Why is segmentation important in some phyla

Just as segmentation could evolve in one organ system at a time, segmentation could also be secondarily lost in one organ system but not another. Evidence for secondary simplification is found in Echiura and in mollusks. Echiura is a group of marine worms that are most probably highly derived annelids [ 46 - 48 ].

While Echiura share many developmental traits with the annelids, they lack the epidermal and muscular segmentation of bona fide segmented worms, leading to debate over their relationship. However, recent phylogenies place them within the annelids [ 47 , 48 ].

Moreover, immunohistochemical analysis of neuronal markers shows that the nervous system of the Echiura Bonellia viridis is arranged in an organized, serial fashion, similar to the nervous systems of segmented worms [ 46 ].

These data suggests that the Echiura evolved from a segmented ancestor and later lost most segmental characteristics. As with the case of Echiura, segmentation may have been secondarily lost in some mollusks.

The cephalopods are considered to be unsegmented. However, recent phylogenies group them with the Monoplacophorans, shelled deep-sea mollusks that have the segmental characteristics of serially repeated gills, nephridia, and muscles [ 49 , 50 ]. While these data could suggest that Monoplacophorans independently evolved segmentation, closer examination of the chambered nautilus instead suggests that segmentation may have been lost in cephalopods [ 51 ].

The nautilus has two pairs of gills, kidneys, and atria, which can be interpreted as secondary simplification from a segmented ancestor. These examples of probable secondary loss of segmentation in annelids and mollusks suggest that there is no biological distinction between segments composed of many versus one organ system, and therefore argue against the requirement that segments be composed of multiple tissue layers.

While most of the arthropod body is universally considered segmented, controversy exists over whether the anterior-most section of the head is a segment, and the segmental affiliation of appendage-like structures, such as the labrum [ 52 ].

As there are general reviews of these subjects elsewhere [ 52 , 53 ], we will focus here on the question of whether the tip of the head is a segment in the context of how phylogenetic assumptions can influence segmental classifications. The anterior-most region of the arthropod head, the ocular lobe protocerebrum , is different from head and trunk segments, as it contains the brain and does not bear a set of antennae or other appendages Figure 4 A [ 52 , 53 ].

However, the ocular lobe also has many morphological similarities to the rest of the segments, making it hard to classify as either unsegmental or segmental [ 22 , 52 , 53 ]. The difficulty in using morphology to classify the ocular lobe as a segment may have lead researchers to depend overly on phylogenetics to solve this question. Before the new molecular phylogeny, the Articulata hypothesis placed the annelids as close relatives to the arthropods. Therefore, it was assumed that the arthropods had an unsegmented anterior region, homologous to the unsegmented anterior region, or prostomium, of annelids Figure 4 B,C [ 1 , 52 ].

The annelid prostomium lies in front of the mouth and contains the brain and sense organs. The prostomium is considered unsegmented because its embryonic origin is different from the segmented body and because it does not have characteristics of other segments, such as coelomic sacs and nephridia [ 52 ]. Additionally, in annelid species that have a trochophore larvae, the prostomium episphere , is located anterior to the first ciliary ring prototroch. If the annelid prostomium and the arthropod ocular lobe were homologous, then, based on annelid data, the ocular lobe would not be considered a segment.

However, since the new molecular phylogeny places the arthropods and annelids in two separate megagroups of the bilatarians, the homology of the annelid prostomium and arthropod ocular lobe, and thus the unsegmented nature of the ocular lobe, has come into dispute [ 5 ]. Annelid, arthropod, and vertebrate heads.

A The segmental nature of the anterior region, or ocular lobe, of the arthropod head is disputed orange. Ventral view of a hour Parhyale embryo. Definitively segmented head segments are shaded in gray antennae 1, antennae 2, mandibles, maxillae 1, maxillae 2, and the maxillipeds. B, C Annelids have an unsegmented anterior region, or prostomium yellow.

