Which Of The Following Animals Is Not A Segmented Worm?

What is a segment?

Roberta Fifty Hannibal

¹Departments of Molecular and Cell Biological science and Integrative Biology, University of California, 519A LSA #3200, Berkeley, CA 94720-3200, USA

²Present Address: Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, United states of america

Nipam H Patel

¹Departments of Molecular and Prison cell Biological science and Integrative Biology, University of California, 519A LSA #3200, Berkeley, CA 94720-3200, The states

Received 2013 Jul 15; Accepted 2013 Nov 19.

Abstract

Animals have been described as segmented for more than 2,000 years, however a precise definition of segmentation remains elusive. Here nosotros requite the history of the definition of division, followed past a give-and-take on current controversies in defining a segment. While there is a general consensus that sectionalization involves the repetition of units along the anterior-posterior (a-p) centrality, long-running debates be over whether a segment can exist composed of only ane tissue layer, whether the most anterior region of the arthropod head is considered segmented, and whether and how the vertebrate head is segmented. Additionally, we discuss whether a segment can be composed of a unmarried cell in a column of cells, or a single row of cells within a grid of cells. We suggest that 'partition' be used in its more general sense, the repetition of units with a-p polarity along the a-p axis, to prevent artificial classification of animals. We further advise that this general definition be combined with an exact description of what is being studied, as well as a clearly stated hypothesis concerning the specific nature of the potential homology of structures. These suggestions should facilitate dialogue amongst scientists who report vastly differing segmental structures.

Keywords: Evolution, Metamere, Pseudosegment, Partitioning

Why is the definition of sectionalization important?

'The merely dogmatic argument we are justified in making is, that when a region exhibits during evolution a sufficient number of the essential structures of a typical segment, information technology may exist assumed to exist at true metamere. What is "sufficient" has to exist decided in each instance.' ES Goodrich, 1897 [i]

'It is hard to find a [concept] in the whole of zoology that is so vaguely defined, but, at the same time, so universally employed equally…metamerism.' RB Clark, 1964 [2]

Arthropods, annelids, and chordates are some of the most successful and diverse animate being groups, as defined by species number and anatomical complexity. The success of these groups may be due to their segmented trunk region, which may enhance locomotion and feeding [ii-four]. While these groups share the trait of trunk segmentation, it is controversial whether partitioning is homologous, since these groups are more closely related to unsegmented phyla than to each other (Figure1A) [v-11]. If segmentation is difficult to evolve, the about parsimonious explanation for three unrelated segmented groups would be that segmentation evolved one time, just was subsequently lost in all taxa related to the arthropods, annelids, and vertebrates. In this instance, we would expect to detect prove of loss of segmentation in related groups. Conversely, if division is like shooting fish in a barrel to proceeds, we would expect to find multiple unrelated segmented taxa. In fact, there may be such evidence in modern and fossil taxa, as there are a number of groups besides the arthropods, annelids, and vertebrates that display serially repeated units, and could therefore exist considered segmented (Effigy1B) [7,12,13]. Still, in order to use these groups to infer the evolutionary history of segmentation, nosotros must outset resolve whether these taxa are actually segmented. The main obstacle in resolving this issue is that in that location is no precise definition of division. Instead, at that place is a range of definitions, depending on what animals and what parts of these animals were studied by a detail author. Here, we give an overview of the various definitions of segmentation, and we talk over current controversies in defining a segment.

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Phylogenetic human relationship among segmented and unsegmented phyla. Phylogeny of bilatarians based on [14]; segmented and pseudosegmented animals identified after [7,12,13]. (A) Segmented phyla (yellowish stars) are more closely related to unsegmented phyla than to each other. (B) Segmentation is no longer a rare characteristic if both segmented and pseudosegmented phyla are considered (cerise stars mark groups identified as segmented or pseudosegmented in several papers, orange stars mark groups identified as segmented or pseudosegmented in 1 paper and unsegmented in another). Hither, 'pseudosegmented' is meant solely to distinguish traditionally segmented chordates, arthropods and annelids from other phyla with repetition of units with anterior-posterior polarity forth the anterior-posterior centrality. It does not necessarily mean that there is a biological distinction between these groups based on their repeated units.

