Evolution Of Radical Body Plan Changes

Morphological novelty also encompasses the evolution of novel body organizations. Radical reorganization of body plans can include both the appearance of new structures and the loss of ancestral characters. The first two examples we discuss here have lost one or more key morphological features characteristic of their clade. The other examples illustrate the appearance of new characters and rearrangements of older features resulting in dramatically different body organization. As with the other types of novelties discussed in this chapter, these morphological changes are correlated with changes in genetic regulatory circuits.

Loss of the ascidian tail, a chordate lacking the notochord

Although the notochord is a defining feature of the chordates, several ascidian species have an abbreviated larval stage that has lost the notochord along with the entire larval tail. Of the more than 3000 ascidian species known, about a dozen are tailless. Loss or reduction of the larval tail has occurred at least six independent times in the ascidian lineage. Taillessness is associated with direct development, including a rapid progression to the sessile adult form.

In some cases, very closely related species differ dramatically in the extent of their tail development. For example, the urodele (tailed) larvae of Molgula oculata develop a notochord, a spinal cord, and striated muscle cells. By contrast, another Molgula species (M. occulta) has an anural (tailless) larval stage that lacks these characteristic chordate features. When these species are interbred in the laboratory, the crosses yield a short-tailed hybrid, complete with notochord (Fig. 6.12). Thus the tailless phenotype of M. occulta can be rescued by the M. oculata genome, suggesting that M. occulta may have lost some genetic function that results in its tailless larval form.

Changes in the tail development program that lead to an anural form occur downstream of Brachyury expression in the notochord. Notochord cells are specified normally in M. occulta and M. tectiformis (another tailless species) but these cells do not divide properly or undergo appropriate morphogenetic movements to form the notochord. The search for genes that are essential for M. oculata tail development, but that are downregulated in M. occulta, has led to the identification of the Manx, Bobcat, and FoxA5 genes. The Manx gene is a zinc-finger transcription factor, Bobcat encodes an RNA helicase, and FoxA5 encodes a winged helix transcription factor. The expression of these genes is largely restricted to the embryonic cells that will give rise to the M. oculata larval tail (including the notochord). These genes are similarly deployed in M. oculata x M. occulta hybrids, and inhibition of any of these genes results in an increase in programmed cell death in notochord and tail muscle cells that generates a tailless embryo. The requirement for Manx, Bobcat, and FoxA5 gene function indicates that these genes are part of the developmental program for tail formation.

Molgula oculata hybrid

Molgula occulta

Figure 6.12

Tailed and tailless forms of two closely related ascidian species

(left) A tailed M. oculata larva has an otolith (a pigmented organ in the head) and a notochord. (right) A tailless M. occulta larva lacks the otolith and notochord. (middle) A hybrid larva, derived from a M. occulta egg fertilized with a M. oculata sperm, displays an otolith and a short tail, complete with notochord. The Manx, bobcat, and FoxA5genes are essential for tail development in M. oculata and in the hybrid.

Source: Swalla BJ, Jeffery WR. Science 1996; 271: 1205-1208. Copyright (1996), reprinted with permission from AAAS.

The reduced expression of the Manx, Bobcat, and FoxA5 genes in the tailless species M. occulta suggests that the tail regulatory hierarchy is terminated early in development. During the evolution of this tailless form, the expression or function of an upstream regulator common to these genes may have been changed that led to the loss of expression of these genes. Interestingly, disruption of tail development seems to have relieved the selective pressure on downstream genes necessary for tail function. Several muscle actin genes, which in urodele ascidians are expressed in tail muscle cells, have become pseudogenes in several independent anural ascidian lineages. The altered expression of a single regulatory gene required for tail development may be sufficient to evolve a novel larval form and to release selective constraint on the network of dependent genes.

Limbless tetrapods, or how the snake lost its legs

The evolution of snakes, with their characteristic elongated bodies and reduced limbs, represents an adaptation of the tetrapod body plan to a novel form. Body elongation and limblessness are associated with burrowing and have evolved independently many times within the reptiles, including once at the base of the snake lineage. Among modern snakes, the python lineage retains some features of the tetrapod hindlimb, including a pelvic girdle and rudimentary hindlimbs, whereas more highly derived snakes are completely limbless. Comparisons between snakes and other tetrapods have revealed key developmental genetic differences in axial patterning and limb development that correlate with the evolutionary transition to the limbless snake body plan.

