Evolution of the genetic control of segmentation in arthropods

Underlying the general similarity of arthropod segmentation are conserved gene expression patterns, which suggests that there may be a common regulatory program for segmentation among arthropods. For example, segmentation in all classes—insects, crustaceans, myriapods, and chelicerates—passes through a stage when the engrailed gene is expressed in a stripe in each segment (Fig. 5.1). In Drosophila, this segment polarity gene—a member of the last tier in the segmentation gene cascade—functions to establish and maintain compartmental and segmental boundaries. In addition, a number of other genes involved in Drosophila segmentation, including even-skipped, hairy, wingless, and mnt, are expressed in patterns that appear to be associated with segmentation in several insects, crustaceans, centipedes, and spiders. Thus, some of the members in the Drosophila segmentation cascade appear to be deployed among most arthropods during the segmentation process. However, a number of

Figure 5.1

Conservation of segmental engrailed expression in arthropods

All arthropods share a segmented body plan. (a) The phylogeny of major arthropod groups is shown with representative animals. (b) The engrailed segment polarity gene is expressed in segmentally iterated stripes during embryogenesis in different arthropods. This similarity indicates that segmental engrailed expression is a conserved stage in the development of all arthropods. Source: Part b from Patel NH. The evolution of arthropod segmentation: insights from comparisons of gene expression patterns. Development 1994(suppl): 201-207; Telford MJ, Thomas RH. Proc Natl Acad Sci USA 1998; 95: 10671-10675; Hughes CL, Kaufman, TC. Dev Biol 2002; 247: 47-61. Copyright (2002), reprinted with permission from Elsevier.

Figure 5.1

Conservation of segmental engrailed expression in arthropods

All arthropods share a segmented body plan. (a) The phylogeny of major arthropod groups is shown with representative animals. (b) The engrailed segment polarity gene is expressed in segmentally iterated stripes during embryogenesis in different arthropods. This similarity indicates that segmental engrailed expression is a conserved stage in the development of all arthropods. Source: Part b from Patel NH. The evolution of arthropod segmentation: insights from comparisons of gene expression patterns. Development 1994(suppl): 201-207; Telford MJ, Thomas RH. Proc Natl Acad Sci USA 1998; 95: 10671-10675; Hughes CL, Kaufman, TC. Dev Biol 2002; 247: 47-61. Copyright (2002), reprinted with permission from Elsevier.

striking differences are also apparent. These may be related to the differences in early embryonic development between arthropods. In Drosophila, segmentation depends on gradients of transcription factor activity in a syncytial embryo; in other arthropods, segmentation occurs over a longer period in a cellularized embryo.

Differences have evolved in earlier stages of segmentation in several distinct ways. First, genes have been independently recruited for a new role in, or potentially lost their role in, segmentation. Second, the regulatory interactions between members of the segmentation cascade have changed. Third, the evolution of new genes and gene functions has changed the architecture of the segmentation regulatory hierarchy. We will examine selected examples of each type of evolutionary change in arthropod segmentation regulation.

Some of the mechanisms that regulate Drosophila segmentation appear to be more the exception rather than the rule for arthropods or even insects. For example, in spiders, Notch pathway genes are expressed in the developing segments and are required for segmentation. However, Notch signaling is not involved in segment formation in Drosophila. Also, although even-skipped is expressed in a segmental pattern in all arthropods, the pair-rule function of the even-skipped gene appears to exist only in Drosophila and a few other insect lineages. Other segmental gene roles appear to be unique to Drosophila, or at least higher dipterans. For example, the Drosophila pair-rule gene ftz does not have a pair-rule function in other insect orders and arthropod classes, in fact, ftz likely has an ancestral role as a Hox gene (see Chapter 4). Thus, some members of the segmentation regulatory hierarchy have changed between different arthropods, in part through the recruitment of genes for new roles.

The evolution of regulatory interactions in segmentation is illustrated by the different means by which the hunchback gene is regulated in beetles and flies. In the beetle Tribolium, the hunchback gene has an expression domain similar to the gap expression domain of Drosophila hunchback, but the beetle ortholog is regulated differently. The Drosophila hunchback cis-regulatory element that directs expression in the gap domain is activated by the Bicoid protein, one of the pivotal regulators of anteroposterior patterning during Drosophila embryogenesis. The equivalent Tribolium hunchback cis-regulatory element is regulated by the Caudal protein. Thus, similar hunchback gap expression domains are governed by cis-regulatory elements that bind different upstream regulators in the beetle and the fruit fly. Homologs of bicoid have not been identified outside of higher Diptera, suggesting a recent origin for this gene. Two of the targets of Bicoid in Drosophila, orthodenticle and hunchback, appear to be sufficient to regulate anterior patterning in Tribolium and this likely reflects the ancestral mode of anterior patterning and segment formation in insects. Following the evolution of the bicoid gene in the lineage that gave rise to the higher dipterans, Bicoid must have acquired the ability to regulate the zygotic expression of orthodenticle and hunchback and thus assumed its role at the top of the anteroposterior patterning hierarchy.

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