The history of the definition of segmentation

The Greeks beginning recorded the observation that some animals are fabricated of segments, reiterated units forth the anterior-posterior (a-p) axis. Aristotle [fifteen] named and classified a group of animals as 'insects' , because of their segmental nature. Entomon ('insect' in Greek) is derived from the Greek word entomos, pregnant 'to cut up' , and was used because these animals had 'nicks' or 'cuts' on their back or bellies, corresponding to boundaries betwixt segments. Latin and related modern languages continued this theme, as the English word 'insect' is derived from the Latin insecure, which also means 'to cut upwardly'.

The scientific revolution of the seventeenth century brought scientific discipline to the forefront of Western society and fix the stage for renewed interest in segmentation in the nineteenth century. During the 1800s, Cuvier grouped arthropods and annelids into the now defunct taxon Articulata because of their similar segmental morphologies [16]. Goodrich as well considered arthropod and annelid segments homologous. From studies on arthropods and annelids, Goodrich defined a segment as a unit, marked off from the balance of the body by transverse grooves, containing a mesodermal hollow space (coelom), a pair of nephridia (excretory glands), and a pair of ventral ganglia [one]. Goodrich also noted that, in polychaetes and arthropods, a segment also contains a pair of appendages. Besides these morphological characteristics, Goodrich used a developmental feature, the sequential improver of segments from inductive to posterior, to define segmentation.

Goodrich'due south definition does not accurately describe all segments. As Goodrich acknowledged, segments containing all of the to a higher place criteria are rarely found, although some features tin transiently exist seen during development [1]. Also, Goodrich'south definition excludes sectionalization in the arthropod Drosophila and in the chordates. In Drosophila, segments are formed by simultaneously subdividing the unabridged body, in contrast with Goodrich's developmental requirement of adding segments from the posterior end [1,17]. In chordates, segments are added progressively from the posterior, just they do not take a number of Goodrich's other morphological characteristics [18]. Some other caveat to Goodrich's definition is that if the formation of reiterated structures is linked, then using all of them to define a segment would exist no more informative and then using one of them [19]. For example, segmentation of the coelom, nephridia, and ganglia might all be based on the aforementioned molecular pattern. Then, since all iii traits would be a read-out of the same pattern, any or all of them could be used equivocally to define that segmental pattern.

Effectually the same time as Goodrich, Bateson defined segmentation as a 'more-or-less' coincident repetition of elements from many organ systems along the a-p body axis [20]. Unlike Goodrich, however, Bateson did non define what these elements had to exist, and based his definition on trunk segmentation in vertebrates, as well as segmentation in arthropods and annelids. While Bateson'southward definition is applicable to body segmentation in the arthropods, annelids and chordates, many scientists prefer a more precise definition.

While segments tin be thought of as the repetition of a variety of structures, Clark suggested that reiteration of coelomic sacs and accompanying musculus was the defining characteristic of a segment [2,3]. The coelom is a fluid-filled body cavity derived from the mesoderm. Clark suggested that segmentation involving the coelom and muscles has evolved because of the need for better locomotion, as a big, unsegmented, coelomic sac would have impeded movement. Clark proposed that the division of the coelom facilitates move by allowing the body to bend at the regions between compartments and that this partition of the coelom is accompanied by musculus sectionalization.

Clark's theory could potentially explain the advantage of partitioning in the arthropods, annelids, and chordates, since segmentation could have evolved for improved locomotion in all of these groups. Even so, segmentation does not seem to be correlated with any kind of locomotion. Clark himself best-selling that ribbon-like animals swim in the same manner whether they are segmented or non, although he suggested that extant animals might not exist skillful representatives of the ancestors of segmented phyla [2]. Like swimming, burrowing does not correlate with division, since many burrowing worms are not segmented [xiii,21].

Another caveat to Clark's theory is DuPorte'due south [22] argument that, 'In that location is no existent foundation for the belief in a primal relation betwixt coelomic sacs and metamerism.' DuPorte suggests that coelomic sacs may exist a phase in mesoderm differentiation and therefore does not have a straight relationship to segmentation. He based this on the observation that protostome mesoderm originates as a solid mass, but only differentiates into coelomic sacs after this mass has already been divided into segments. Clark'due south definition of partitioning has also been used sparingly in modern times, perchance because of the emergence of the arthropod ectoderm equally a model for segmentation. Experimental evidence suggests that, in arthropods, the ectoderm can segment unremarkably without the mesoderm [23-27].

