Maternal Co-ordinate Gene Regulation and Axis Polarity in the Scuttle Fly Megaselia abdita

Abstract

Axis specification and segment determination in dipteran insects are an excellent model system for comparative analyses of gene network evolution. Antero-posterior polarity of the embryo is established through systems of maternal morphogen gradients. In Drosophila melanogaster, the anterior system acts through opposing gradients of Bicoid (Bcd) and Caudal (Cad), while the posterior system involves Nanos (Nos) and Hunchback (Hb) protein. These systems act redundantly. Both Bcd and Hb need to be eliminated to cause a complete loss of polarity resulting in mirror-duplicated abdomens, so-called bicaudal phenotypes. In contrast, knock-down of bcd alone is sufficient to induce double abdomens in non-drosophilid cyclorrhaphan dipterans such as the hoverfly Episyrphus balteatus or the scuttle fly Megaselia abdita. We investigate conserved and divergent aspects of axis specification in the cyclorrhaphan lineage through a detailed study of the establishment and regulatory effect of maternal gradients in M. abdita. Our results show that the function of the anterior maternal system is highly conserved in this species, despite the loss of maternal cad expression. In contrast, hb does not activate gap genes in this species. The absence of this activatory role provides a precise genetic explanation for the loss of polarity upon bcd knock-down in M. abdita, and suggests a general scenario in which the posterior maternal system is increasingly replaced by the anterior one during the evolution of the cyclorrhaphan dipteran lineage.

Gap gene regulatory dynamics evolve along a genotype network

“…This kind of compensatory evolution leads to system drift [5,[53][54][55][56]. It enables the gap gene networks of both species to produce equivalent patterning outputs despite differing maternal inputs [46,47].…”

“…Evidence from genetic, molecular, and data-driven modeling approaches have shown that it implements five basic regulatory principles (Figure 1B) [36]: (i) activation of gap genes by maternal gradients of Bicoid (Bcd) and Caudal (Cad), (ii) gap gene auto-activation, (iii) strong repression between mutually exclusive pairs hb/kni and Kr/gt, (iv) weak repression with posterior bias between overlapping gap genes causing domain shifts towards the anterior over time, and (v) repression by terminal gap genes tailless (tll) and huckebein (hkb) in the posterior pole region. In addition to evidence from D. melanogaster, gap gene expression and regulation has been studied in a range of non-drosophilid dipteran species [37][38][39][40][41][42][43][44][45][46][47][48][49]. This work indicates that the gap gene network is highly conserved within the cyclorrhaphan dipteran lineage of the higher flies ( Figure 1B).…”

“…In this report, we present a data-driven dynamical modeling approach to analyze and compare regulation of the trunk gap genes between D. melanogaster and the non-drosophilid scuttle fly Megaselia abdita, a member of the basally branching cyclorrhaphan family Phoridae ( Figure 1A, [46,47]). We chose M. abdita as our system of study because it is experimentally tractable [50] and features a conserved set of gap genes (and upstream regulators) identical to D. melanogaster [46].…”

“…Yet, it was also shown that the precise temporal and spatial dynamics of gene expression differ between them [46]. Specifically, in M. abdita, it is thought that a broadened Bcd gradient [39,47,51] and absence of maternal Cad [47,52] lead to gap domains appearing more posteriorly, and retracting from the pole later, than in D. melanogaster. Strikingly, however, the system compensates those differences to restore expression boundaries to comparable positions at the onset of gastrulation.…”

A damped oscillator imposes temporal order on posterior gap gene expression inDrosophila

“…In different species of dipteran insects, as well as in T. castaneum, travelling kinematic waves of gene expression are involved in segment determination [9,26,39,50,67]. Cad is always involved in the initial activation of these patterns [9,39,50,[79][80][81][82]. It also appears to control aspects of pair-rule gene regulation in centipedes [55,56].…”