Lateral view of a polychaete trochophore larva B , and ventral view of the anterior region of an earthworm C after [ 54 ]. D Vertebrates have head structures with segmental characteristics, such as the rhombomeres red and pharyngeal arches blue. Lateral view of the anterior region of a hour zebrafish embryo, head slightly curved ventrally.

While molecular data likely resolved the relationship between arthropods and annelids, molecular studies have not yet solved the question of whether the ocular lobe is a segment. In Drosophila , analysis of mutations in genes with roles in head development suggests that it is a segment [ 55 ].

Also, segmental and appendage genes are expressed in the ocular lobes of many arthropod species [ 36 , 55 - 61 ]. However, expression of segment polarity or appendage genes is limited to one, often transient, region per ocular lobe, unlike other segments, where there is a persistent domain of strong expression.

This may be due to the highly derived nature of the head, or, since these genes are all pleiotropic, this may indicate a fundamental difference in the ocular lobe versus the undisputed segments of the rest of the body.

While this problem may never be fully solved, studying the arthropod head will undoubtedly yield interesting insights that would never be uncovered if the assumption about head homology had not been questioned. Vertebrates have structures in their heads that could be considered segmental, but that are distinct from their trunk segments.

Controversy exists on whether these head structures are segmented as they do not easily fit into the already tenuous definition of segmentation formed from studies on trunk segments. Moreover, researchers have divided the vertebrate head it into segments in numerous different ways, some of which may be artificial. To clarify what parts of the head are most likely to be segmented, here we give an overview of how some head structures are probably misconstrued as segmented, followed by a brief discussion of the head structures that have the most evidence for being considered segmented, the rhombomeres and pharyngeal arches.

The vertebrate head has been divided into segments in many different ways [ 62 - 70 ]. While the vertebrate head probably contains a number of independently segmented structures, there is little or no reliable morphological or molecular data to support some of these claims. Two examples are the somitomeres and prosomeres. Somitomeres are defined as segmental structures of the paraxial mesoderm that resemble somites, the trunk mesodermal segments [ 66 , 67 ]. Somitomeres are an attractive theory, as their existence would suggest that the head and trunk share a unified segmental developmental program.

However, there is only disputed scanning electron microscope data to support their existence, and no data to support a shared segmental program between the vertebrate head and trunk. Prosomeres, or forebrain segments, would also provide a framework to organize the vertebrate head [ 70 , 71 ].

However, while the forebrain may be partitioned, there is neither repeated morphological pattern nor molecular segmental polarity to support segmentation.

Hox gene expression has often been used to support the claim that the vertebrate head is segmented for example, see [ 63 , 67 ]. Hox gene expression often correlates with anterior segmental or parasegmental boundaries and Hox proteins determine what type of structure will form from each segment [ 72 , 73 ]. However, this does not imply that Hox genes are a marker of segmentation and, therefore, Hox expression should not be used to define a body region, such as the head, as segmented.

In support of not equating nested Hox gene expression to segmentation, knock-out, and overexpression of Hox genes alters segment identity, but do not prevent the formation of segments [ 72 , 73 ]. Moreover, many unsegmented animals express Hox genes along their a-p axis but are not segmented, no matter what definition is used for example, see [ 74 , 75 ].

Although clearly important for patterning segmental structures, Hox gene expression by itself should not be used as molecular evidence of segmentation. While more evidence is needed to support many of the claims for segmentation in the vertebrate head, there is morphological and molecular evidence to support two structures, the rhombomeres and pharyngeal arches, as segmented Figure 4 D [ 66 ]. The rhombomeres are seven transient compartments in the chordate hindbrain that control neural organization and architecture [ 76 ].

If each rhombomere were a segment, we would expect a repeated pattern of segment polarity, such as the expression of a gene in only the anterior or posterior part of each rhombomere. Instead, there is a two-rhombomere periodicity of gene expression, where the ephrin ligands are expressed in even-numbered rhombomeres, and their receptors, the Ephs , are expressed in odd-numbered rhombomeres [ 77 ]. While this is often compared to the two-segment periodicity of pair-rule genes in Drosophila , each segment in Drosophila ultimately has its own segment polarity [ 17 ].

