Abstract
Many species exhibit distinct phenotypic classes, such as sexes in dioecious species or castes in social species. The evolution of these classes is affected by the genetic architecture governing traits shared between phenotypes. However, estimates of the genetic and environmental factors contributing to phenotypic variation in distinct classes have rarely been examined. We studied the genetic architecture underlying morphological traits in phenotypic classes in the social wasp Vespula maculifrons. Our data revealed patriline effects on a few traits, indicating weak genetic influences on caste phenotypic variation. Interestingly, traits exhibited higher heritability in queens than workers. This result suggests that genetic variation has a stronger influence on trait variation in the queen caste than the worker caste, which is unexpected because queens typically experience direct selection. Moreover, estimates of heritability for traits were correlated between the castes, indicating that variability in trait size was governed by similar genetic architecture in the two castes. However, we failed to find evidence for a significant relationship between caste dimorphism and caste correlation, as would be expected if trait evolution was constrained by intralocus genetic conflict. Our analyses also uncovered variation in the allometric relationships for traits. These analyses suggested that worker traits were proportionally smaller than queen traits for most traits examined. Overall, our data provide evidence for a strong environmental and moderate genetic basis of trait variation among castes. Moreover, our results suggest that selection previously operated on caste phenotype in this species, and phenotypic variation is now governed primarily by environmental differences.
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Data has been deposited with DRYAD: https://datadryad.org/stash/share/-6vbC_EUConsGh4vWYs_oJBdgU19vizbsaXB087aFa4.
References
Alattal Y, Al-Ghamdi A, Alsharhi DRM, Fuchs S (2014) Morphometric characterisation of the native Honeybee, Apis mellifera Linnaeus, 1758, of Saudi Arabia. Zool Middle East 60:226–235
Amin MR, Bussière LF, Goulson D (2012) Effects of Male age and Size on Mating Success in the Bumblebee Bombus terrestris. J Insect Behav 25:362–374
Bargum K, Boomsma JJ, Sundström L (2004) A genetic component to size in queens of the ant, Formica truncorum. Behav Ecol Sociobiol 57:9–16
Beekman M, Oldroyd BP (2019) Conflict and major transitions — why we need true queens. Curr Opin Insect Sci 34:73–79
Boomsma JJ, Ratnieks FLW (1997) Paternity in eusocial Hymenoptera. Philos Trans R Soc Lond B Biol Sci 351:947–975
Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2010) A basic introduction to fixed-effect and random-effects models for meta-analysis. Res Synth Methods 1:97–111
Brown JH, West GB (2000) Scaling in Biology. Oxford University Press, New York, USA
Burrows M, Sutton GP (2008) The effect of leg length on jumping performance of short- and long-legged leafhopper insects. J Exp Biol 211:1317–1325
Constant N, Santorelli LA, Lopes JFS, Hughes WOH (2012) The effects of genotype, caste, and age on foraging performance in leaf-cutting ants. Behav Ecol 23:1284–1288
Cox RM, Calsbeek R (2009) Sexually antagonistic selection, sexual dimorphism, and the resolution of intralocus sexual conflict. Am Nat 173:176–187
Daly D, Archer ME, Watts PC, Speed MP, Hughes MR, Barker FS et al. (2002) Polymorphic microsatellite loci for eusocial wasps (Hymenoptera: Vespidae). Mol Ecol Notes 2:273–275
Dussutour A, Simpson SJ (2008) Carbohydrate regulation in relation to colony growth in ants. J Exp Biol 211:2224–2232
Dyson CJ, Crossley HG, Ray CH, Goodisman MAD (2022) Social structure of perennial Vespula squamosa wasp colonies. Ecol Evol 12:e8569
Dyson CJ, Piscano OL, Durham RM, Thompson VJ, Johnson CH, Goodisman MAD (2021) Temporal Analysis of Effective Population Size and Mating System in a Social Wasp. J Hered 112:626–634
Elvin CM, Carr AG, Huson MG, Maxwell JM, Pearson RD, Vuocolo T et al. (2005) Synthesis and properties of crosslinked recombinant pro-resilin. Nature 437:999–1002
Fairbairn DJ (1997) Allometry for Sexual Size Dimorphism: Pattern and Process in the Coevolution of Body Size in Males and Females. Annu Rev Ecol Syst 28:659–687