The concomitant loss of snake forelimbs and expansion of thoracic axial identities suggest that a common genetic mechanism may underlie these evolutionary transitions. In Chapter 5, we discussed the correlation between the python axial skeleton identities and the anterior expansion of the expression domains of Hoxc6and Hoxc8. In other tetrapods, the axial position of the forelimb is determined by the anterior boundary of Hoxc6 expression in lateral plate mesoderm at the cervical-thoracic transition (see Fig. 5.6). Thus the extension of the expression pattern of python Hoxc6 and Hoxc8 up to the cranial region may disrupt the Hox-regulated positioning of the forelimb. Without the proper axial patterning cues, this limb bud never forms. The correlation between trunk elongation and limb loss in several other vertebrate taxa may be explained by similar changes in axial patterning caused by altered Hox expression patterns.

The fossil record and developmental studies indicate the reduction and loss of the snake hindlimb occurred via a separate series of evolutionary events. The initial development of the vestigial python hindlimb appears normal, indicating that the axial specification cues and early induction of python hindlimb development remain intact. As in other tetrapods, the posterior boundaries of Hoxc6 and Hoxc8 expression mark the python thoracic-lumbar transition at the position of the rudimentary pelvic girdle, and a limb bud does form. Ultimately, however, development of the hindlimb is arrested and no outgrowth is observed.

The python hindlimb bud lacks some of the characteristic features of other developing tetrapod limbs, such as an apical ectodermal ridge (AER) and a zone of polarizing activity (ZPA). Nevertheless, experimental manipulations have shown that the python limb bud mesenchyme retains the capacity to induce an AER and a ZPA; indeed, it can form a complete limb in response to an inductive signal from an exogenous AER. Thus much of the developmental program of limb formation is present in the python limb bud, but at least one essential element must be missing. The termination of python hindlimb development suggests that this field fails to initiate or maintain the signaling events that are required for AER formation and hindlimb outgrowth.

The loss of a structure is not necessarily accompanied by the loss of the genes—or even genetic regulatory circuitry—required to build that structure. The condition of limblessness can be reversed, as evidenced both by rare individuals in wild populations and by stable evolutionary lineages. For example, rare natural occurrences of cetaceans (whales and dolphins) with well-developed hindlimbs have been reported. Also, the snake fossil record shows that a limbless ancestor may have given rise to a group of snakes that had substantial limbs (Fig. 6.13). For example, the fairly well-developed hindlimbs of the snake fossils Pachyrhachis problematicus and Hassiophis terrasanctus may represent a reversal from a limbless state. Based on these cases of reversion to the ancestral limbed condition, it appears that the limb developmental program may still be present in limbless animals. As the genes required for limb patterning have other developmental functions, they are retained in the genomes of limbless taxa. More surprising, however, is that an otherwise cryptic regulatory circuitry required for limb development is retained in a limbless tetrapod.

The evolution of the turtle shell

The turtle shell is the novel structure that defines the order Chelonia. The two main components of the shell are the dorsal carapace and the ventral plastron (Fig. 6.14a,b), which are linked loss/ reduction of snake hindlimbs

Hindlimbs

Advanced snakes none

Pythons, boas gain of well-developed hindlimbs vestigial

Pachyrhachis well-developed

Haasiophis well-developed

Pipesnakes, shieldtails

Blindsnakes

Lizards complete

Figure 6.13

Evolutionary transitions in snake limblessness

The phylogeny of snakes indicates that the loss of snake hindlimbs may have evolved once at the base of the snake lineage. The existence of well-developed hindlimbs in the fossils Pachyrachis and Haasiophis suggests that hindlimbs reappeared during the evolution of these species, as their ancestor may have been limbless. Alternatively, snake hindlimbs could have been independently lost in each limbless snake lineage.

Source: Redrawn from Greene HW, Cundall D. Science 2000; 287: 1939-1941.

laterally by several bony bridges. The evolution of this bony casing encompassed a large number of modifications to the tetrapod body plan including rearrangements of the pectoral girdle, ribcage, vertebrae, neck, and skull. While dermal ossification is a primitive character for vertebrates as evidenced by numerous fossil fish specimens that display extensive exoskeletons, the turtle shell represents an extreme elaboration of the dermal skeleton among tetrapods.