Assay of modern molecular data has also failed to produce a concise definition of segmentation. Instead of finding a few genes and mechanisms that could be used to define segmentation, studies have yielded a large number [28]. Even when homologous genes or gene families are involved in sectionalisation, they often play different roles in dissimilar animals [viii,11,29]. For example, although members of the Notch, Wnt, and fibroblast growth gene signaling pathways oscillate to produce segmental torso mesoderm in mouse, chick, and zebrafish, the individual genes that oscillate differ between species [29]. This may be only a minor difference, in that it might not affair which component of the pathway oscillates, as long as some components oscillate [10]. Major differences are also found, particularly among different species of arthropods. Inside arthropods, there are multiple changes in which genes appear to be involved in segmentation, and, unlike many other arthropods and vertebrates, Drosophila does not have any evidence of Notch or other oscillators (for case, see [30-33]). Moreover, morphologically similar segments tin be formed by different developmental and molecular mechanisms in the same animal. For example, although all of the somites, segmental units in vertebrate trunk mesoderm, appear morphologically homologous in zebrafish, there is variation in how they form, depending on their position along the a-p centrality [34]. The evolution of the anterior trunk, posterior body, and tail somites depend on different genes or take dissimilar degrees of dependence on the aforementioned genes, or both. Instead of yielding a precise definition of a segment, modern molecular studies accept highlighted the complexity of segmentation.

Current controversies in the field of segmentation

While at that place is a full general understanding that partitioning involves reiterated units along the a-p body axis, there are still a number of points of contention. The major debates surrounding the definition of a segment are: (1) whether a segment tin can be composed of only one tissue layer, (ii) whether the anterior arthropod head is considered segmented, and (three) whether and how the vertebrate head is segmented. An additional complicating gene for defining partition is whether a segment can be composed of a unmarried cell in an a-p column of cells, or a single row of cells within a filigree of cells. We will discuss this issue first, as it has bearing on the contentions over segmentation in the literature.

Can a segment be a single cell in a column of cells?

During development, some animals have an arrangement of cells along the a-p axis in which each single cell (or row of unmarried cells) could be considered a segment. For example, the notochord of the sea squirt Ciona savignyi is composed of a single column of cells (Figure2A) [35]. Similarly, the trunk of the arthropod Parhyale hawaiensis, too as the trunks of other malacostracan crustaceans, is composed of columns of cells where segments arise from single-prison cell-broad rows within a grid of cells (Figure2B,C) [36-38]. For a column of cells along the a-p axis to be considered a column of segments, each prison cell or row of cells needs a definable inductive and posterior (Figure3A,B) [39]. Having an anterior and a posterior distinguishes each cell from its neighbors, while making each cell a reiteration of a unit of measurement. In segments composed of ii or more than rows of cells, an a-p segmental design can be accomplished by having different morphology or cistron expression in anterior versus posterior rows of a single segment (segment polarity). In segments composed of only a single jail cell, or that are but a single cell broad, the anterior and posterior of the single cell must exhibit molecular or morphological a-p asymmetry (jail cell polarity).

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A single cell (row) may be a segment. (A) Lateral view of a Ciona savignyi late tailbud-stage embryo where the notochord is equanimous of a column of unmarried cells (yellowish). The planar-cell polarity proteins Prickle and Strabismus (orange) are located at the inductive and the nucleus (blue) is located at the posterior of each prison cell. (A after [35].) (B, C) Segmentation in the trunk of Parhyale hawaiensis. Left side of the embryo is depicted, right side is mirror epitome. Red arrows correspond progression in fourth dimension. (B) In one case ectodermal cells condense into rows (PSPRs), each PSPR divides to produce ane parasegment of ectoderm. After the showtime PSPRs segmentation, Ph-hedgehog (Ph-hh, orange) is expressed in the anterior row (row a/b) [40]. After the second division, both En and Ph-hh (carmine) are expressed in the anterior row (row a) [36]. While the division of one PSPR produces one parasegment of ectoderm, in general, one segment's worth of ectoderm (bracket) forms from the Engrailed (En) negative cells of one parasegment (rows b to d), and the En positive cells from some other parasegment (row a) [36]. (C) 1 row of mesoblasts produces one segment's worth of mesoderm (bracket). Afterwards the outset mesoblasts sectionalisation, Ph-twist (greenish) and Ph-even-skipped (purple) are expressed in a subset of the inductive daughters [27,37,40]. (D) Segmentation in the leech ectoderm. One side of the embryo is depicted, other side is mirror prototype. The ectoderm is formed from the progeny of four ectoteloblasts, N, O, P, and Q, [41]. Each progeny, or blast cell (greenish), of O and P gives rise to one segmental unit of measurement. However, 2 adjacently produced blasts cells from Northward and Q, ns (xanthous) and nf (bluish) and qs (xanthous) and qf (blue), respectively, give rise to i segmental unit. a, anterior; p, posterior, PSPR, parasegment forerunner row.

