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Genetic and environmental effects on morphological traits of social phenotypes in wasps

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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Fig. 1: The Eastern Yellowjacket Wasp, Vespula maculifrons, and morphological variability among queen and worker castes.
Fig. 2: Principle component analysis reveals new morphological variables.
Fig. 3: Scaling relationships in queen and worker V. maculifrons castes.
Fig. 4: Heritability for 14 morphological traits in queen and worker V. maculifrons.
Fig. 5: The across colony caste correlation for V. maculifrons traits.
Fig. 6: Weak relationships between caste correlations and caste dimorphism reveal a lack of evolutionary conflict.

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Data availability

Data has been deposited with DRYAD: https://datadryad.org/stash/share/-6vbC_EUConsGh4vWYs_oJBdgU19vizbsaXB087aFa4.

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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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Correspondence to Michael A. D. Goodisman.

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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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