There is still polarity in each rhombomere, however, since motor neurons and their axon trajectories have a repeated pattern in each rhombomere [ 68 ]. Pharyngeal arches also have segmental characteristics. The pharyngeal arches are bulges on the lateral surface of the embryonic head that give rise to skeletal and muscular derivatives, sensory ganglia, and motor innervations [ 78 ].

The pharyngeal arches are composed from ectoderm, mesoderm, endoderm, and neural crest cells. Together, these tissues are arranged so that there is a reiterated pattern within each arch. Morphologically, cartilage is in the anterior region while a blood vessel is in the posterior region.

Molecularly, the ETS-type transcription factor polyomavirus enhancer activator 3 is expressed in the anterior mesenchyme and in the posterior epithelium [ 79 ]. These data suggest that pharyngeal arches are segmented. Despite their segmental characteristics, rhombomeres and pharyngeal arches are often not considered in comparisons of segmentation among the arthropods, annelids, and chordates. Perhaps this is because rhombomeres and the neural crest component of pharyngeal arches are vertebrate innovations, and therefore do not have homologous counterparts in the arthropods and annelids.

Although, as some authors suggest, these seemingly vertebrate specific segmental head structures could have been superimposed upon an ancestral segmental body plan, similar to that of the arthropods and annelids [ 63 ] see [ 67 ] for a persuasive counterpoint.

Most importantly, the a-p pattern within each rhombomere and pharyngeal arch suggest that they are segmental and therefore should be considered in further studies and discussions of segmentation. As vertebrate innovations, they are especially interesting as models of segmental evolution in novel structures.

Ideally, a precise definition of segmentation would facilitate our understanding of mechanisms of development, and inform our thoughts on evolutionary processes and events. Instead, more than two millennia of studying segmentation in animals have failed to produce a definition of segmentation that is applicable in even a majority of cases. Moreover, discussions on segmentation are often reduced to debates over the definition of segmentation and whether the animal or system described is actually segmented, rather than to debates over the developmental mechanisms and evolutionary processes.

This inclusive definition should then be combined with an exact description of the segmented structures in the animals or systems being discussed, as well as a clearly stated hypothesis concerning the specific nature of the potential homology of structures. While we support a general definition of segmentation, it is also crucial that authors be explicit in what they are implying about ancestors and shared traits versus convergence, to facilitate the advancement of new ideas, versus circular discussions.

A broader definition of segmentation could also impact molecular studies. New studies on segmentation should examine multiple genes, since there is a wide range of molecular mechanisms involved in segmentation, even within groups with segmental homology. Advancements in sequencing technologies have made it possible to find and analyze many genes involved in the segmentation process simultaneously.

Moreover, these studies can yield an unbiased list of genes involved in segmentation in a particular organism or structure, as opposed to the candidate-gene approach used in the past. It will be exciting to see how broader knowledge about segmental molecular mechanisms impacts our thoughts on the core features of segmentation and the shared homology among segmented animals. The authors declare that they have no competing interests. No funding was received for this review.

RLH drafted the manuscript. NHP critically revised the manuscript. We thank Craig Miller and David Weisblat for discussions on the nature of segmentation.

We thank David Stafford and Craig Miller for helpful comments on the manuscript. National Center for Biotechnology Information , U. Journal List EvoDevo v. Published online Dec Author information Article notes Copyright and License information Disclaimer. Corresponding author. Roberta L Hannibal: ude. Received Jul 15; Accepted Nov This article has been cited by other articles in PMC. Abstract Animals have been described as segmented for more than 2, years, yet a precise definition of segmentation remains elusive.

