Section I: The Diversity of Segmentation

1 Segmentation

Segmentation: A Zoological Concept of Seriality

Gerhard Scholtz

CONTENTS

• 1.1 Segments and Segmentation.............................................................................3
• 1.2 Segments and Series.........................................................................................6
• 1.3 Ontogeny of Seriality and Segmentation..........................................................8
• 1.4 Theories on the Evolution of Seriality and Segmentation..............................10
• 1.5 How Often Did Segments Evolve?..................................................................16
• 1.6 Problems with Structural Definitions of a Segment.......................................17
• 1.7 Problems with Ontogenetic Definitions of a Segment....................................18
• 1.8 Structural and Ontogenetic Segment Definitions Lead to Paradoxes.............19
• 1.9 Segments Do Not Form Spatial and Differential Units..................................19
• 1.10 Simple Anomalies Disturb the Pattern of Segmentation................................20
• 1.11 Criticism of the Term “Segment”...................................................................21

Acknowledgments....................................................................................................22

References................................................................................................................22

Segments and Segmentation

The physical organization of arthropods, annelids, and chordates is characterized by serially arranged body sections along the longitudinal axis that can be referred to as segments (Figure 1.1, top).^[1] In zoology, segments are generally understood to be integral units that are characterized with respect to structure, function, ontogeny, and evolution. According to this view, segments are seen as fundamentally different from other repetitive structures along the body axis (see later). Segmentation is thus considered constitutive for arthropods, annelids, and chordates, distinguishing these three groups from the numerous other unsegmented animals such as cnidarians, mollusks, flatworms, roundworms, and echinoderms, although these too display some serially arranged external and internal structures (Figure 1.1, bottom; also see Chapter 8).

FIGURE 1.1 Examples of segmented (top row) and unsegmented (bottom row) bilat- erians. A. Myriapod (Arthropoda), B. marine bristle worm (Annelida), C. fish (Chordata), D. polyclade fiatworm (Platyhelminthes), E. chiton (Mollusca), F. kinorhynch (Cycloneuralia). Chiton and kinorhynch exhibit a serial body arrangement that, however, is not interpreted as segmentation.

Depending on the animal group, segments are structurally characterized by the joint occurrence of a set of serially aligned internal and external elements such as mesodermal body cavities (coeloms), sexual organs, nephridia, nerve ganglia, muscular systems, extremities, and external rings (Scholtz 2002). In particular the serially arranged coeloms play a crucial role for this concept of segmentation. The comprehensive presentation of an elaborated coelom theory by Oskar and Richard Hertwig (1881) had a tremendous influence on the zoological thinking of the time, and the presence of a coelom was interpreted and used as the essential morphological, systematic, and evolutionary property. The coelom was regarded as identifying a more complex body organization and a higher evolutionary development. Accordingly, the presence of a serial coelom was for a long time the decisive and essential criterion in distinguishing between “true” segments and other serial structures (called pseudo- metameres) (for a current view of the coelom, see Rieger and Purschke 2005).

Ontogenetically, segments are differentiated from non-segments through their sequential formation from a posterior budding zone (see Scholtz 2002, 2010). The serially arranged sections of a tapeworm (proglottids), which also depict a series of repeated structures, would not be segments according to this definition, since they are formed from an anterior growth zone behind the head (see Scholtz 2010). In today’s age of molecular biology, the explanation of morphogenetic phenomena in development has shifted to the level of gene expression and gene regulation. Accordingly, the genes involved in forming the segments, especially the expression of segment polarity genes, are viewed as the key criterion for distinguishing between segments and other serial structures (e.g., Tautz 2004; Hannibal and Patel 2013).

The significance attributed to segmentation comes from a variety of sources. For one thing, aesthetic reasons play a role here. Serial structures are formed by figures translated onto themselves through shifting, thereby representing a special form of symmetry. This regularity, referred to as “translational symmetry,” has since antiquity formed a key aesthetic criterion, evidently having an appeal of its own, as confirmed by numerous examples in art and architecture (Figure 1.2) (Schramke 2017). The frequent use of anatomical terms such as ribs, legs, wings, or bodies in architecture even allows one to speculate that in addition to mathematical proportions,

FIGURE 1.2 Aesthetics of seriality in nature and culture. Whale skeleton in a gothic church building (German Oceanographic Museum, Stralsund).

knowledge of human and animal anatomies can be seen as a point of departure for forms of symmetry in artifacts. This certainly also applies for seriality in plants and animals, at least when they are not too long and comprise too many repeated elements. Mobius (1908, 36) used the examples of earthworms and millipedes, and wrote in his Asthetik der Tierwelt (Aesthetics of the Animal World): “Most (symmetrical animals) are comprised of sections, metameres, or segments in the direction of their longitudinal axis, from anterior to posterior. A large number of metameres is not pleasing. You see nothing new and become fatigued and bored.” Nevertheless, the aesthetic perspective on seriality also directly refers to its function, since the repetition of structural elements as a construction principle includes technical and economic aspects in addition to all questions of proportion and symmetry (see Riedl 1975). Finally, the observed structural repetition in segmentation represents an intellectual challenge. This concerns in particular the questions as to the evolutionary emergence and significance of segments. According to a popular view, segmentation forms a key characteristic that enabled and advanced the great evolutionary success of arthropods, annelids, and chordates. Thus, the arthropods—with more than one million species—are by far the most species-rich and biodiverse animal group; and the vertebrates include the human being, a species capable of reflecting on such problems.

The scientific literature on segments and segmentation is correspondingly vast (e.g., see reviews by Budd 2001; Scholtz 2002; Minelli and Fusco 2004; Tautz 2004; Seaver 2003; Deutsch 2004; Chipman 2008; Hannibal and Patel 2013; Altenburger 2016). From the problem of defining a segment to the ontogenetic and evolutionary emergence of segments, and finally to the role of segmentation for the evolutionary success of individual groups of animals, all aspects are being discussed, sometimes in a very heated, controversial manner. There is a particularly intense debate whether the segments of annelids, arthropods, and chordates are homologous and, therefore, if their last common ancestor was already segmented (e.g., Balavoine and Adoutte 2003).

This chapter discusses whether segmentation and segments are biologically meaningful concepts in order to understand the ontogenetic and evolutionary genesis and the modifications of repeated structures along the body axis, or if the term “segment” should instead be deconstructed and replaced by an emphasis on the concept of series and seriality of individual structures and processes.

• [1] Segments are often referred to in zoological literature as metameres. Some authors, however, use theterm “metamere” to refer only to the subdivision of the coelomic cavities, distinguishing it from theterm “segment” (Remane 1950). Accordingly, segmentation is considered a specific case of metamerism (see Schmidt-Rhaesa 2007.48).