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A segment tin can be equanimous of one or more tissue layers. Subclass marks one cell or segment, except in (A), where it marks one putative prison cell or segment. (A) Yellowish circles represent cells (putative segments) in i layer of tissue. (B) Each cell in a column of cells tin can be called a segment if there is a-p jail cell polarity in each cell. Cells (circles) now have a-p jail cell polarity, represented by difference in coloration from yellowish (anterior) to carmine (posterior). (C, D) Segments are ofttimes defined as having reiterated units (segments) equanimous of derivatives of both mesoderm (yellow-red circles) and ectoderm (yellowish-blue (C) and blue (D) circles). Each dorsal-ventral row of cells forms one segment. (C) Both the mesoderm and the ectoderm take a-p cell polarity, represented by deviation in coloration. (D) Merely the mesoderm (xanthous-red) has intrinsic a-p cell polarity. The ectoderm (blue), does not have reiterated pattern on its own, but does contribute to the segmental pattern of each segment equally a whole, since it is associated with the anterior of each segment. a, anterior; p, posterior.

The most obvious molecular machinery to distinguish the anterior from the posterior of cells is the planar-cell polarity pathway. Indeed, expression of members of this pathway supports the hypothesis that each prison cell in the notochord of the sea squirt Ciona savignyi is a segment (FiguretwoA) [35]. By expressing tagged Ciona Prickle and Strabismus proteins, Jiang et al. [35] revealed localization of these proteins at the anterior edge of each notochord cell. Additionally, they found that each notochord nucleus is asymmetrically positioned nigh the posterior of each cell. These information bear witness that each Ciona notochord cell has a-p cell polarity, supporting the classification of the Ciona notochord as segmented, with the segmental units beingness single cells along the a-p axis.

Unlike Ciona, a-p prison cell polarity has not all the same been found in the torso of the malacostracan arthropod Parhyale hawaiensis during the stage where segments, or more accurately for the ectoderm, parasegments, are destined to form from single-prison cell-wide rows of cells within a grid of cells. Parhyale segments are composed of both ectoderm and mesoderm. In the trunk, ectodermal parasegments grade via the division of parasegment precursor rows (PSPRs), while mesodermal segments class via the segmentation of mesoblasts, which are produced via the asymmetrical division of mesodermal stem cells (mesoteloblasts; Figure2B,C) [36,37]. In Parhyale, each parasegment/segment has polarity later on the beginning partitioning of the PSPRs and mesoblasts, equally there is differential gene expression in the anterior versus posterior row of each segment (Figure2B,C) [27,37,40]. It will be interesting to determine whether a-p polarity is established before PSPR and mesoblast division, as well as what molecular pathways govern this patterning. Equally both cell types divide forth the a-p axis, there may be intrinsic asymmetric determinants, and therefore a-p cell polarity, in the PSPRs and mesoblasts. Alternatively, the PSPRs and mesoblasts may only take intrinsic instructions for dividing in an a-p orientation, and so require subsequent signaling from the inductive of the embryo to distinguish the anterior daughter from the posterior girl.

The discovery of molecular markers of a-p polarity in Parhyale segmental precursor cells will as well resolve the question of whether segmental precursor cells are segments if they practise not divide. If the ectoderm is ablated in Parhyale, mesoteloblasts withal divide to form mesoblasts [27]. However, these mesoblasts do non divide nor practice they limited known markers of segment polarity normally seen later on the offset mesoblast sectionalisation. If these mesoblasts accept a-p cell polarity, they would be segments, and segmentation of the ectoderm and mesoderm could be considered to occur independently of i some other. If private mesoblasts are not considered segments because they lack a-p polarity, then the mesoderm requires either a permissive or an instructive signal from the ectoderm to proceeds segmental identity. An instructive signal from the ectoderm would further complicate the debate on defining a segment. If the ectoderm is required to impart a segmental blueprint onto the mesoderm, and so segmentation in Parhyale could be seen as simply an ectodermal characteristic, and the general definition of sectionalisation would then include that the segmental pattern must be an intrinsic property of the germ layer being studied. We do not propose using intrinsic pattern as a criteria for segmentation, as gathering this level of information would make it hard, if not impossible, to define even universally agreed upon segmental tissue every bit segmented.

