primitively eusocial bee Augochlorella striata (Hymenoptera: Halictidae). J Kans Entomol Soc 69:116–138Google Scholar
  41. Nygren GH, Bergstrom A, Soren N (2008) Latitudinal body size clines in the butterfly Polyommatus icarus are shaped by gene-environment interactions. J Insect Sci 8:47CrossRefPubMedCentralGoogle Scholar
  42. Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, PrincetonGoogle Scholar
  43. Packer L (1990) Solitary and eusocial nests in a population of Augochlorella striata (Provancher) (Hymenoptera; Halictidae) at the northern edge of its range. Behav Ecol Sociobiol 27:339–344CrossRefGoogle Scholar
  44. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefPubMedGoogle Scholar
  45. Peterson J, Roitberg B (2006) Impact of resource levels on sex ratio and resource allocation in the solitary bee, Megachile rotundata. Environ Entomol 35:1404–1410CrossRefGoogle Scholar
  46. Plateaux-Quénu C (2008) Subsociality in halictine bees. Insect Soc 55:335–346CrossRefGoogle Scholar
  47. Porter EE, Hawkins BA (2001) Latitudinal gradients in colony size for social insects: termites and ants show different patterns. Am Nat 157:97–106CrossRefPubMedGoogle Scholar
  48. Purcell J (2011) Geographic patterns in the distribution of social systems in terrestrial arthropods. Biol Rev Camb Philos Soc 86:475–491CrossRefPubMedGoogle Scholar
  49. Rau P (1928) The nesting habits of the little carpenter-bee, Ceratina calcarata. Ann Entomol Soc Am 21:380–396CrossRefGoogle Scholar
  50. Rehan SM, Richards M (2010a) Nesting biology and subsociality in Ceratina calcarata (Hymenoptera: Apidae). Can Entomol 142:65–74CrossRefGoogle Scholar
  51. Rehan SM, Richards M (2010b) The influence of maternal quality on brood sex allocation in the small carpenter bee, Ceratina calcarata. Ethology 116:876–887Google Scholar
  52. Rehan SM, Richards M (2013) Reproductive aggression and nestmate recognition in a subsocial bee. Anim Behav 85:733–741CrossRefGoogle Scholar
  53. Rehan SM, Toth AL (2015) Climbing the social ladder: molecular evo-lution of sociality. Trends Ecol Evol 30:426–433CrossRefPubMedGoogle Scholar
  54. Rehan SM, Berens AJ, Toth AL (2014) At the brink of eusociality: transcriptomic correlates of worker behaviour in a small carpenter bee. BMC Evol Biol 14:260CrossRefPubMedPubMedCentralGoogle Scholar
  55. Riechert S, Jones T (2008) Phenotypic variation in the social behaviour of the spider Anelosimus studiosus along a latitudinal gradient. Anim Behav 75:1893–1902CrossRefGoogle Scholar
  56. Roff DA (1980) Optimizing development time in a seasonal environment—the ups and downs of clinal variation. Oecologia 45:202–208CrossRefPubMedGoogle Scholar
  57. Roff DA (1992) The evolution of life histories: theory and analysis. Chapman and Hall, LondonGoogle Scholar
  58. Sakagami SF, Munakata M (1972) Distribution and bionomics of a transpalaearctic eusocial halictine bee, Lasioglossum (Evylaeus) calceatum in northern Japan with notes on its solitary life cycle at high altitude. J Fac Sci Hokkaido Univ Ser VI Zool 18:411–439Google Scholar
  59. Sakagami S, Maeta Y (1977) Some presumably presocial habits of Japanese Ceratina bees, with notes on various social types in Hymenoptera. Insect Soc 24:319–343CrossRefGoogle Scholar
  60. Sakagami SF, Maeta Y (1984) Multifemale nests and rudimentary castes in the normally solitary bee Ceratina japonica (Hymenoptera: Xylocopinae). J Kans Entomol Soc 57:639–656Google Scholar
  61. Sakagami SF, Maeta Y (1989) Compatibility and incompatibility of solitary life with eusociality in two normally solitary bees Ceratina japonica and Ceratina okinawana (Hymenoptera, Apoidea), with notes on the incipient phase of eusociality. Jpn J Entomol 57:417–439Google Scholar
  62. Sakagami S, Maeta Y (1995) Task allocation in artificially induced colonies of a basically solitary bee Ceratina (Ceratinidia) okinawana, with a comparison of sociality between Ceratina and Xylocopa (Hymenoptera, Anthophoridae, Xylocopinae). Jpn J Ecology 63:115–150Google Scholar
  63. Schulte PM, Healy TM, Fangue NA (2011) Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr Comp Biol 51:691–702CrossRefPubMedGoogle Scholar
  64. Schwarz MP, Silberbauer LX, Hurst PS (1997) Intrinsic and extrinsic factors associated with social evolution in allodapine bees. In: Choe JC, Crespi B (eds) The Evolution of Social Behaviour in Insects and Arachnids. Cambridge University Press, Cambridge, pp 476–498Google Scholar
  65. Shell WA, Rehan SR (2017) The price of insurance: costs and benefits of worker production in a facultatively social bee. Behav Ecol.  https://doi.org/10.1093/beheco/arx146 CrossRefGoogle Scholar
  66. Skandalis D, Richards MH, Sformo TS et al (2011) Climate limitations on the distribution and phenology of a large carpenter bee, Xylocopa virginica (Hymenoptera: Apidae). Can J Zool 89:785–795CrossRefGoogle Scholar
  67. Sniegula S, Richards MH, Sformo TS et al (2011) Differentiation in developmental rate across geographic regions: a photoperiod driven latitude compensating mechanism? Oikos 121:1073–1082CrossRefGoogle Scholar
  68. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 4th edn. W. H. Freeman and Co, New YorkGoogle Scholar
  69. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  70. Tauber JM, Tauber CA, Masaki S (1986) Seasonal adaptation of insects. Oxford University Press, OxfordGoogle Scholar
  71. Wcislo W (1997) Behavioural environments of sweat bees (Halictidae) in relation to variability in social organization. In: Choe JC, Crespi B (eds) The evolution of social behavior. Cambridge University Press, Cambridge, pp 316–332Google Scholar
  72. Williams CM, Szejner-Sigal A, Morgan TJ et al (2016) Adaptation to low temperature exposure increases metabolic rates independently of growth rates. Integr Comp Biol 56:62–72CrossRefPubMedPubMedCentralGoogle Scholar
  73. Wilson EO (1975) Sociobiology. Belknap, CambridgeGoogle Scholar
  74. Wohlschlag DE (1960) Metabolism of an Antarctic fish and the phenomenon of cold adaptation. Ecology 41:287–292CrossRefGoogle Scholar
  75. Välimäki P, Kivela SM, Maenpaa MI et al (2013) Latitudinal clines in alternative life histories in a geometrid moth. J Evol Biol 26:118–129CrossRefPubMedGoogle Scholar
  76. Vickruck J (2010) The nesting biology of Ceratina (Hymenoptera: Apidae) in the Niagara region: new species, nest site selection and parasitism. Masters thesis, Department of Biology, Brock University, St. Catharines, Ontario, CanadaGoogle Scholar
  77. Vickruck J, Richards MH (2012) Niche partitioning based on nest site selection in the small carpenter bees Ceratina mikmaqi and C. calcarata. Anim Behav 83:1083–1089CrossRefGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of New HampshireDurhamUSA

Personalised recommendations