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Abstract
Morphological consistency in metazoans is remarkable given the pervasive occurrence of genetic variation, environmental effects, and developmental noise. Developmental stability, the ability to reduce developmental noise, is a fundamental property of multicellular organisms, yet its genetic bases remains elusive. Imperfect bilateral symmetry, or fluctuating asymmetry, is commonly used to estimate developmental stability. We observed that Drosophila melanogaster overexpressing Cyclin G (CycG) exhibit wing asymmetry clearly detectable by sight. Quantification of wing size and shape using geometric morphometrics reveals that this asymmetry is a genuine—but extreme—fluctuating asymmetry. Overexpression of CycG indeed leads to a 40-fold increase of wing fluctuating asymmetry, which is an unprecedented effect, for any organ and in any animal model, either in wild populations or mutants. This asymmetry effect is not restricted to wings, since femur length is affected as well. Inactivating CycG by RNAi also induces fluctuating asymmetry but to a lesser extent. Investigating the cellular bases of the phenotypic effects of CycG deregulation, we found that misregulation of cell size is predominant in asymmetric flies. In particular, the tight negative correlation between cell size and cell number observed in wild-type flies is impaired when CycG is upregulated. Our results highlight the role of CycG in the control of developmental stability in D. melanogaster. Furthermore, they show that wing developmental stability is normally ensured via compensatory processes between cell growth and cell proliferation. We discuss the possible role of CycG as a hub in a genetic network that controls developmental stability.
Highlights
Precision of developmental processes is of great evolutionary importance since it conditions the accurate replication of the selected phenotype
fluctuating asymmetry (FA) of sd.RCG76 wings increased dramatically (6.8-fold for females and up to 47.9-fold for males) as compared to control +/+ siblings (Table S2). These results demonstrate that any Cyclin G (CycG) overexpression has a very strong effect on wing FA, the driver can affect the intensity of the asymmetry response. qRT-PCRs showed that CycG overexpression driven by Act was weaker than the one driven by da (Figure S3), suggesting that the strength of the FA effect depends on the level of CycG expression
The CycG gene of Drosophila melanogaster encodes a cyclin involved in transcriptional regulation, cell growth and cell cycle [21,22]
Summary
Precision of developmental processes is of great evolutionary importance since it conditions the accurate replication of the selected phenotype. Waddington was the first to suggest that the ability to buffer variation – referred to as developmental homeostasis – is a fundamental property of organisms [2]. Complex genetic networks can be intrinsically robust to perturbations [9], questioning the existence of specific robustness genes To accommodate these contradictory results, it was suggested that some genes of particular importance for robustness might exist as hubs in complex networks [10]. Whether these results apply to developmental stability is not known [11,12,13]
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