Keywords: Evolution, Metamere, Pseudosegment, Segmentation. Why is the definition of segmentation important? Open in a separate window. Figure 1. The history of the definition of segmentation The Greeks first recorded the observation that some animals are made of segments, reiterated units along the anterior-posterior a-p axis. Current controversies in the field of segmentation While there is a general agreement that segmentation involves reiterated units along the a-p body axis, there are still a number of points of contention.

Can a segment be a single cell in a column of cells? Figure 2. Figure 3. Can a segment be composed of only one tissue layer? Is the tip of the arthropod head a segment? Figure 4. What parts of the vertebrate head are segmented? Conclusions Ideally, a precise definition of segmentation would facilitate our understanding of mechanisms of development, and inform our thoughts on evolutionary processes and events.

Competing interests The authors declare that they have no competing interests. Acknowledgements We thank Craig Miller and David Weisblat for discussions on the nature of segmentation.

References Goodrich ES. On the relation of the arthropod head to the annelid prostomium. Q J Microsc Sci. Oxford: Clarendon Press; Dougherty EC, editor. Berkeley: University of California Press; The evolution of the celom and metameric segmentation; pp. Dev Cell. Evidence for a clade of nematodes, arthropods and other moulting animals. Parallel evolution of segmentation by co-option of ancestral gene regulatory networks.

Segmentation, metamerism and the Cambrian explosion. Int J Dev Biol. The origin and evolution of segmentation. As a result, the exoskeleton must be much thicker to bear the pull of the muscles in large insects than in small ones, so there is a limit to how big an arthropod body can be. Another limitation on size is the fact that in many arthropods, including insects, all parts of the body need to be near a respiratory passage to obtain oxygen.

The reason for this is that the respiratory system, not the circulatory system, carries oxygen to the tissues. In fact, the great majority of arthropod species consist of small animals—mostly about a millimeter in length— but members of the phylum range in adult size from about 80 micrometers long some parasitic mites to 3.

Some lobsters are nearly a meter in length. The largest living insects are about 33 centimeters long, but the giant dragonflies that lived million years ago had wingspans of as much as 60 centimeters! Arthropod bodies are segmented like those of annelids, from which they almost certainly evolved. Individual segments often exist only during early development, however, and fuse into functional groups as adults. For example, a caterpillar a larval stage has many segments, while a butterfly and other adult insects has only three functional body regions—head, thorax, and abdomen—each composed of several fused segments.

Some of the segmentation can still be seen in the grasshopper, especially in the abdomen. About two-thirds of all named species on earth are arthropods. Scientists estimate that a quintillion a billion billion insects are alive at any one time— million insects for each living human!

Ponder this. Why don't annelids develop an exoskeleton and appendages as arthropods do? Why do some arthropods go through metamorphosis, while others remain unchanged throughout their life cycles? Divide groups to analyze the skeletal, muscular, circulatory, digestive, and any other principle systems of the human body. Discuss about segmentation in those systems. Details may include segmentation in the cellular, tissue, and organs of each bodily system and how the structure contributes to their function.

Further reading. Annelids , also known as the ringed worms or segmented worms, are a large phylum, with over 22, extant species. Annelid fossils , from the Virtual Fossil Museum. Arthropod fossils , from the Virtual Fossil Museum. Seth S. Thus while a posterior to anterior gradient of FGF is important for somitogenesis [ 5 ], this is not true of pharyngeal or hindbrain segmentation.

Another similarity lies in the identity of the segments being dependent on Hox genes, but this reflects the more general role of these genes in anteroposterior patterning of the body. Hox genes assign identity to segmented and unsegmented regions, such as the lateral plate mesoderm, alike. The segmentation of the paraxial mesoderm to generate individually packaged somites underpins the locomotory strategies of the vertebrates, resulting in the formation of separate bilateral bocks of muscle lying either side of an articulated backbone.

This arrangement is essential for lateral undulatory locomotion of fish and many tetrapods. In contrast, the segmentation of the hindbrain generates subdivisions within a contiguous region which allows for seamless connections between the different hindbrain nuclei and ongoing connections, and for through traffic that connects higher brain centres with the spinal cord.