As with malacostracan arthropods, segments in annelids can form from single-cell-wide precursors. In the leech, segments class from the asymmetrical division of teloblasts (Figure2D) [41]. On either side of the torso, progeny of four ectoteloblasts, Due north, O, P, and Q, and one mesoteloblast, M, come together to class a segment. Each progeny, or blast cell, of Thou, O, and P gives rise to 1 segmental unit. Although, dissimilar the malacostracan Parhyale, where a single-cell-wide row of cells gives ascent to one segment/parasegment, in the leech, the progeny of each blast cell can spread over more one segment and intermix with progeny of neighboring blast cells. Moreover, for the leech teloblasts N and Q, two adjacently produced blast cells give rise to i segmental unit. N alternatively gives ascent to the blast cells ns and nf, while Q alternatively gives rising to qs and qf [41,42]. These alternate blast cells accept unlike fates, as ns gives rise mostly to inductive neurons and epidermis, while nf gives rise to mostly posterior neurons, peripheral neurons, and neuropil glia, and qs gives rise to both ventral and dorsal cells, while qf only gives rise to dorsal cells [42]. Experiments with the more tractable Due north lineage support the hypothesis that ns and nf are different from birth. Ablation experiments indicate that ns and nf are non an equivalence group [42]. Additionally, molecular segment polarity is found in the progeny, as the activated class of the cell cycle poly peptide Cdc42 is expressed in higher levels in ns versus nf [43]. These data suggest that N, and by extension, Q, produce segments with intrinsic segmental polarity. Therefore, the N and Q lineage provide a model for further studies on how teloblasts may impose intrinsic segmental polarity on their progeny. It will be interesting to explore whether N and Q use like mechanisms equally the single progeny teloblasts Yard, O and P, and also as teloblasts in other systems such as the malacostracans.

The vertebrate trunk axons are an excellent example of how segmental pattern can be non-intrinsic. Vertebrate trunk axons are arranged in a reiterated pattern along the a-p axis. These axons contribute to the overall segment polarity within each trunk segment by running through the anterior one-half of each somite [44]. However, the segmental arrangement of axons is extrinsic, caused by axon guidance cues in the anterior half of the somite. Therefore, the segmental blueprint of axons is purely dependent on the polarity of the somites. These information suggest that body axons must be considered with the somites in order to exist segmental.

Can a segment be composed of only 1 tissue layer?

The arthropods, annelids, and chordates are universally considered segmented. Even so, in that location are a number of other beast groups that as well brandish serially repeated units, and could therefore also be considered segmented (Figure1B) [7,12,13]. To distinguish these serially repeated units from undisputed segments, these units are oftentimes called pseudosegments or metameres, depending on the author [7,12,13]. Here, we will use 'pseudosegments' to refer to these structures, every bit 'metameres' has ofttimes been used as a synonym for segments (for example, [i]).

While the merely difference between the pseudosegmented and segmented animals may be taxonomic classification, ane possible biological difference could exist that the arthropods, annelids, and chordates are the but groups with segments composed of both ectodermal and mesodermal derivatives. Segments in arthropods and annelids are derived from both the ectoderm and mesoderm and have segmental pattern in both tissue layers (FigureiiiC) [11,25]. In vertebrates, although trunk segments are equanimous of both the ectoderm-derived nervous system and the mesoderm, there is just segmental pattern in the mesoderm (EffigyiiiD). In that location is pattern in the ectoderm-derived rhombomeres of the vertebrate head, but, every bit at that place is contention about the segmental status of rhombomeres, they volition be discussed in more than depth in a later section.

