Genetic variation for sexual dimorphism in developmental traits in <i>Drosophila melanogaster</i>

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Abstract

Sexual dimorphism in traits of insects during the developmental stages could potentially be the direct or indirect result of sex-specific selection provided that genetic variation for sexual dimorphism is present. We investigated genetic variation in sexual dimorphism in a set of Drosophila melanogaster inbred lines for 2 traits: egg to adult development time and pupation site preference. We observed considerable genetic variation in sexual dimorphism among lines in both traits. The sexual dimorphic patterns remained relatively consistent across multiple trials, despite both traits being sensitive to environmental conditions. Additionally, we measured 2 sexually dimorphic adult morphological traits in 6 sampled lines and investigated correlations in the sexual dimorphism patterns with the 2 developmental traits. The abundance of genetic variation in sexual dimorphism for D. melanogaster developmental traits demonstrated in this study provides evidence for a high degree of evolvability of sex differences in preadult traits in natural populations.

Most cited references 51

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Fitting Linear Mixed-Effects Models Usinglme4

Steve Walker, Martin Mächler, Ben Bolker … (2023)

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The Drosophila melanogaster Genetic Reference Panel

Trudy Mackay, Stephen J. Richards, Eric Stone … (2012)

A major challenge of biology is understanding the relationship between molecular genetic variation and variation in quantitative traits, including fitness. This relationship determines our ability to predict phenotypes from genotypes and to understand how evolutionary forces shape variation within and between species. Previous efforts to dissect the genotype-phenotype map were based on incomplete genotypic information. Here, we describe the Drosophila melanogaster Genetic Reference Panel (DGRP), a community resource for analysis of population genomics and quantitative traits. The DGRP consists of fully sequenced inbred lines derived from a natural population. Population genomic analyses reveal reduced polymorphism in centromeric autosomal regions and the X chromosome, evidence for positive and negative selection, and rapid evolution of the X chromosome. Many variants in novel genes, most at low frequency, are associated with quantitative traits and explain a large fraction of the phenotypic variance. The DGRP facilitates genotype-phenotype mapping using the power of Drosophila genetics.

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Comparing evolvability and variability of quantitative traits.

D. Houle (1992)

There are two distinct reasons for making comparisons of genetic variation for quantitative characters. The first is to compare evolvabilities, or ability to respond to selection, and the second is to make inferences about the forces that maintain genetic variability. Measures of variation that are standardized by the trait mean, such as the additive genetic coefficient of variation, are appropriate for both purposes. Variation has usually been compared as narrow sense heritabilities, but this is almost always an inappropriate comparative measure of evolvability and variability. Coefficients of variation were calculated from 842 estimates of trait means, variances and heritabilities in the literature. Traits closely related to fitness have higher additive genetic and nongenetic variability by the coefficient of variation criterion than characters under weak selection. This is the reverse of the accepted conclusion based on comparisons of heritability. The low heritability of fitness components is best explained by their high residual variation. The high additive genetic and residual variability of fitness traits might be explained by the great number of genetic and environmental events they are affected by, or by a lack of stabilizing selection to reduce their phenotypic variance. Over one-third of the quantitative genetics papers reviewed did not report trait means or variances. Researchers should always report these statistics, so that measures of variation appropriate to a variety of situations may be calculated.

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Author and article information

Contributors

Tianyu Li

Rebecca S Zhang:

ORCID: https://orcid.org/0009-0001-5194-2474

John R True:

ORCID: https://orcid.org/0000-0001-5124-5495

E Betran: Role: Editor

Journal

Journal ID (nlm-ta): G3 (Bethesda)

Journal ID (iso-abbrev): Genetics

Journal ID (publisher-id): g3journal

Title: G3: Genes|Genomes|Genetics

Publisher: Oxford University Press (US )

ISSN (Electronic): 2160-1836

Publication date Collection: April 2024

Publication date (Electronic): 01 March 2024

Publication date PMC-release: 01 March 2024

Volume: 14

Issue: 4

Electronic Location Identifier: jkae010

Affiliations

Department of Ecology and Evolution, Stony Brook University , Stony Brook, NY 11794, USA

Department of Biology, Massachusetts Institute of Technology , Cambridge, MA 02139, USA

Department of Ecology and Evolution, Stony Brook University , Stony Brook, NY 11794, USA

Author notes

Corresponding author: Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY 11794, USA. Email: john.true@ 123456stonybrook.edu

Conflicts of interest. The authors declare no conflict of interest.

Author information

Rebecca S Zhang https://orcid.org/0009-0001-5194-2474

John R True https://orcid.org/0000-0001-5124-5495

Article

Publisher ID: jkae010

DOI: 10.1093/g3journal/jkae010

PMC ID: 10989870

PubMed ID: 38427952

SO-VID: 6e331598-0c05-46a8-8f1e-5b8c8f177cff

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

History

Date received : 12 December 2023

Date accepted : 10 January 2024

Date: 01 March 2024

Page count

Pages: 9

Funding

Funded by: Stony Brook University, DOI 10.13039/100007259;

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Genetic variation for sexual dimorphism in developmental traits in Drosophila melanogaster

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