Lastly, the segmentation of the pharynx relates to its activities in feeding and respiration. The two most anterior pharyngeal segments of the gnathostomes will contribute to the jaw apparatus and the more posterior segments will form gills with an abundant vasculature and thus perform respiratory functions. To further clarify the relationships between the vertebrate segmentation processes; somitogenesis, rhombomeric subdivisions of the hindbrain and pharyngeal arches, it is important to ask about their evolutionary origins.

Vertebrates are chordates and one defining feature of this phylum is the presence of segmented muscle blocks. We might therefore expect somitogenesis to be a shared characteristic of the chordates.

Yet somites are lacking in urochordates and while they do form in cephalochordates this process seems to be somewhat distinct from that described in vertebrates [ 51 ]. The more anterior somites in amphioxus form as bilateral pairs by enterocoelus evagination of the wall of the archenteron while the posterior somites form by schizocoely, alternating between the left and right sides.

It has also been shown that, while the very anterior somites are dependent upon FGF signalling, most of the other somites forming by enterocoely and those formed by schizocoely are FGF insensitive. However, the lineages leading to the extant representatives of the chordate subphyla diverged a very long time ago and thus ancestral characteristics may have been lost or obscured.

Moving outside the chordates, and considering other deuterostomes one cannot find evidence for somites. Thus, it is reasonable to assume that somitogenesis evolved with the chordates but has undergone major modification in the different chordate lineages. Gene expression studies in other chordates and in hemichordates have established that a region of the nervous system expressing anterior Hox genes, and thus homologous to the vertebrate hindbrain domain, exists in these groups [ 52 ].

There are, however, no indications that rhombomeres exist outside vertebrates. There is neither morphological nor molecular evidence to support segmentation of the nervous system in an analogous region.

For example, amphioxus has a single Krox20 gene but it is not expressed segmentally in the developing nervous system [ 53 ]. Pharyngeal segmentation is, however, relatively ancient. As with somites, pharyngeal gill slits are characteristic of the chordates and it is clear that the simple perforations of the pharynx seen in other chordates such as amphioxus are homologous to the endodermal segmentation of the vertebrate pharynx.

The pharyngeal pouches of vertebrates express a Pax-Six-Eya regulatory network as does the pharyngeal endoderm in amphioxus [ 54 , 55 ]. Recent results from the hemichordate Saccoglossus kowalevskii have shown that pharyngeal segmentation is likely to be a general feature of deuterostomes [ 57 ]. Furthermore, although echinoderms lack gill slits, this is likely to result from secondary loss as fossil evidence has shown that the earliest echinoderms were bilateral and did possess gill slits [ 58 ], which further indicates that pharyngeal segmentation is a characteristic of the deuterostomes.

An important point that emerges from this is that there was no ancestral process of segmentation that was co-opted by each of these processes. The three segmental systems of the vertebrates each arose de novo at different points during evolution Figure 2. The most ancient is pharyngeal segmentation, and that is a feature of the deuterostomes, with somitogenesis following with the emergence of the chordates and finally rhombomere formation and the evolution of the vertebrates.

The evolutionary history of segmentation in the vertebrate lineage. Three instances of segmentation are found in extant vertebrates that are conserved with different invertebrate groups. Pharyngeal segmentation can be dated to the deuterostome ancestor, while somitogenesis dates to the chordate ancestor and rhombomeric organisation of the hindbrain to the vertebrate stem.

There have been many discussions as to the evolutionary origin s of segmentation and there are two key issues here that must be confronted. The first is whether or not there is any evidence to support homology between the manifestations of segmentation seen in vertebrates with those displayed by other bilaterian clades.

Attempts to homologize between segmentation in vertebrates and that seen in arthropods and annelids, have been strongly affected by their time. In the late s and early s comparisons were invariably drawn between the mechanisms underpinning the segmentation of the hindbrain and those directing segmentation in Drosophila. Both involved specification via transcription factor hierarchies and both resulted in the formation of lineage restricted compartments.

