Abstract
One of the major goals in evolutionary developmental biology is to understand the relationship between gene regulatory networks and the diverse morphologies and their functionalities. Are the diversities solely triggered by random events, or are they inevitable outcomes of an interplay between evolving gene networks and natural selection? Segmentation in arthropod embryogenesis represents a well-known example of body plan diversity. Striped patterns of gene expression that lead to the future body segments appear simultaneously or sequentially in long and short germ-band development, respectively. Moreover, a combination of both is found in intermediate germ-band development. Regulatory genes relevant for stripe formation are evolutionarily conserved among arthropods, therefore the differences in the observed traits are thought to have originated from how the genes are wired. To reveal the basic differences in the network structure, we have numerically evolved hundreds of gene regulatory networks that produce striped patterns of gene expression. By analyzing the topologies of the generated networks, we show that the characteristics of stripe formation in long and short germ-band development are determined by Feed-Forward Loops (FFLs) and negative Feed-Back Loops (FBLs) respectively, and those of intermediate germ-band development are determined by the interconnections between FFL and negative FBL. Network architectures, gene expression patterns and knockout responses exhibited by the artificially evolved networks agree with those reported in the fly Drosophila melanogaster and the beetle Tribolium castaneum. For other arthropod species, principal network architectures that remain largely unknown are predicted. Our results suggest that the emergence of the three modes of body segmentation in arthropods is an inherent property of the evolving networks.
Highlights
Evolutionary diversification of multi-cellular organisms largely depends on body plans, in which complex morphologies develop under the integrated control of multiple genes [1]
We have discovered that multiple Feed-Forward Loops (FFLs) (Fig. 2A) are always included in the core networks in the long germ modes while at least one negative Feed-Back Loops (FBLs) (Fig. 2B) is always included in the short germ mode
These results suggest that parallel connection of FFL and negative FBL organizes the combinatorial stripe formation
Summary
Evolutionary diversification of multi-cellular organisms largely depends on body plans, in which complex morphologies develop under the integrated control of multiple genes [1]. A fundamental key to understanding evolutionary developmental biology is to elucidate how a gene network determines body plan, its diversity, and its potential to evolve [2,3,4,5,6]. Arthropod segmentation exhibits three developmental modes of the stripe pattern formation in gene expression that specify the future elementary segments of an adult body [7,8]. Many of the descendant arthropod species (Fig. 1A; e.g., the fly Drosophila melanogaster [9]) follow the ‘long germ-band’ mode of development where stripes appear simultaneously along the anterior-posterior axis. Ancestral species (Fig. 1B; e.g., the beetle Tribolium castaneum [10] and the spider Cupiennius salei [11]) exhibit ‘short germ-band’ mode where stripes appear sequentially. A combination of both is found in ‘intermediate germ-band’ mode; anterior stripes appear simultaneously while the remaining posterior stripes appear sequentially
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