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).
Aguinaldo, A.M. et al., 1997. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature, 387(6632), pp.489–493. Available at: http://dx.doi.org/10.1038/387489a0.
Arthur, W., Jowett, T. & Panchen, A., 1999. Segments, limbs, homology, and co-option. Evolution & development, 1, pp.74–76. Available at: https://doi.org/10.1046/j.1525-142x.1999.98004.x.
Budd, G.E., 2001. Why are arthropods segmented? Evolution & development, 3(5), pp.332–342. Available at: http://www.ncbi.nlm.nih.gov/pubmed/11710765.
Chipman, A.D., 2010. Parallel evolution of segmentation by co-option of ancestral gene regulatory networks. BioEssays: news and reviews in molecular, cellular and developmental biology, 32(1), pp.60–70. Available at: https://doi.org/10.1002/bies.200900130.
Couso, J.P., 2009. Segmentation, metamerism and the Cambrian explosion. The International journal of developmental biology, 53(8-10), pp.1305–1316. Available at: http://dx.doi.org/10.1387/ijdb.072425jc.
Damen, W.G.M., 2007. Evolutionary conservation and divergence of the segmentation process in arthropods. Developmental dynamics: an official publication of the American Association of Anatomists, 236(6), pp.1379–1391. Available at: https://doi.org/10.1002/dvdy.21157.
Davis, G.K. & Patel, N.H., 1999. The origin and evolution of segmentation. Trends in cell biology, 9(12), pp.M68–72. Available at: http://www.ncbi.nlm.nih.gov/pubmed/10611687.
De Robertis, E.M., 1997. Evolutionary biology. The ancestry of segmentation. Nature, 387(6628), pp.25–26. Available at: http://dx.doi.org/10.1038/387025a0.
De Robertis, E.M., 2008. The molecular ancestry of segmentation mechanisms. Proceedings of the National Academy of Sciences of the United States of America, 105(43), pp.16411–16412. Available at: https://doi.org/10.1073/pnas.0808774105.
Dray, N. et al., 2010. Hedgehog signaling regulates segment formation in the annelid Platynereis. Science, 329(5989), pp.339–342. Available at: http://dx.doi.org/10.1126/science.1188913.
Dunn, C.W. et al., 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature, 452(7188), pp.745–749. Available at: http://dx.doi.org/10.1038/nature06614.
Dunn, C.W. et al., 2014. Animal Phylogeny and Its Evolutionary Implications. Annual review of ecology, evolution, and systematics, 45(1), pp.371–395. Available at: https://doi.org/10.1146/annurev-ecolsys-120213-091627.
Edgecombe, G.D. et al., 2011. Higher-level metazoan relationships: recent progress and remaining questions. Organisms, diversity & evolution, 11(2), pp.151–172. Available at: http://dx.doi.org/10.1007/s13127-011-0044-4.
Eernisse, D.J., 1998. Arthropod and annelid relationships re-examined. In Arthropod Relationships. The Systematics Association Special Volume Series. Springer Netherlands, pp. 43–56. Available at: http://link.springer.com/chapter/10.1007/978-94-011-4904-4_5.
Graham, A. et al., 2014. What can vertebrates tell us about segmentation? EvoDevo, 5(1), p.24. Available at: http://dx.doi.org/10.1186/2041-9139-5-24.
Hannibal, R.L. & Patel, N.H., 2013. What is a segment? EvoDevo, 4(1), p.35. Available at: http://dx.doi.org/10.1186/2041-9139-4-35.
Hejnol, A. et al., 2009. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proceedings. Biological sciences / The Royal Society, 276(1677), pp.4261–4270. Available at: http://dx.doi.org/10.1098/rspb.2009.0896.
Kimmel, C.B., 1996. Was Urbilateria segmented? Trends in genetics: TIG, 12(9), pp.329–331. Available at: http://www.ncbi.nlm.nih.gov/pubmed/8855654.
Migotto, A.E. & Vellutini, B.C., 2011. Cifonauta – marine biology image database. Cifonauta, an image database for marine biology. Available at: http://cifonauta.cebimar.usp.br/ [Accessed December 16, 2015].
Minelli, A. & Fusco, G., 2004. Evo-devo perspectives on segmentation: model organisms, and beyond. Trends in ecology & evolution, 19(8), pp.423–429. Available at: http://dx.doi.org/10.1016/j.tree.2004.06.007.
Patel, N.H., 2003. The ancestry of segmentation. Developmental cell, 5(1), pp.2–4. Available at: http://www.ncbi.nlm.nih.gov/pubmed/12852844.
Peel, A. & Akam, M., 2003. Evolution of segmentation: rolling back the clock. Current biology: CB, 13(18), pp.R708–10. Available at: http://www.ncbi.nlm.nih.gov/pubmed/13678609.
Scholtz, G., 2002. The Articulata hypothesis – or what is a segment? Organisms, diversity & evolution, 2(November 2001), pp.197–215. Available at: https://doi.org/10.1078/1439-6092-00046.
Scholtz, G., 2010. Deconstructing morphology. Acta zoologica , 91(1), pp.44–63. Available at: https://doi.org/10.1111/j.1463-6395.2009.00424.x.
Seaver, E.C., 2003. Segmentation: mono- or polyphyletic? The International journal of developmental biology, 47(7-8), pp.583–595. Available at: http://www.ncbi.nlm.nih.gov/pubmed/14756334.
Shubin, N., Tabin, C. & Carroll, S.B., 2009. Deep homology and the origins of evolutionary novelty. Nature, 457(7231), pp.818–823. Available at: http://dx.doi.org/10.1038/nature07891.
Tautz, D., 2004. Segmentation. Developmental cell, 7(3), pp.301–312. Available at: http://dx.doi.org/10.1016/j.devcel.2004.08.008.
Willmer, P., 1990. Body divisions – metamerism and segmentation. In Invertebrate Relationships: Patterns in Animal Evolution. Cambridge University Press, pp. 39–45. Available at: http://www.amazon.com/Invertebrate-Relationships-Patterns-Animal-Evolution/dp/0521337127.
- In addition to the somites, vertebrates also show segmentation in the rhombomeres and in the pharyngeal archs; segmented structures that likely evolved independently in the deuterostome lineage (Graham et al., 2014).↩