The ventral plastron and dorsal carapace arise by different mechanisms during turtle development. Cells in the plastron express molecular markers of bone-forming neural crest cells, suggesting that the turtle plastron is derived from neural crest cells. However, in extant tetrapods trunk neural crest cells generally do not contribute to skeletogenesis. The turtle may have retained this ability or recruited the head neural crest cells to elaborate the ventral portion of this unique structure.

While formation of the ventral plastron in turtles might reflect the retention or redeployment of dermal armor found in early gnathostomes, the dorsal carapace arises from a novel structure, the carapacial ridge (CR), a bulge of ectoderm and mesoderm that arises on the dorsal flank of the turtle embryo. During turtle development, the ribs become trapped by the CR, enclosed within the dorsal dermis, and displaced laterally (Fig. 6.14d), later fusing with the dermis of the carapace (Fig. 6.14c). The tissue composition of the carapacial ridge is similar to that of the early vertebrate limb bud. Perhaps not surprisingly, the Fgf10 and Msx genes are expressed in the distal mesenchyme of the CR, similar to their expression patterns none none a b

Figure 6.14

Origin of the turtle shell.

Generalized pattern of the bones of the turtle (a) carapace and (b) plastron. These dermal bones are unique to the order Chelonia.

(c) Ventral view of Chelydra serpentina carapace (plastron has been removed) showing the fusion of ribs, vertebrae, and dermal bones.

(d) Cross-section of Trachemys scripta embryo at day 29 of incubation. The ribs have become trapped in the carapacial ridge and grow laterally rather than ventrally. R, rib; V, vertebrae.

Source: Gilbert SF, Loredo GA, et al. EvolDev2001; 3: 47-58. Reproduced with permission of Blackwell Publishing Ltd.

in the growing limb bud underlying the AER. The expression of these genes in the CR, coupled with the similarities in morphology and development between the limb AER and the turtle shell CR, suggests that the same mechanisms may initiate the formation of these two structures. The CR does not express Fgf8 however, a crucial molecule required for limb outgrowth. The

CR may have arisen during evolution as the result of co-option of part of the limb initiation pathway.

Evolution of the cephalopod body plan

The molluscs appear in the fossil record of the early Cambrian about 530 million years ago. Extant molluscan species display a wide range of body plans but the typical mollusc has three defining features: a shell, a mantle, and a ventral locomotory foot (see Fig. 6.15a). Despite a close affinity to gastropod molluscs (snails, slugs, etc.), cephalopod molluscs (squids, nautiluses, octopuses, cuttlefish) have evolved striking modifications to these features. The cephalopod mantle has evolved new roles in respiration and locomotion while the ventral foot has been modified to form the arms of the brachial crown (tentacles) and funnel tube, used for locomotion. In addition, except for Nautilus, the cephalopod shell has been greatly reduced or lost (Fig. 6.15a,b).

Cephalopod squids (Euprymna scalopes) possess a complement of Hox genes typical of Lophotrochozoans: one anterior, one paralog group 3, five central, and two posterior group Hox genes. Six of these Hox genes are expressed in the central nervous system and while their expression patterns do not violate the principle of colinearity, they also do not display a canonical nested pattern. Strikingly, the Hox genes are expressed in morphological novelties unique to the cephalopods such as the arms of the brachial crown and the funnel tube. However, the anteroposterior expression domains of the Hox genes in these structures do not agree with Hox colinearity. Different subsets of Hox gene are expressed in nested domains within the funnel tube, while multiple Hox genes are expressed in dynamic combinations in the arms of the brachial crown (Fig. 6.15c). Other novel structures show the recruitment of individual Hox genes.

These radical changes in Hox gene expression domains suggest that the evolution of cephalopod morphological novelties was accompanied by, or even precipitated by, the deployment of Hox genes in unique patterns defining new structures. While collinear expression of Hox genes is evident in other molluscs, the loss of collinear regulation in cephalopods may be tied to the use of Hox genes to regulate developmental events other than anteroposterior patterning.

