Chapter 22:  “Unity of Type” and “Conditions of Existence”

Charles Darwin's synthesis

In the 1800s, debates over the origin of species pitted against each other two ways of looking at nature. One view (championed by Georges Cuvier and Charles Bell) focused on the differences among species that allowed each species to adapt to its environment. Thus, the fingers of the human hand, the flipper of the seal, and the wings of birds and bats were seen as marvelous contrivances, fashioned by the Creator, to allow these animals to adapt to their “conditions of existence.” The other view, championed by Geoffroy St. Hilaire and Richard Owen, was that these adaptations were secondary, and that the “unity of type” (what Owen called “homologies”) was critical. The human hand, the seal's flipper, and the wings of bats and birds are each modifications of the same basic plan (see Figure 1.13). In discovering that basic plan, one can find the form upon which the Creator designed these animals. The adaptations were secondary.

Darwin acknowledged his debt to these earlier debates when he wrote in 1859, “It is generally acknowledged that all organic beings have been formed on two great laws—Unity of Type, and Conditions of Existence.” Darwin went on to explain that his theory would explain unity of type by descent from a common ancestor. Moreover, the changes creating the marvelous adaptations to the conditions of existence were explained by natural selection. Darwin called this concept “descent with modification.” As mentioned in Chapter 1, Darwin found that homologies between the embryonic and larval structures of different phyla provided excellent evidence for descent with modification. He also argued that adaptations that depart from the “type” and allow an organism to survive in its particular environment develop late in the embryo. Thus, Darwin recognized two ways of looking at “descent with modification.” One could emphasize the common descent by pointing out embryonic homologies between two or more groups of animals, or one could emphasize the modifications by showing how development was altered to produce structures that enabled animals to adapt to particular conditions.

E. B. Wilson and F. R. Lillie

Darwin did not attempt to construct complete phylogenies from embryological data, but his work inspired many of his contemporaries to do so. One of the first scientists to realize the evolutionary importance of von Baer's laws (see Chapter 1) was Elie Metchnikoff. Metchnikoff appreciated that evolution consists of modifying embryonic organisms, not adult ones. In 1891, he wrote:

But if changes in embryonic development effected evolutionary changes, how did these developmental changes take place? During the late 1800s, many investigators attempted to link development to phylogeny through the analysis of cell lineages. They meticulously observed each cell in developing embryos and compared the ways in which different organisms formed their tissues. In 1898, two eminent embryologists gave cell lineage lectures at the Marine Biological Laboratory at Woods Hole, Massachusetts, that served to emphasize the two ways in which embryology was being used to support evolutionary biology. The first lecture, presented by E. B. Wilson, was a landmark in the use of embryonic homologies to establish phylogenetic relationships. Wilson had observed the spiral cleavage patterns of flatworms, molluscs, and annelids, and he had discovered that in each case, the same organs came from the same groups of cells. For him this meant that these phyla all had a common ancestor. Indeed, modern research using DNA sequences has confirmed Wilson's conclusion and placed these three phyla together.

The other lecturer was F. R. Lillie, who had also done his research on the development of molluscan embryos and on modifications of cell lineages. He stressed the modifications, not the similarities, of cleavage. His research on Unio, a mussel whose cleavage pattern is altered to produce the “bear-trap” larva that enables it to survive in flowing streams, was highlighted in Chapter 8. Lillie argued that “modern” evolutionary studies would do better to concentrate on changes in embryonic development that allowed for survival in particular environments than to focus on ancestral homologies that united animals into lines of descent.

In 1898, then, the two main avenues of approach to evolution and development were clearly defined: to find underlying unities that link disparate groups of animals, and to detect those differences in development that enable species to adapt to particular environments. Darwin thought these two approaches to be temporally distinguished—that is, that one would find underlying unities in the earliest stages of development, while the later stages would diverge to allow specific adaptations (see Ospovat 1981). However, Wilson and Lillie were both discussing the cleavage stage of embryogenesis. These two ways of characterizing evolution and development are still the major approaches today.

“Life's splendid drama”

Until this decade, “many invertebrate biologists saw the reconstruction of relationships among the phyla as an insoluble dilemma. … Indeed, as late as 1990, a comprehensive summary concluded that the relationships between most of the higher animal groups were entirely unresolved” (Erwin et al. 1997). However, in the 1990s, a broad consensus on the general form of a phylogenetic tree of life began to emerge among paleontologists, molecular biologists, and developmental geneticists (see Winnepenninckx et al. 1998; Davidson and Ruvkun 1999; Erwin 1999). This consensus (one representation of which is shown in Figure 22.1A) came about from (1) improved methods of analyzing DNA, taking into account its variation within groups of animals, (2) new data on conserved regulatory gene sequences such as the Hox genes, which are usually stable within phyla but can diverge between phyla, (3) morphological evidence for the related nature of some structures that had once been thought to be distinct, and (4) computer programs that can sort out enormous amounts of data, not privileging any particular set of relationships over others. The results were surprising to many scientists.

• 1

  The animal kingdom can be divided into Porifera (sponges), Cnidaria and Ctenophora (jellyfish and comb jellies), and the Bilateria. The Porifera lack any coherent epithelium or any symmetry. The Cnidaria and Ctenophora are diploblastic (with two epithelial layers, lacking mesoderm) and have radial symmetry.