Some pseudosegmented animals have reiteration only in the ectoderm, but at that place are other then-chosen pseudosegmented animals with reiterations in both the ectoderm and the mesoderm. The bdelloid rotifers, some species of nematodes, and chiton, a type of clam, only accept reiteration in the ectoderm [12]. Bdelloid rotifers have repeated rings of intraepithelial skeletal laminae, some species of nematodes have repeated cuticular rings, and chitons have reiterated dorsal plates. However, other so-called pseudosegmented animals take reiterations in both the ectoderm and the mesoderm. The bodies of kinorhynchs are composed of 13 to 14 units with repetitive ganglia, muscles, and epidermal and cuticular structures [12]. Therefore, the criteria of segments being composed of both ectoderm and mesoderm is not sufficient to separate 'classically' segmented and so-called pseudosegmented animals. Moreover, equally at that place are many invertebrate animals whose development and anatomy are all the same not well characterized, there are likely to be more than species that accept segmental pattern in at least one tissue layer. More information on pseudosegmented animals will also aid decide whether there is an actual distinction between reiterated structures in segmented versus pseudosegmented phyla.

An evolutionary argument also suggests that requiring segments to be composed of both ectodermal and mesodermal derivatives, versus one tissue layer, is an artificial distinction [45]. According to Budd [45], instead of considering segmentation as a property of the entire animal, division should exist thought of every bit a property of an organ system. Budd defines segmentation as a characteristic of organ systems, because he views the evolution of division as a gradual aggregating of reiterated organ structures. If one organ system becomes reiterated commencement and another organisation becomes reiterated afterwards in evolution, and so the distinction between having multiple reiterated structures, or segments, and having just one reiterated structure, or pseudosegments, is artificial. Therefore, any reiterated organ system should be considered segmented, and there would be no reason to consider the segmented organ systems of arthropods, annelids, and chordates as singled-out from the segmented organ systems of pseudosegmented animals.

Just as segmentation could evolve in 1 organ system at a fourth dimension, partition could too exist secondarily lost in i organ system only not another. Show 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 human relationship. Notwithstanding, recent phylogenies place them within the annelids [47,48]. Moreover, immunohistochemical analysis of neuronal markers shows that the nervous organization 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 nearly segmental characteristics. As with the example of Echiura, partitioning may have been secondarily lost in some mollusks. The cephalopods are considered to be unsegmented. However, contempo phylogenies group them with the Monoplacophorans, shelled deep-bounding main mollusks that have the segmental characteristics of serially repeated gills, nephridia, and muscles [49,l]. While these data could suggest that Monoplacophorans independently evolved sectionalisation, closer exam 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 tin be interpreted as secondary simplification from a segmented ancestor. These examples of probable secondary loss of sectionalization in annelids and mollusks propose that there is no biological stardom between segments composed of many versus 1 organ system, and therefore argue against the requirement that segments be composed of multiple tissue layers.

Is the tip of the arthropod head a segment?

While most of the arthropod body is universally considered segmented, controversy exists over whether the inductive-most section of the caput is a segment, and the segmental amalgamation of appendage-like structures, such as the labrum [52]. As at that place are general reviews of these subjects elsewhere [52,53], nosotros 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 information technology contains the brain and does not bear a set of antennae or other appendages (Figure4A) [52,53]. Still, the ocular lobe also has many morphological similarities to the rest of the segments, making information technology hard to classify as either unsegmental or segmental [22,52,53]. The difficulty in using morphology to allocate 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 every bit 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 (FigurefourB,C) [one,52]. The annelid prostomium lies in front of the mouth and contains the encephalon and sense organs. The prostomium is considered unsegmented because its embryonic origin is different from the segmented trunk and because it does non accept characteristics of other segments, such equally coelomic sacs and nephridia [52]. Additionally, in annelid species that accept a trochophore larvae, the prostomium (episphere), is located anterior to the start ciliary ring (prototroch). If the annelid prostomium and the arthropod ocular lobe were homologous, then, based on annelid information, the ocular lobe would not be considered a segment. Still, since the new molecular phylogeny places the arthropods and annelids in two dissever 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].

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Annelid, arthropod, and vertebrate heads. (A) The segmental nature of the inductive region, or ocular lobe, of the arthropod head is disputed (orange). Ventral view of a 96-hour Parhyale embryo. Definitively segmented head segments are shaded in gray (antennae ane, 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 afterward [54]). (D) Vertebrates have head structures with segmental characteristics, such equally the rhombomeres (crimson) and pharyngeal arches (blue). Lateral view of the inductive region of a 24-hr zebrafish embryo, head slightly curved ventrally. a, inductive; p, posterior.

While molecular information likely resolved the human relationship betwixt arthropods and annelids, molecular studies take non notwithstanding 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 bagginess genes is limited to one, often transient, region per ocular lobe, unlike other segments, where at that place is a persistent domain of stiff expression. This may be due to the highly derived nature of the head, or, since these genes are all pleiotropic, this may betoken a fundamental difference in the ocular lobe versus the undisputed segments of the residue of the torso. 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 most head homology had not been questioned.