Evolution of the echinoderm body plan

The defining features of the Bilateria, including the evolution of bilateral symmetry with distinct rostrocaudal and D/V axes, arose before the radiation of most animal phyla. Although the echinoderms (sea stars, sea urchins, sea cucumbers, brittle stars, and crinoids) are a basal deuterostome lineage derived from a bilaterian ancestor, echinoderm adults have a radially symmetric body organization. Whereas echinoderm larvae exhibit a more typical bilateral form, adult echinoderms are radically rearranged, making it difficult to identify any vestiges of bilateral symmetry (Fig. 6.16). The fivefold symmetry of the adult nervous system, connected by a central nerve ring, has led to the proposal that each echinoderm "arm" represents a duplication of the bilaterian A/P axis. Alternatively, the distribution of mesodermal tissue in the adult may indicate that the orthogonal adult oral—aboral axis is derived from the larval A/P axis. The origin of the unique and highly derived body plan of adult echinoderms remains a puzzle.

Shell

Shell

Mouth

Shell

Mouth

Foot

Monoplacophoran-like ancestor

Mantle Gills

Mantle cavity

Mouth

Gladius (reduced s hell)

Mantle

Shell

Mouth

Early cephalopod

Foot

Monoplacophoran-like ancestor

Gills Mantle cavity Arms Foot (anterior foot) (posterior)

Early cephalopod

Mouth

Mouth

Mantle

Gills Mantle cavity

Funnel (posterior foot)

Brachial crown (anterior foot)

Coleoid cephalopod

Mantle

Gills Mantle cavity

Funnel (posterior foot)

Brachial crown (anterior foot)

Coleoid cephalopod

Arm Arm Arm Arm Arm I II III IV V

Funnel tube

Arm Arm Arm Arm Arm I II III IV V

Funnel tube c

Figure 6.15

Evolution of the cephalopod mollusc body plan

(a) Proposed scheme of cephalopod evolution from a monoplacophoran-like ancestor, illustrating shell internalization/reduction, mantle expansion and co-option for locomotion/respiration, and foot modifications forming the brachial crown and funnel tube (anterior, left; dorsal, top). (b) Euprymna scolopes hatchling, (dorsal, top), and diagram showing the characteristic adult cephalopod body plan. Scale bar, 1 mm. (c) Summary of two embryonic stages highlighting the dynamic temporal and spatial pattern of Hox expression in the brachial crown and funnel tube during development (relative expression levels indicated by shading intensity). Source: Lee PN, Callaerts P, et al. Nature 2003; 424: 1061-1065. Copyright (2003), reprinted with permission from Nature.

Figure 6.15

Evolution of the cephalopod mollusc body plan

(a) Proposed scheme of cephalopod evolution from a monoplacophoran-like ancestor, illustrating shell internalization/reduction, mantle expansion and co-option for locomotion/respiration, and foot modifications forming the brachial crown and funnel tube (anterior, left; dorsal, top). (b) Euprymna scolopes hatchling, (dorsal, top), and diagram showing the characteristic adult cephalopod body plan. Scale bar, 1 mm. (c) Summary of two embryonic stages highlighting the dynamic temporal and spatial pattern of Hox expression in the brachial crown and funnel tube during development (relative expression levels indicated by shading intensity). Source: Lee PN, Callaerts P, et al. Nature 2003; 424: 1061-1065. Copyright (2003), reprinted with permission from Nature.

The development of other structural novelties of echinoderms, including the water vascular system and the calcitic endoskeleton, appears to involve regulatory genes shared with other phyla. These genes have been recruited for deployment in echinoderm-specific tissues in the developing juvenile sea urchin. Runt, Dll, and Otx (in direct developers) are expressed in the tube feet (podia), which are extensions of the water vascular system. Hox3 is expressed in the nascent tooth sacs, which give rise to the echinoderm mouthparts. The pattern of en expression in the ectoderm reflects the organization of the underlying endoskeleton. In short, these regulatory genes appear to have been co-opted for new patterning roles associated with the evolution of novel echinoderm structural elements.

Sea stars

Brittle stars

Sea urchins

Sea cucumbers

Crinoids

Bilaterally symmetric larvae

Radially symmetric adult

Sea cucumbers

Otx Sea Urchin
0 0

Post a comment