However, as our molecular understanding of somitogenesis advanced it became more common to draw comparisons between that process and other modes of arthropod segmentation.

For example, it was noted that segmentation in spiders involves Notch and Delta signalling [ 59 ]. Yet, for both of these comparisons, our extensive knowledge of the developmental processes underpinning rhombomere formation and somitogenesis would indicate that the highlighted commonalities are but simply superficial similarities.

The mechanisms underpinning the segmentation of the Drosophila embryo are quite different from those in vertebrates. Drosophila segments are formed within a syncytium by a transcription factor cascade. While rhombomeres are formed via cell sorting, using Eph-ephrin signalling, lying downstream of a very different system of signalling molecules and transcriptional effectors.

Furthermore, rhombomeres evolved with the vertebrates Figure 2 ; they are clearly lacking in other deuterostomes, and thus it is unlikely that they could have a common origin with the segmental patterning systems of arthropods. The formation of somites and the segments of many arthropods do share the characteristic that they are generated sequentially and that this is tied to axis elongation.

But, as such, some of the shared features associated with somite formation and arthropod segmentation may indicate more general conserved bilaterian features, such as the involvement of a posterior wnt-secreting growth zone [ 60 , 61 ].

It is also very possible that the association between notch signalling and segments is the result of this very ancient signalling pathway becoming subservient to the segmentation processes in animals that organise their body plan in such a manner, and indeed as we have pointed out Notch signalling is not required for somite formation in vertebrates. Finally, it should be stressed again that somites are a chordate feature Figure 2 and are not found in other deuterostomes and thus it seems again unlikely that somitogenesis could have a common origin with any mode of arthropod segmentation.

The second issue is the relative paucity of segmentation within the bilateria and its implications. As Hannibal and Patel point out, if segmentation is difficult to evolve, this would suggest that it had a single origin but that it was subsequently lost by the great majority of animal phyla and only retained in a few [ 2 ]. One conclusion following from this hypothesis would be that segmentation is readily dispensable in the generation of a functional body plan.

By contrast, if segmentation is relatively easy to evolve then one would expect to observe unrelated, non-homologous, instances of segmentation in different phyla. Our discussion of the segmented systems of vertebrates would point us towards the latter option. We find that there is no single process of segmentation and, that in the lineage leading to the vertebrates, segmented structures evolved at least three times independently, in different germ layers and using different mechanics, at least three times.

Thus it would seem that it is relatively easy to evolve segmentation. Hannibal and Patel make the excellent point that there is no merit in talking about segmentation without being explicit about what is being discussed.

Thus with regards to segmentation in vertebrates, it is unhelpful to talk generally of segmentation and to lump together the processes of somitogenesis, rhombomere formation and pharyngeal arch development; these are chalk and cheese comparisons. It is more correct and useful to discuss how somites form, how rhombomeres emerge and how pharyngeal arches are generated.

Furthermore, as Hannibal and Patel note, it is incredibly difficult to arrive at a precise definition of segmentation and we would argue that this is because there is no single process of segmentation. Consequently, all definitions of segmentation are superficial; that is, repetition of structures along the main body axis - there is nothing deeper to be indicated.

An analogous situation is that of wings - what is a wing? It is a structure that allows an animal to fly. Wings are a feature of flies, birds and bats but the definition of a wing has to be superficial because it describes non-homologous structures. Thus, many of the problems that arise with the concept of segmentation, and that we have discussed here, ultimately reflect a problem of terminology. The names that we apply to biological processes do not necessarily indicate anything beyond being useful appellations.

Of course this is the problem of homoplasy and the only route to resolving this is to map any given biological process to the phylogeny. Tautz D: Segmentation. Dev Cell. Pourquie O: Vertebrate segmentation: from cyclic gene networks to scoliosis. Dubrulle J, Pourquie O: fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo.

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