What parts of the vertebrate head are segmented?

Vertebrates have structures in their heads that could be considered segmental, merely that are distinct from their trunk segments. Controversy exists on whether these head structures are segmented as they do non hands fit into the already tenuous definition of segmentation formed from studies on body segments. Moreover, researchers accept 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 near probable to exist segmented, here nosotros 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 piddling 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, equally their being would advise that the head and trunk share a unified segmental developmental program. However, there is but disputed scanning electron microscope data to back up their beingness, 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 [seventy,71]. Nevertheless, while the forebrain may be partitioned, there is neither repeated morphological pattern nor molecular segmental polarity to back up segmentation.

Hox gene expression has frequently been used to support the claim that the vertebrate head is segmented (for example, encounter [63,67]). Hox gene expression oftentimes correlates with inductive segmental or parasegmental boundaries and Hox proteins decide what type of structure will class from each segment [72,73]. Nevertheless, this does not imply that Hox genes are a marker of segmentation and, therefore, Hox expression should not be used to ascertain a body region, such as the caput, as segmented. In support of not equating nested Hox gene expression to sectionalisation, knock-out, and overexpression of Hox genes alters segment identity, merely practise non preclude the formation of segments [72,73]. Moreover, many unsegmented animals limited Hox genes along their a-p axis only are not segmented, no matter what definition is used (for example, see [74,75]). Although conspicuously of import for patterning segmental structures, Hox gene expression past itself should non exist used as molecular prove of sectionalization.

While more evidence is needed to back up many of the claims for segmentation in the vertebrate caput, at that place is morphological and molecular testify to back up 2 structures, the rhombomeres and pharyngeal arches, as segmented (Figure4D) [66]. The rhombomeres are seven transient compartments in the chordate hindbrain that command neural system 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-dominion genes in Drosophila, each segment in Drosophila ultimately has its ain segment polarity [17]. In that location is still polarity in each rhombomere, nonetheless, since motor neurons and their axon trajectories have a repeated pattern in each rhombomere [68].

Pharyngeal arches as well have segmental characteristics. The pharyngeal arches are bulges on the lateral surface of the embryonic caput 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 information suggest that pharyngeal arches are segmented.

Despite their segmental characteristics, rhombomeres and pharyngeal arches are ofttimes non considered in comparisons of sectionalization among the arthropods, annelids, and chordates. Perhaps this is considering rhombomeres and the neural crest component of pharyngeal arches are vertebrate innovations, and therefore do not accept 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, like 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 division. Equally vertebrate innovations, they are particularly interesting as models of segmental evolution in novel structures.

Conclusions

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 ii millennia of studying segmentation in animals have failed to produce a definition of segmentation that is applicative in fifty-fifty a majority of cases. Moreover, discussions on segmentation are often reduced to debates over the definition of partition and whether the beast or system described is really segmented, rather than to debates over the developmental mechanisms and evolutionary processes.

To bring the focus back to developmental and evolutionary biology, we suggest that 'sectionalization' be used in its near general significant: the repetition of units along the a-p axis, where each unit has a-p polarity [twenty,45]. This inclusive definition should and so exist combined with an verbal clarification of the segmented structures in the animals or systems existence discussed, as well as a clearly stated hypothesis concerning the specific nature of the potential homology of structures. While we back up 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 round discussions.

A broader definition of sectionalization could besides impact molecular studies. New studies on partitioning should examine multiple genes, since there is a wide range of molecular mechanisms involved in sectionalisation, fifty-fifty within groups with segmental homology. Advancements in sequencing technologies have fabricated information technology possible to find and analyze many genes involved in the sectionalisation 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 arroyo used in the past. It will be exciting to encounter how broader knowledge about segmental molecular mechanisms impacts our thoughts on the core features of partition and the shared homology among segmented animals.

Abbreviations

a-p: anterior-posterior; En: Engrailed; Ph-hh: Parhyale-hedgehog; PSPR: Parasegment forerunner row.

Competing interests

The authors declare that they have no competing interests. No funding was received for this review.

Authors' contributions

RLH drafted the manuscript. NHP critically revised the manuscript. RLH and NHP read and canonical the final manuscript.

Acknowledgements

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.

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