Feinerman O, Traniello JFA (2016) Social complexity, diet, and brain evolution: modeling the effects of colony size, worker size, brain size, and foraging behavior on colony fitness in ants. Behav Ecol Sociobiol 70:1063–1074
Fjerdingstad EJ (2005) Control of body size of Lasius niger ant sexuals — worker interests, genes and environment. Mol Ecol 14:3123–3132
Fjerdingstad EJ, Crozier RH (2006) The Evolution of Worker Caste Diversity in Social Insects. Am Nat 167:390–400
Foster KR, Ratnieks FL (2001) Paternity, reproduction and conflict in vespine wasps: a model system for testing kin selection predictions. Behav Ecol Sociobiol 50:1–8
Foster KR, Ratnieks FLW, Gyllenstrand N, Thorén PA (2001) Colony kin structure and male production in Dolichovespula wasps. Mol Ecol 10:1003–1010
Frumhoff PC, Ward PS (1992) Individual-Level Selection, Colony-Level Selection, and the Association between Polygyny and Worker Monomorphism in Ants. Am Nat 139:559–590
Glazier DS (2021) Biological scaling analyses are more than statistical line fitting. J Exp Biol 224:241059
Goodisman MAD, Kovacs JL, Hoffman EA (2007a) Lack of conflict during queen production in the social wasp Vespula maculifrons. Mol Ecol 16:2589–2595
Goodisman MAD, Kovacs JL, Hoffman EA (2007b) The Significance of Multiple Mating in the Social Wasp Vespula maculifrons. Evolution 61:2260–2267
Hadfield JD (2010) MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package. Journal of Statistical Software 33:1–22
Hall DW, Goodisman MAD (2012) The Effects of Kin Selection on Rates of Molecular Evolution in Social Insects. Evolution 66:2080–2093
Hallgrímsson B, Katz DC, Aponte JD, Larson JR, Devine J, Gonzalez PN et al. (2019) Integration and the Developmental Genetics of Allometry. Integr Comp Biol 59:1369–1381
Hasegawa E, Takahashi J (2002) Microsatellite loci for genetic research in the hornet Vespa mandarinia and related species. Mol Ecol Notes 2:306–308
Hoffman EA, Kovacs JL, Goodisman MA (2008) Genetic structure and breeding system in a social wasp and its social parasite. BMC Evol Biol 8:239
Holman L (2014) Caste load and the evolution of reproductive skew. Am Nat 183:84–95
Holman L, Linksvayer TA, d’Ettorre P (2013) Genetic constraints on dishonesty and caste dimorphism in an ant. Am Nat 181:161–170
Hopkins BR, Kopp A (2021) Evolution of sexual development and sexual dimorphism in insects. Curr Opin Genet Dev 69:129–139
Jeanson R, Weidenmüller A (2014) Interindividual variability in social insects – proximate causes and ultimate consequences. Biol Rev 89:671–687
Kelemen EP, Skyrm K, Dornhaus A (2022) Selection on size variation: more variation in bumble bee workers and in the wild. Insectes Sociaux 69:93–98
Kingsolver JG, Pfennig DW (2004) Individual‐Level Selection as a Cause of Cope’s Rule of Phyletic Size Increase. Evolution 58:1608–1612
Koffler S, de Matos Peixoto Kleinert A, Jaffé R (2017) Quantitative conservation genetics of wild and managed bees. Conserv Genet 18:689–700
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 41:1612–1620
Kovacs JL, Hoffman EA, Goodisman MAD (2008) Mating Success in the Polyandrous Social Wasp Vespula maculifrons. Ethology 114:340–350
Kovacs JL, Hoffman EA, Marriner SM, Goodisman MAD (2010a) Detecting selection on morphological traits in social insect castes: the case of the social wasp Vespula maculifrons. Biol J Linn Soc 101:93–102
Kovacs JL, Hoffman EA, Marriner SM, Rekau JA, Goodisman MAD (2010b) Environmental and genetic influences on queen and worker body size in the social wasp Vespula maculifrons. Insectes Sociaux 57:53–65
Laciny A, Nemeschkal HL, Zettel H, Metscher B, Druzhinina IS (2019) Caste-specific morphological modularity in the ant tribe Camponotini (Hymenoptera, Formicidae). BMC Zool 4:9
Leimar O, Hartfelder K, Laubichler MD, Page Jr RE (2012) Development and evolution of caste dimorphism in honeybees – a modeling approach. Ecol Evol 2:3098–3109
Lester PJ, Beggs JR (2019) Invasion Success and Management Strategies for Social Vespula Wasps. Annu Rev Entomol 64:51–71
Linksvayer TA, Wade MJ (2005) The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: maternal effects, sib-social effects, and heterochrony. Q Rev Biol 80:317–336
