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The role of maternal effects on offspring performance in familiar and novel environments

Abstract

Maternal effects are an important evolutionary force that may either facilitate adaptation to a new environment or buffer against unfavourable conditions. The degree of variation in traits expressed by siblings from different mothers is often sensitive to environmental conditions. This could generate a Maternal-by-Environment interaction (M × E) that inflates estimates of Genotype-by-Environment effects (G × E). We aimed to test for environment-specific maternal effects (M × E) using a paternal full-sib/half-sib breeding design in the seed beetle Callosobruchus maculatus, where we split and reared offspring from the same mother on two different bean host types—original and novel. Our quantitative genetic analysis indicated that maternal effects were very small on both host types for all the measured life-history traits. There was also little evidence that maternal oviposition preference for a particular host type predicted her offspring’s performance on that host. Further, additive genetic variance for most traits was relatively high on both hosts. While there was higher heritability for offspring reared in the novel host, there was no evidence for G × Es, and most cross-host genetic correlations were positive. This suggests that offspring from the same family ranked similarly for performance on both host types. Our results point to a genetic basis of host adaptation in the seed beetle, rather than maternal effects. Even so, we encourage researchers to test for potential M × Es because, due to a lack of testing, it remains unclear how often they arise.

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Fig. 1: Illustration of how maternal effects might differ between environments (host beans in our study).

Data availability

Data with accompanying R code are stored at OSF (link: https://osf.io/ft7eq/?view_only=0bab0a33bb4246adb64c919601a72757) and FigShare repository (link: https://figshare.com/s/7878e68e31590dce594d).

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Acknowledgements

We appreciate detailed comments by three anonymous referees that helped us to improve the manuscript. We thank Timothée Bonnet and Loeske E. B. Kruuk (RSB ANU) for very helpful discussions about phenotypic variation partitioning and Bayesian mixed-effect models. We are thankful to Carolina Dolan, Krish S. Sanghvi and Elroy Kwan Au (RSB ANU) for their help with the experiment. MV and PJCC were both supported by 6-month Endeavour fellowships from the Australian Government.

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MV, PJCC, MLH and MDJ conceived and designed the study; MV, PJCC, MIC and ZZ collected data; MV analyzed the data and drafted the manuscript; and PJCC, MIC, ZZ, MLH and MDJ revised it. All authors approved the final version of the manuscript.

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Correspondence to Milan Vrtílek.

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Vrtílek, M., Chuard, P.J.C., Iglesias-Carrasco, M. et al. The role of maternal effects on offspring performance in familiar and novel environments. Heredity (2021). https://doi.org/10.1038/s41437-021-00431-y

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