Conserved developmental functions rebuilding the bilaterian ancestor from phylogenetic inference

Although the conservation of biochemical functionality may simply reflect evolutionary constraint on protein sequence evolution, similarities in the developmental function of homologous genes raise the possibility of deeper evolutionary significance. For example, how should we interpret the striking similarity in the developmental function of Hox genes in regulating regional identities along the A/P axis of both mice and Drosophila? One possibility is that this similarity is mere coincidence—that the transcription factors independently evolved roles in patterning the A/P axis of protostomes and deuterostomes. More interestingly, the Hox genes may have played a role in patterning the A/P axis of the last common ancestor of protostomes and deuterostomes—the hypothetical ancestor of all bilaterians, dubbed "Urbilateria."

One way to distinguish between the possibility that observed similarities are convergent and the likelihood that they reflect conservation of features in a common ancestor is to examine other phyla. The more taxa that share a characteristic, the less likely that the similarity is due to convergence. The deployment of Hox genes along the A/P axis of Amphioxus, annelids, flatworms, and other bilaterians, for example, suggests that Hox colinearity is an ancestral feature of bilaterians.

Not only may we infer the ancestral function of toolkit genes from shared developmental functions among living bilaterians, but we may also infer some of the morphological characteristics of Urbilateria. No fossils have been identified that provide direct knowledge about the morphological complexity of early bilaterian ancestors. Instead, we must use comparative developmental genetic data from living animals in our attempt to rebuild a picture of Urbilateria. The identification of conserved developmental regulatory genes, expressed in similar patterns or cell types among multiple phyla, implies that the same genes were utilized in a common ancestor to control pattern formation and cell differentiation; the open question concerns the complexity of the resulting structures in animal ancestors.

The logic that underlies inferences about the development and morphology of Urbilateria is illustrated by the conserved role of Pax6 genes in eye development. Both the mouse Pax6 gene and the Drosophila ortholog eyeless are at the top of the regulatory hierarchies that direct eye development in each organism. Other components of the Pax6-regulated circuit, including the sine oculis, eyes absent, and opsin genes, are also shared between flies and mice. Furthermore, Pax6 orthologs are expressed during eye development in many other bilaterian phyla and a related Pax gene (with a Pax6-like homeodomain) is expressed in the eyes of a cnidarian (Fig. 4.11), providing more evidence that the functional similarities

Developing eyes Figure 4.11

express Pax6 expression during eye development in --different bilaterian phyla

-Vertebrates Yes Pax6 protein expression has been characterized

Pax6 protein expression has been characterized in many bilaterian phyla. This protein is

Urbilateria: Pax6

-Cephalochordates Yes expressed in the eyes of vertebrates, urochordates, arthropods, annelids, molluscs, flatworms, and nemerteans (not shown). Thus the

Urochordates Yes common bilaterian ancestor may have deployed an ancestral Pax6 gene in photoreceptor cells during the development of a primitive "eye"or light-sensing organ.

expressed in a primitive

Echinoderms expressed in a primitive

-Arthropods Yes

Onychophora

Annelids

-Molluscs

-Flatworms

Lophophorates

(Related Pax gene Cnidaria expressed in photoreceptor cells)

between the mouse Pax6and Drosophila eyeless genes in eye development may be inherited from a common ancestor. The remarkable conservation of Pax6 expression and the Pax6-regulated circuit suggests that all bilaterian eyes share a common developmental genetic circuit and that this circuit was present in the bilaterian ancestor. Although we cannot say whether Urbilateria had eyes per se, it is likely to have possessed light sensing cells whose differentiation depended upon Pax6 function.

Several other developmental features of Urbilateria may be inferred from the conservation of developmental patterning roles of toolkit genes (Fig. 4.12). The similarity between D/V axis polarization by the short gastrulation/chordin genes and TGF-$ signaling in insects and vertebrates, and A/P axis regionalization by Hox genes in many bilaterians, suggests that these genes also controled the patterning of the primary body axes of Urbilateria. A suite of common mesoderm patterning genes (including Brachyury, Twist, mef2, and Snail) is shared among insects and vertebrates. In fact, all of these genes and patterning systems have been identified in cnidarians as well, and their roles as developmental regulatory genes clearly predated Urbilateria. Cnidarians have a very different body organization, but do deploy the TGF-$ and Wnt signaling cascades during formation of the primary body axis, Hox and ParaHox genes in restricted axial domains, and several anterior patterning genes (homologs of Brachyury, emx, forkhead, and paired-like genes) during head formation. Several bilaterian mesoderm patterning genes (Brachyury, Twist, mef2, and Snail) are expressed in striated muscles in the medusa stage of a hydrozoan, suggesting that bilaterian mesoderm may have an ancestral relationship to cnidarian striated muscle.

Using similar logic, additional patterning mechanisms present in Urbilateria can be inferred from other shared regulatory roles for toolkit genes in deuterostomes and protostomes. Anteroposterior patterning of the Urbilaterian endoderm, ectoderm, and nervous system may have been regulated by the ParaHox genes (Gsx, Xlox, Cdx), certain segmentation genes (hairy, engrailed, Notch), and brain patterning genes (emx, otx, Hox), respectively. Even the expression patterns of the genes involved in dorsal-ventral patterning of the central nerve cord of flies and mice are similar (vnd/NK-2, ind, msh, netrins). Perhaps most surprisingly, similarities in the genetic regulatory mechanisms that control the development of cardiac tissue (tinman/Nkx2.5) and appendages (Dll/Dlx; hth/Meis + Exd/Pbx) in insects and vertebrates suggest that Urbilateria could have possessed a primitive contractile organ and structures that projected from the body.

Without fossils of early animal ancestors, we can only speculate about the complexity of the primitive bilaterian body plan. Perhaps the "organs"of Urbilateria were simple structures composed of a few specific cell types. For example, Urbilateria may have had a simple photoreceptor complex rather than an optically sophisticated eye, a contractile muscle regulating hemacoel fluids rather than a modern heart, and a simple outgrowth of the body wall or tentacle-like feeding structure rather than a modern locomotory appendage (Fig. 4.12). Although the anatomical details remain uncertain, the development of such structures could sufficiently constrain gene evolution to conserve the function of regulatory genes across Bilateria.

All of these features combine to build a fairly complex image of the "primitive" bilaterian, representing an animal that could move (or perhaps crawl) through sediment and could sense and interact with the environment. Perhaps most importantly, this type of ancestor would have many morphological features and genetic tools that might have facilitated a successful evolutionary response to changes in the natural history of early animal life, including

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