Earthworms and millipedes are made of a dazzling series of repeated body parts known as segments. This nearly mathematical body architecture has driven dozens of biologists throughout the last centuries to investigate how segments are built during embryogenesis and how they evolved in the first place—a longstanding and highly debated topic in biology (Sedgwick 1884; Masterman 1899; Hyman 1951a; Clark 1963; Beklemishev 1969c; Willmer 1990). Although arthropods, annelids, and vertebrates are the only groups typically considered to be fully segmented (see caveats in Budd 2001), meticulous studies on comparative morphology have long recognized that repetitive traits are present in many other bilaterians—the group of animals with bilateral symmetry.

The rise of developmental genetics, and with it, the discovery of genes and signaling pathways that regulate segment formation, gave the topic a new breadth. The field revealed that common molecular players can be involved in the segmentation of animals as dissimilar as fruit flies and mice, fueling a debate about the segmental nature of the last common ancestor of bilaterians, and inspiring new perspectives on the homology and co-option of segmentation mechanisms (Kimmel 1996; De Robertis 1997, 2008; Davis and Patel 1999; Scholtz 2002; Balavoine and Adoutte 2003; Seaver 2003; Minelli and Fusco 2004; Tautz 2004; Blair 2008; Couso 2009; Chipman 2010; Arendt 2018).

These discussions, however, have largely revolved around the segmentation mechanisms uncovered in laboratory species such as the fruit fly, zebrafish, and mouse, where tools to unravel genetic and developmental details were available. Although we now comprehend these mechanisms with unprecedented detail, the sole comparison between such distantly related species is not sufficient to understand how segments evolved or how the body of the bilaterian ancestor was organized, because it is hard to distinguish inheritance from convergent evolution over long distance phylogenetic comparisons (Sanger and Rajakumar 2018). Therefore, it is crucial to investigate other related bilaterian groups and their repeated traits to better reconstruct the evolutionary steps that gave rise to the segmented body patterns of today (Budd 2001; Scholtz 2002; Minelli and Fusco 2004).

Fortunately, molecular tools as well as sequencing and imaging technologies are becoming more widely applicable to many groups traditionally outside the range of laboratory species. In addition, improved phylogenies of animal relationships are providing better grounds to map and infer character evolution (Dunn et al. 2014). These advancements lay the foundations to investigate the evolution of segmentation mechanisms in greater depth and in a wider diversity of groups. Nevertheless, a comprehensive overview about the diversity of repeated structures across bilaterians is still lacking.

Even though only a few groups have a segmental organization comparable to that of annelids, arthropods, and vertebrates, the vast majority of bilaterians shows some kind of segmental trait (Figure 9.1).

The most notable examples are tapeworms (i.e., parasitic flatworms) and mud dragons (i.e., kinorhynchs), whose adult bodies are not only subdivided into well- defined external segments, but their internal structures also follow a repetitive

Examples of segmental traits in bilaterians

FIGURE 9.1 Examples of segmental traits in bilaterians. Phylogenetic relationships based on recent data sets (Dunn et al. 2014; Kocot et al. 2017). Groups typically considered to be segmented (vertebrates, arthropods, and annelids) are depicted in the tree by a representative drawing. Groups highlighted in bold are illustrated on the right side in featured boxes.

organization. Other groups have a variable set of individual segmental traits—from the dorsal shells of chitons, to the cuticle annulation of nematodes, to the ovaries of nemerteans—which can occur in every organ system, such as the body wall, nervous system, musculature, gonads, or excretory system (Beklemishev 1969c; Willmer 1990; Scholtz 2002; Minelli and Fusco 2004; Schmidt-Rhaesa 2007; Blair 2008; Couso 2009; Hannibal and Patel 2013).

In this chapter, I review the segmental traits of non-segmented bilaterians— namely, every bilaterian group other than arthropods, annelids, and vertebrates— describing their morphology, the developmental processes that give rise to the segmental pattern at the cellular level, and, when available, the genetic interactions patterning these traits. Non-bilaterians are beyond the scope of this chapter even though they also exhibit serially repeated structures (see examples in Beklemishev 1969c).

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