Abstract
The segmentation gene network in insects can produce equivalent phenotypic outputs despite differences in upstream regulatory inputs between species. We investigate the mechanistic basis of this phenomenon through a systems-level analysis of the gap gene network in the scuttle fly Megaselia abdita (Phoridae). It combines quantification of gene expression at high spatio-temporal resolution with systematic knock-downs by RNA interference (RNAi). Initiation and dynamics of gap gene expression differ markedly between M. abdita and Drosophila melanogaster, while the output of the system converges to equivalent patterns at the end of the blastoderm stage. Although the qualitative structure of the gap gene network is conserved, there are differences in the strength of regulatory interactions between species. We term such network rewiring 'quantitative system drift'. It provides a mechanistic explanation for the developmental hourglass model in the dipteran lineage. Quantitative system drift is likely to be a widespread mechanism for developmental evolution.
Highlights
An important question for evolutionary biology is how developmental processes can compensate for variable environmental, signalling, or regulatory inputs to create a constant phenotypic outcome (Waddington, 1942)
Sample size and resolution of this dataset are comparable to our previously published gap gene mRNA expression data for D. melanogaster (Table 1, Supplementary file 1) (Crombach et al, 2012a) and are much higher than those achieved for our quantitative dataset of gap gene expression in another non-model dipteran, the moth midge Clogmia albipunctata (Crombach et al, 2014)
We find that reduced levels of bcd in RNA interference (RNAi) embryos result in an increasingly anterior position of the hb boundary in M. abdita (Figure 4), suggesting that the placement of gap domains is dependent on Bcd levels as in D. melanogaster
Summary
An important question for evolutionary biology is how developmental processes can compensate for variable environmental, signalling, or regulatory inputs to create a constant phenotypic outcome (Waddington, 1942). The segmentation gene network produces very robust and conserved output patterns despite fast-evolving upstream inputs through maternal gradients and vastly different modes of segmentation dynamics in different insect taxa (Sander, 1976; Davis and Patel, 2002). This type of neutral network evolution—producing the same output based on different regulatory principles—is called developmental system drift or phenogenetic drift (Weiss and Fullerton, 2000; True and Haag, 2001; Weiss, 2005; Haag, 2007; Pavlicev and Wagner, 2012). Genotype networks consist of different regulatory network structures— connected by simple mutational steps—that produce the same patterning or phenotypic output (Ciliberti et al, 2007a, 2007b; Wagner and Lynch, 2008; Draghi et al, 2010; Wagner, 2011)
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