Comparative analysis of hox gene expression in the polychaete Chaetopterus: Implications for the evolution of body plan regionalization

American Zoologist, Jun 2001 by Irvine, Steven Q, Martindale, Mark Q

Changes in regulation of posterior expression boundaries: an avenue for evolutionary change?

From the foregoing, it is apparent that correlation of posterior Hox gene expression boundaries with morphological boundaries in various taxa is common. One observation that could be made is that posterior expression boundaries do not appear to be under a constraint comparable to the colinear constraint of anterior boundaries, and that the position of the posterior boundary can be independent of the relative segmental register of the anterior boundary. For example CH-Hoxl and CH-Hox2 share a posterior boundary even though their anterior boundaries are staggered, and this boundary is rostral to that of CH-Hox3. On the other hand, CH-Hox5 has a posterior expression boundary rostral to that of CH-Hox4, the opposite relationship in terms of colinearity (Fig. 2A). A similar opposition is found between the leech genes Lox20Hox5 and Lox5/Hox6 as versus Lox5/Hox6 and Lox2 and Lox4 (paralogy groups 7/8) (Fig. 2B). In the arthropods, as in annelids, posterior boundaries are free to "bunch up," as seen for the Anemia Hox6, 7, and 8 genes (Fig. 3C), and for the spider Hoxl-5 genes (Fig. 3D).

If posterior boundaries are under looser regulatory constraints than anterior boundaries they may be more available for evolutionary change. The effect of changes in posterior boundaries would be to change the Hox code, or combination of Hox genes acting in a segment or portion of a segment. Restriction of posterior boundaries of multiple Hox genes together, such as CH-Hoxl and CH-Hox2 in Chaetopterus and the Hoxl-5 genes in spiders could amount to a radical change in Hox code allowing a major transition in body plan morphology, like that from tagma A to tagma B in Chaetopterus or from prosoma to opisthosoma in spiders.

Patterns of Hox gene regulatory changes

Evidence of intermediate-scale regulatory changes, as compared to these more phylogenetically distant examples of differences in Hox gene expression patterns, have been found in arthropods. Averof and Patel (Averof and Patel, 1997) showed in comparisons of Ubx expression in crustaceans that the anterior boundary of this gene shifted posteriorly in species which had evolved differences in the morphology of thoracic appendages. In species, such as Anemia, with homonomous thoracic appendages,

Ubx has an anterior boundary of expression in the T I segment, a condition considered primitive for crustaceans with uniform trunk segments. In separately derived groups, however, with anterior thoracic swimming appendages recruited to aid in feeding (called maxillipeds) the Ubx expression boundary shifted from one to four segments posteriorly in correspondence to the morphological change.

A study of Scr expression in insects from five different orders (Rogers et al., 1997) demonstrated an expansion of late patterns of expression into lateral and ventral portions of the first thoracic segment in more derived groups. This expansion of the posterior expression boundaries was examined in detail and correlated with derived morphological structures of the prothorax as compared with the most primitive apterygote species.