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Size of organs/organisms is a polygenic trait. Many of the growth‐regulatory genes constitute conserved growth signaling pathways. However, how these multiple genes are orchestrated at the systems level to attain the natural variation in size including sexual size dimorphism is mostly unknown. Here we take a multi‐layered systems omics approach to study size variation in the Drosophila wing. We show that expression levels of many critical growth regulators such as Wnt and TGFβ pathway components significantly differ between sexes but not between lines exhibiting size differences within each sex, suggesting a primary role of these regulators in sexual size dimorphism. Only a few growth genes including a receptor of steroid hormone ecdysone exhibit association with between‐line size differences. In contrast, we find that between‐line size variation is largely regulated by genes with a diverse range of cellular functions, most of which have never been implicated in growth. In addition, we show that expression quantitative trait loci (eQTLs) linked to these novel growth regulators accurately predict population‐wide, between‐line wing size variation. In summary, our study unveils differential gene regulatory systems that control wing size variation between and within sexes., The study investigates transcriptomic variation that reflects a natural genetic diversity in fly wings. Through a multi‐layered systems omics approach, regulatory systems that control two distinct aspects of wing size variation are determined.

Paxillin is a protein containing four LIM domains, and functions in integrin signaling. We report here that two transcripts are generated from the paxillin gene locus in Drosophila; one encodes a protein homolog of the vertebrate Paxillin (DPxn37), and the other a protein with only three LIM domains, partly encoded by its own specific exon (PDLP). At the myotendinous junctions of Drosophila embryos where integrins play important roles, both DPxn37 and PDLP are highly expressed with different patterns; DPxn37 is predominantly concentrated at the center of the junctions, whereas PDLP is highly enriched at neighboring sides of the junction centers, primarily expressed in the mesodermal myotubes. Northern blot analysis revealed that DPxn37 is ubiquitously expressed throughout the life cycle, whereas PDLP expression exhibits a biphasic pattern during development, largely concomitant with muscle generation and remodeling. Our results collectively reveal that a unique system exists in Drosophila for the generation of a novel type of LIM-only protein, highly expressed in the embryonic musculature, largely utilizing the Paxillin LIM domains.