• 2

  The Bilateria are triploblastic (with true endoderm, mesoderm, and ectoderm), have bilateral symmetry and can be divided into two groups, the deuterostomes and the protostomes. The deuterostomes include the echinoderms and the chordates. (Echinoderm larvae are originally bilateral.) Deuterostomes form their anuses from their blastopores. They probably arose from a tornaria larva similar to that of the pluteus.

• 3

  The protostomes can be divided into two groups, the Ecdysozoa (animals whose bodies are covered by an exoskeleton, which therefore molt as they grow) and the Lophotrochozoa (animals that have most or all of their soft tissues in contact with the environment and which generally use cilia in feeding or locomotion). Nematodes and flatworms (which lack true coeloms) had formerly been considered basal groups, perhaps ancestral to both the protostomes and the deuterostomes. However, the new studies have shown that the nematodes belong to the Ecdysozoa and the flatworms (as Wilson had predicted) to the Lophotrochozoa. Each of these two groups is monophyletic, meaning that the phyla in each of them share a common ancestor.

The search for the Urbilaterian ancestor

It is doubtful that we will find a fossilized representative of the ancestral phylum that gave rise to both the deuterostomes and the protostomes. Such a hypothetical animal is sometimes called the Urbilaterian ancestor or the PDA (protostome-deuterostome ancestor). Since such an animal probably had neither a bony endoskeleton (a deuterostome trait) nor a hard exoskeleton (characteristic of ecdysozoans), it would not fossilize well. However, we can undertake what Sean Carroll (quoted in DiSilvestro 1997) has called “paleontology without fossils.” The logic of this approach is to find homologous genes that are performing the same functions in both a deuterostome (usually a chick or a mouse) and a protostome (generally an arthropod such as Drosophila). Many such genes have been found (Table 22.1), and their similarities of structure and function in protostomes and deuterostomes make it likely that these genes emerged in an animal that is ancestral to both groups.

Pax6, for example, plays a role in forming eyes in both vertebrates and invertebrates (see Chapters 4 and 5). Ectopic expression of Pax6 will form extra eyes in both Drosophila and Xenopus, representatives of the protostomes and deuterostomes, respectively (Chow et al. 1999; see Figure 5.14). Moreover, the ectopic expression of a deuterostome (mouse) Pax6 gene in a fly larva will also induce ectopic fly eyes (Figure 22.1B; Halder et al. 1995). Therefore, it is a safe assumption that the same Pax6 gene is involved in eye production in both deuterostomes and protostomes. Moreover, at least three other genes—sine oculis, eyes absent, and dachshund—are also used to form eyes in both Drosophila and vertebrates (Jean et al, 1998; Relaix and Buckingham, 1999). Since it is extremely unlikely that deuterostomes and protostomes would have evolved the Pax6 (and other) genes independently and used it independently for the same function, it is very likely that the PDA had a Pax6 gene and used it for generating eyes.

Another such gene shared by deuterostomes and protostomes is the homeobox-containing gene tinman. The Tinman protein is expressed in the Drosophila splanchnic mesoderm, eventually residing in the region of the cardiac mesoderm. Loss-of-function mutants of tinman lack a heart (hence its name, after the Wizard of Oz character) (Bodmer 1993). In mice, the homologous gene is called Nkx2–5 and it, too, is originally expressed in the splanchnic mesoderm and then continues to be expressed in those cells that form the heart tubes (see Chapter 15; Manak and Scott 1994). Thus, although the heart of vertebrates and the heart of insects have hardly anything in common except their ability to pump fluids, they both appear to be predicated on the expression of the same gene, Nkx2–5/tinman. Therefore, it is probable that the PDA had a circulatory system with a pump based on the expression of the Nkx2–5/tinman gene.

Another set of genes shared by the deuterostomes and protostomes are those for the transcription factors involved in head formation (Finkelstein and Boncinelli 1994; Hirth and Reichert 1999). In Drosophila, the brain is composed of three segments called neuromeres. These neuromeres are specified by three transcription factors. The genes encoding these factors are tailless (tll) and orthodenticle (otd), which are expressed predominantly in the anteriormost neuromere, and empty spiracles (ems), which is expressed in the posterior two neuromeres (Monaghan et al. 1995; Hirth et al. 1998). Loss-of-function mutations of otd eliminate the anteriormost neuromere of the developing Drosophila embryo, and loss-of-function mutations of ems eliminate the second and third neuromeres (Hirth et al. 1995). In frogs and mice, the homologues of these genes (Otx-1, Otx-2, Emx-1, Emx-2) are also expressed in the brain (Simeone et al. 1992), although the exact patterns of transcription are not identical (Figure 22.2). The Otx-2 gene has been experimentally knocked out by gene targeting (Acampora et al. 1995; Matsuo et al. 1995; Ang et al. 1996), and the resulting mice have neural and mesodermal head deficiencies anterior to the r3 rhombomere. In humans, mutations of EMX2 lead to a rare condition known as schizencephaly, in which there are clefts ripping through the entire cerebral cortex (Brunelli et al. 1996). Even though the Drosophila otd and ems genes are specified by the Bicoid and Hunchback gradients and the mammalian Otx and Emx transcripts are induced by the anterior dorsal mesoderm, it appears that the same genes are used for specifying the anterior brain regions.

It appears, then, that the ancestor of all bilaterian organisms had sensory organs based on Pax6, a heart based on tinman, and a head based on Otx, Ems, and tll. It also had something else: an anterior-posterior polarity based on the expression of Hox genes. The analysis of Hox genes has given us critical clues as to how morphological changes could occur through alterations of development. So we return to our analysis of Hox genes.