Linksvayer TA, Wade MJ (2009) Genes with Social Effects Are Expected to Harbor More Sequence Variation Within and Between Species. Evolution 63:1685–1696
MacDonald JF, Matthews RW (1981) Nesting Biology of the Eastern Yellowjacket, Vespula maculifrons (Hymenoptera: Vespidae). J Kans Entomol Soc 54:433–457
Mank JE (2017) Population genetics of sexual conflict in the genomic era. Nat Rev Genet 18:721–730
McCoy MW, Bolker BM, Osenberg CW, Miner BG, Vonesh JR (2006) Size correction: comparing morphological traits among populations and environments. Oecologia 148:547–554
Miller SE, Sheehan MJ (2021) Ecogeographical patterns of body size differ among North American paper wasp species. Insectes Sociaux 68:109–122
Molet M, Wheeler DE, Peeters C (2012) Evolution of Novel Mosaic Castes in Ants: Modularity, Phenotypic Plasticity, and Colonial Buffering. Am Nat 180:328–341
Montagna TS, Antonialli-Junior WF (2016) Morphological Differences between Reproductive and Non-reproductive Females in the Social Wasp Mischocyttarus consimilis Zikán (Hymenoptera: Vespidae). Sociobiology 63:693–698
Mountcastle AM, Combes SA (2013) Wing flexibility enhances load-lifting capacity in bumblebees. Proc R Soc B Biol Sci 280:20130531
Mountcastle AM, Combes SA (2014) Biomechanical strategies for mitigating collision damage in insect wings: structural design versus embedded elastic materials. J Exp Biol 217:1108–1115
Nijhout HF, Wheeler DE (1996) Growth Models of Complex Allometries in Holometabolous Insects. Am Nat 148:40–56
Noirot C (1989) Social structure in termite societies. Ethol Ecol Evol 1:1–17
Ohyama L, Booher D, King J (2023) Ecological traits of social insects: Colony, queen and worker size relationships reveal a nexus trait with broad ecological relevance. Funct Ecol 37:2194–2206
Okada Y, Plateaux L, Peeters C (2013) Morphological variability of intercastes in the ant Temnothorax nylanderi: pattern of trait expression and modularity. Insectes Sociaux 60:319–328
Orr SE, Hedrick NA, Murray KA, Pasupuleti AK, Goodisman MAD (2024) Novel insights into paternity skew in a polyandrous social wasp. Insect Sci. https://doi.org/10.1111/1744-7917.13343. Online ahead of print
Oster GF, Wilson EO (1978) Caste and Ecology in the Social Insects. Princeton University Press. Princeton, NJ, USA.
Pauw A, Kahnt B, Kuhlmann M, Michez D, Montgomery GA, Murray E et al. (2017) Long-legged bees make adaptive leaps: linking adaptation to coevolution in a plant–pollinator network. Proc R Soc B Biol Sci 284:20171707
Pélabon C, Firmat C, Bolstad GH, Voje KL, Houle D, Cassara J et al. (2014) Evolution of morphological allometry. Ann N Y Acad Sci 1320:58–75
Pennell TM, Holman L, Morrow EH, Field J (2018) Building a new research framework for social evolution: intralocus caste antagonism. Biol Rev Camb Philos Soc 93:1251–1268
Pennell TM, Morrow EH (2013) Two sexes, one genome: the evolutionary dynamics of intralocus sexual conflict. Ecol Evol 3:1819–1834
Perez R, Aron S (2020) Adaptations to thermal stress in social insects: recent advances and future directions. Biol Rev 95:1535–1553
Perrard A, Villemant C, Carpenter JM, Baylac M (2012) Differences in caste dimorphism among three hornet species (Hymenoptera: Vespidae): forewing size, shape and allometry. J Evol Biol 25:1389–1398
Radloff SE, Hepburn HR, Hepburn C, Fuchs S, Otis GW, Sein MM et al. (2005) Multivariate morphometric analysis of Apis cerana of southern mainland Asia. Apidologie 36:127–139
Roisin Y (2000) Diversity and Evolution of Caste Patterns. In: Abe T, Bignell DE, Higashi M (eds) Termites: Evolution, Sociality, Symbioses, Ecology. Springer Netherlands, Dordrecht, pp 95–119
Sandoval-Arango S, Cárdenas Henao H, Montoya-Lerma J (2020) Divergence in Bergmann’s clines: elevational variation and heritability of body size in a leaf-cutting ant. Insectes Sociaux 67:355–366
Shingleton AW, Frankino WA, Flatt T, Nijhout HF, Emlen Douglas J (2007) Size and shape: the developmental regulation of static allometry in insects. BioEssays 29:536–548
Shingleton AW, Vea IM (2023) Sex-specific regulation of development, growth and metabolism. Semin Cell Dev Biol 138:117–127
Skaldina O, Sorvari J (2020) Phenotypic diversity in red wood ants (Hymenoptera: Formicidae): Is kinship involved? EJE 117:27–33
Smith CR (2023) Sexual dimorphism as a facilitator of worker caste evolution in ants. Ecol Evol 13:e9825
