Segmentation, a question of boundaries

Read the previous section: Spiral cleavage, an oblique matter.

Annelids, arthropods and vertebrates show a remarkable morphological diversity (Chipman, 2010). Beneath this multiplicity of shapes and forms lies a common pattern of body organization—a trunk divided into repeated parts. This pattern and the developmental process that generates it are known as segmentation (Minelli and Fusco, 2004). While the vertebrate trunk is divided into somites¹ (a portion of the mesoderm), the body of annelids and arthropods is divided into intricate repeated compartments spanning the ectoderm and mesoderm—the segments (Scholtz, 2002). The morphological similarity between these body segments previously was taken as support for a kinship between Annelida and Arthropoda, in a group called Articulata (Scholtz, 2002; Seaver, 2003). In this scenario, segmentation would have evolved only once in the protostomes and once in the deuterostomes (Davis and Patel, 1999; Peel and Akam, 2003; Seaver, 2003).

Analyses arising from the area of molecular phylogenetics have disputed the monophyly of Articulata, suggesting that annelids and arthropods occupy different branches of protostomes, the Lophotrochozoa (=Spiralia) and Ecdysozoa, respectively (Aguinaldo et al., 1997; Eernisse, 1998). This phylogenetic hypothesis indicates that annelids and arthropods are more closely related to groups without body segmentation than to each other (Seaver, 2003); a topology that favors the independent evolution of annelid and arthropod body segmentation, in addition to the independent evolution of the different segmented tissues of vertebrates (Graham et al., 2014). Subsequent phylogenetic studies continue to corroborate the distant relationship between annelids, arthropods and vertebrates (Dunn et al., 2008; Dunn et al., 2014; Edgecombe et al., 2011; Hejnol et al., 2009), reinforcing the homoplasy of their body segmentation.

Remarkably, the molecular mechanisms of body segmentation in arthropods and vertebrates show a number of striking similarities (Damen, 2007; Davis and Patel, 1999; Kimmel, 1996; Patel, 2003; Peel and Akam, 2003; Seaver, 2003; Tautz, 2004). These molecular similarities were taken as evidence to support the homology of bilaterian segmentation (De Robertis, 1997; De Robertis, 2008; Dray et al., 2010; Kimmel, 1996), despite the opposing data from phylogenetics. To reconcile this apparent conflict between developmental and phylogenetic data, we must apply a comprehensive evolutionary approach to the problem.

The concept of segmentation is often used in a typological—and not evolutionary—manner (Budd, 2001). The result is a taxonomic bias, where the evolution of segmentation is regarded from the point of view of the groups considered to be segmented, i.e., annelids, arthropods and vertebrates (Budd, 2001). As a matter of fact, there is no conceptual basis to restrict segmentation to these three groups, because the repetition of parts along the body axis (Budd, 2001; Hannibal and Patel, 2013; Minelli and Fusco, 2004) also occurs in varying degrees in other bilaterians—usually considered to be pseudosegmented or unsegmented (Budd, 2001; Minelli and Fusco, 2004; Scholtz, 2002; Willmer, 1990).

Another aspect to be considered is that segmentation—as much as spiral cleavage—is a complex of characters that ought to be individually compared between taxa (Scholtz, 2010). Breaking down segmentation into comparable traits (Scholtz, 2010), such as seriated nerve chords, segmented mesoderm or ectodermal boundaries, should provide a better overview of their evolutionary history.

Nevertheless, the sole comparison of traits between distantly related groups can still be misleading for understanding the evolution of a character (e.g., trunk segmentation), because the ancestral conditions of closer taxa are unknown. Since developmental mechanisms can be coopted to nonhomologous structures (Shubin et al., 2009), the phylogenetic context of a character is essential to distinguish homology from convergence. A recurrent proposal to better understand the evolution of segmentation is to expand taxonomic sampling (Arthur et al., 1999; Budd, 2001; Couso, 2009; Davis and Patel, 1999; Minelli and Fusco, 2004; Patel, 2003; Peel and Akam, 2003; Seaver, 2003; Tautz, 2004). Thus, examining segmentation traits in a wider range of taxa, including those without obvious segmented features, might help us to grasp the evolution of the developmental mechanisms that form repeated body parts in bilaterians.

This text is the final section of my PhD thesis (published on this blog).

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