What is a segment?

Abstract

Animals have been described as segmented for more than 2,000 years, yet a precise definition of segmentation remains elusive. Here we give the history of the definition of segmentation, followed by a discussion on current controversies in defining a segment. While there is a general consensus that segmentation involves the repetition of units along the anterior-posterior (a-p) axis, long-running debates exist over whether a segment can be composed of only one 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 single cell in a column of cells, or a single row of cells within a grid of cells. We suggest that 'segmentation' 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 suggest 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 among scientists who study vastly differing segmental structures.

Figure 1

Phylogenetic relationship among segmented and unsegmented phyla. Phylogeny of bilatarians based on [14]; segmented and pseudosegmented animals identified after [7,12,13]. (A) Segmented phyla (yellow 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 (red stars mark groups identified as segmented or pseudosegmented in several papers, orange stars mark groups identified as segmented or pseudosegmented in one paper and unsegmented in another). Here, ‘pseudosegmented’ is meant solely to distinguish traditionally segmented chordates, arthropods and annelids from other phyla with repetition of units with anterior-posterior polarity along the anterior-posterior axis. It does not necessarily mean that there is a biological distinction between these groups based on their repeated units.

Figure 2

A single cell (row) may be a segment. (A) Lateral view of a Ciona savignyi late tailbud-stage embryo where the notochord is composed of a column of single cells (yellow). The planar-cell polarity proteins Prickle and Strabismus (orange) are located at the anterior and the nucleus (blue) is located at the posterior of each cell. (A after [35].) (B, C) Segmentation in the trunk of Parhyale hawaiensis. Left side of the embryo is depicted, right side is mirror image. Red arrows represent progression in time. (B) Once ectodermal cells condense into rows (PSPRs), each PSPR divides to produce one parasegment of ectoderm. After the first PSPRs division, Ph-hedgehog (Ph-hh, orange) is expressed in the anterior row (row a/b) [40]. After the second division, both En and Ph-hh (red) 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 another parasegment (row a) [36]. (C) One row of mesoblasts produces one segment’s worth of mesoderm (bracket). After the first mesoblasts division, Ph-twist (green) and Ph-even-skipped (purple) are expressed in a subset of the anterior daughters [27,37,40]. (D) Segmentation in the leech ectoderm. One side of the embryo is depicted, other side is mirror image. The ectoderm is formed from the progeny of four ectoteloblasts, N, O, P, and Q, [41]. Each progeny, or blast cell (green), of O and P gives rise to one segmental unit. However, two adjacently produced blasts cells from N and Q, ns (yellow) and nf (blue) and qs (yellow) and qf (blue), respectively, give rise to one segmental unit. a, anterior; p, posterior, PSPR, parasegment precursor row.

Figure 3

A segment can be composed of one or more tissue layers. Bracket marks one cell or segment, except in (A), where it marks one putative cell or segment. (A) Yellow circles represent cells (putative segments) in one layer of tissue. (B) Each cell in a column of cells can be called a segment if there is a-p cell polarity in each cell. Cells (circles) now have a-p cell polarity, represented by difference in coloration from yellow (anterior) to red (posterior). (C, D) Segments are often defined as having reiterated units (segments) composed of derivatives of both mesoderm (yellow-red circles) and ectoderm (yellow-blue (C) and blue (D) circles). Each dorsal-ventral row of cells forms one segment. (C) Both the mesoderm and the ectoderm have a-p cell polarity, represented by difference in coloration. (D) Only the mesoderm (yellow-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 as a whole, since it is associated with the anterior of each segment. a, anterior; p, posterior.

Figure 4

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 96-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 24-hour zebrafish embryo, head slightly curved ventrally. a, anterior; p, posterior.