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Genetic variation of morphological scaling in Drosophila melanogaster

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Abstract

Morphological scaling relationships between the sizes of individual traits and the body captures the characteristic shape of a species, and their evolution is the primary mechanism of morphological diversification. However, we have almost no knowledge of the genetic variation of scaling, which is critical if we are to understand how scaling evolves. Here we explore the genetics of population scaling relationships (scaling relationships fit to multiple genetically-distinct individuals in a population) by describing the distribution of individual scaling relationships (genotype-specific scaling relationships that are unseen or cryptic). These individual scaling relationships harbor the genetic variation in the developmental mechanisms that regulate trait growth relative to body growth, and theoretical studies suggest that their distribution dictates how the population scaling relationship will respond to selection. Using variation in nutrition to generate size variation within 197 isogenic lineages of Drosophila melanogaster, we reveal extensive variation in the slopes of the wing-body and leg-body individual scaling relationships among genotypes. This variation reflects variation in the nutritionally-induced size plasticity of the wing, leg, and body. Surprisingly, we find that variation in the slope of individual scaling relationships primarily results from variation in nutritionally-induced plasticity of body size, not leg or wing size. These data allow us to predict how different selection regimes affect scaling in Drosophila, and is the first step in identifying the genetic targets of such selection. More generally, our approach provides a framework for understanding the genetic variation of scaling, an important prerequisite to explaining how selection changes scaling and morphology.

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Fig. 1: Individual and population scaling relationships.
Fig. 2: The population scaling relationships of the wing and leg size against body size in Drosophila melanogaster.
Fig. 3: Distribution of individual scaling relationships among isogenic fly lineages.
Fig. 4: The relationship between mean relative wing and leg size and the slope of individual scaling relationships among isogenic fly lineages.
Fig. 5: Variation in slope among lineages reflects variation in wing-, leg- and body-size plasticity.

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Data availability

All data as well as the R scripts used to analyze them are provided on Dryad (https://doi.org/10.5061/dryad.98sf7m0nd).

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Acknowledgements

This work was made possible through the assistance of undergraduate members of the Shingleton and Frankino labs, who reared and measured the flies used in the study. Additional financial support was provided by the University of Illinois at Chicago. WAF was supported by NSF IOS-1558098. AWS was supported by NSF IOS-1952385.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Illinois Chicago, 840 W Taylor St, Chicago, IL, 60607, USA

    Austin S. Wilcox, Isabelle M. Vea & Alexander W. Shingleton

  2. Department of Biology and Biochemistry, University of Houston, Houston, TX, 77204, USA

    W. Anthony Frankino

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  1. Austin S. Wilcox
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  2. Isabelle M. Vea
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  3. W. Anthony Frankino
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  4. Alexander W. Shingleton
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Contributions

AWS and WAF designed and oversaw execution of the study; ASW and IMV oversaw the collection of the data; ASW, IMV, WAF and AWS contributed to the data analysis and in preparing the manuscript for publication.

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Correspondence to Alexander W. Shingleton.

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Wilcox, A.S., Vea, I.M., Frankino, W.A. et al. Genetic variation of morphological scaling in Drosophila melanogaster. Heredity 130, 302–311 (2023). https://doi.org/10.1038/s41437-023-00603-y

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