Smith CR, Suarez AV (2010) The Trophic Ecology of Castes in Harvester Ant Colonies. Funct Ecol 24:122–130
Sommer S, Wehner R (2012) Leg allometry in ants: Extreme long-leggedness in thermophilic species. Arthropod Struct Dev 41:71–77
Szathmáry E, Smith JM (1995) The major evolutionary transitions. Nature 374:227–232
Taylor D, Bentley MA, Sumner S (2018) Social wasps as models to study the major evolutionary transition to superorganismality. Curr Opin Insect Sci 28:26–32
Taylor BA, Reuter M, Sumner S (2019) Patterns of reproductive differentiation and reproductive plasticity in the major evolutionary transition to superorganismality. Curr Opin Insect Sci 34:40–47
Teder T, Kaasik A, Taits K, Tammaru T (2021) Why do males emerge before females? Sexual size dimorphism drives sexual bimaturism in insects. Biol Rev 96:2461–2475
Toth AL, Sumner S, Jeanne RL (2016) Patterns of longevity across a sociality gradient in vespid wasps. Curr Opin Insect Sci 16:28–35
Treanore E, Derstine N, Amsalem E (2021) What Can Mechanisms Underlying Derived Traits Tell Us About the Evolution of Social Behavior? Ann Entomol Soc Am 114:547–561
Trible W, Kronauer DJC (2017) Caste development and evolution in ants: it’s all about size. J Exp Biol 220:53–62
Tschinkel W (2010) Back to basics: Sociometry and sociogenesis of ant societies (Hymenoptera: Formicidae). Myrmecol News 14:49–54
Wald A (1945) Sequential Tests of Statistical Hypotheses. Ann Math Stat 16:117–186
Walsh JT, Garnier S, Linksvayer TA (2020) Ant Collective Behavior Is Heritable and Shaped by Selection. Am Nat 196:541–554
Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10:506–513
West-Eberhard MJ (2003) Developmental Plasticity and Evolution. Oxford University Press. New York, USA.
Wheeler DE (1991) The Developmental Basis of Worker Caste Polymorphism in Ants. Am Nat 138:1218–1238
Wills BD, Powell S, Rivera MD, Suarez AV (2018) Correlates and Consequences of Worker Polymorphism in Ants. Annu Rev Entomol 63:575–598
Wilson EO (1953) The Origin and Evolution of Polymorphism in Ants. Q Rev Biol 28:136–156
Wilson EO (1971) The insect societies. Harvard University Press. Cambridge, Massachusetts, USA.
Wilson EO, Hölldobler B (2005) Eusociality: Origin and consequences. Proc Natl Acad Sci 102:13367–13371
Winston ME, Thompson A, Trujillo G, Burchill AT, Moreau CS (2017) Novel approach to heritability detection suggests robustness to paternal genotype in a complex morphological trait. Ecol Evol 7:4179–4191
Wolak M (2012) Nadiv: An R package to create relatedness matrices for estimating non-additive genetic variances in animal models. Methods Ecol Evol 3:792–796
Wright CM, Lichtenstein JLL, Tibbetts EA, Pruitt JN (2019) Individual variation in queen morphology and behavior predicts colony performance in the wild. Behav Ecol Sociobiol 73:122
Wyman MJ, Stinchcombe JR, Rowe L (2013) A multivariate view of the evolution of sexual dimorphism. J Evol Biol 26:2070–2080
Yang C-H, Andrew Pospisilik J (2019) Polyphenism – A Window Into Gene-Environment Interactions and Phenotypic Plasticity. Front Genet 10:132
Yoon KJ, Cunningham CB, Bretman A, Duncan EJ (2023) One genome, multiple phenotypes: decoding the evolution and mechanisms of environmentally induced developmental plasticity in insects. Biochem Soc Trans 51:675–689
Yoshimura H, Yamada YY (2018) 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
Acknowledgements
Research funding provided by NSF-DEB: 2105033 and NSF-IOS: 2019799 to M.A.D.G. and USDA: 2023-67012-39886 to S.E.O. We would like to thank Paige Caine and Andrew Robertson for their assistance with collecting the wasp colonies.
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SEO and MADG conceived the work and designed the research; SEO, NAH, KAM, AKP performed the research and collected the data; SEO and JLK analyzed the data with support from MADG; SEO wrote the manuscript with support from MADG.
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Orr, S.E., Hedrick, N.A., Murray, K.A. et al. Genetic and environmental effects on morphological traits of social phenotypes in wasps. Heredity (2024). https://doi.org/10.1038/s41437-024-00701-5
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DOI: https://doi.org/10.1038/s41437-024-00701-5