biology articles

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).

Taxa with a segmented trunk. Annelida: the holoplanktonik polychaete Tomopteris sp., Arthropoda: a mantis shrimp (Stomatopoda), Vertebrata: a Teleostei fish larva. Yellow lines mark the anterior and posterior boundary of one segment. Image on the right is a closeup of the ectodermal segmentation of the fire worm Eurythoe complanata. Images not to scale. Photos by Alvaro E. Migotto (Migotto and Vellutini, 2011).
Taxa with a segmented trunk. Annelida: the holoplanktonik polychaete Tomopteris sp., Arthropoda: a mantis shrimp (Stomatopoda), Vertebrata: a Teleostei fish larva. Yellow lines mark the anterior and posterior boundary of one segment. Image on the right is a closeup of the ectodermal segmentation of the fire worm Eurythoe complanata. Images not to scale. Photos by Alvaro E. Migotto (Migotto and Vellutini, 2011).

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:

Arthur, W., Jowett, T. & Panchen, A., 1999. Segments, limbs, homology, and co-option. Evolution & development, 1, pp.74–76. Available at:

Budd, G.E., 2001. Why are arthropods segmented? Evolution & development, 3(5), pp.332–342. Available at:

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:

Couso, J.P., 2009. Segmentation, metamerism and the Cambrian explosion. The International journal of developmental biology, 53(8-10), pp.1305–1316. Available at:

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:

Davis, G.K. & Patel, N.H., 1999. The origin and evolution of segmentation. Trends in cell biology, 9(12), pp.M68–72. Available at:

De Robertis, E.M., 1997. Evolutionary biology. The ancestry of segmentation. Nature, 387(6628), pp.25–26. Available at:

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:

Dray, N. et al., 2010. Hedgehog signaling regulates segment formation in the annelid Platynereis. Science, 329(5989), pp.339–342. Available at:

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:

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:

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:

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:

Graham, A. et al., 2014. What can vertebrates tell us about segmentation? EvoDevo, 5(1), p.24. Available at:

Hannibal, R.L. & Patel, N.H., 2013. What is a segment? EvoDevo, 4(1), p.35. Available at:

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:

Kimmel, C.B., 1996. Was Urbilateria segmented? Trends in genetics: TIG, 12(9), pp.329–331. Available at:

Migotto, A.E. & Vellutini, B.C., 2011. Cifonauta – marine biology image database. Cifonauta, an image database for marine biology. Available at: [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:

Patel, N.H., 2003. The ancestry of segmentation. Developmental cell, 5(1), pp.2–4. Available at:

Peel, A. & Akam, M., 2003. Evolution of segmentation: rolling back the clock. Current biology: CB, 13(18), pp.R708–10. Available at:

Scholtz, G., 2002. The Articulata hypothesis – or what is a segment? Organisms, diversity & evolution, 2(November 2001), pp.197–215. Available at:

Scholtz, G., 2010. Deconstructing morphology. Acta zoologica , 91(1), pp.44–63. Available at:

Seaver, E.C., 2003. Segmentation: mono- or polyphyletic? The International journal of developmental biology, 47(7-8), pp.583–595. Available at:

Shubin, N., Tabin, C. & Carroll, S.B., 2009. Deep homology and the origins of evolutionary novelty. Nature, 457(7231), pp.818–823. Available at:

Tautz, D., 2004. Segmentation. Developmental cell, 7(3), pp.301–312. Available at:

Willmer, P., 1990. Body divisions – metamerism and segmentation. In Invertebrate Relationships: Patterns in Animal Evolution. Cambridge University Press, pp. 39–45. Available at:

  1. 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).
articles biology

Spiral cleavage, an oblique matter

Read the previous section: Larvae as the epitome of evolution.

By the end of the 19th century, a series of biologists had dedicated themselves to following and discovering the fate of individual cells of an embryo during ontogeny. These works, known as cell lineage studies1, were critical to disambiguate the relationship between ontogeny and phylogeny, directly challenging the idea of recapitulation (Guralnick, 2002; Maienschein, 1978).

The detailed work of the cell lineage biologists Edmund B. Wilson, Edwin G. Conklin, Frank R. Lillie and others, revealed something remarkable. After carefully tracing the embryonic cells of different organisms, they discovered that animals such as molluscs, annelids, nemerteans and polyclad flatworms, whose adult stages are so different, actually share a similar embryogenesis2 (Child, 1900; Conklin, 1897; Heath, 1899; Lillie, 1895; Mead, 1897; Wilson, 1892). Their embryos show the same cleavage pattern, in which cell divisions occur with the mitotic spindles oblique to the animal/vegetal axis, switching direction (clockwise and counterclockwise) at each division cycle (Costello and Henley, 1976; Hejnol, 2010; Henry and Martindale, 1999; Lambert, 2010). A quartet of vegetal macromeres sequentially gives rise to animal micromeres, and the resulting symmetry of these cleaving blastomeres, when viewed from the animal pole, was described as spiral. This developmental pattern thus became known as spiral cleavage (Wilson, 1892).

The spiral cleavage pattern.
The spiral cleavage pattern. (A) Animal pole view of a generalized spiral-cleaving embryo. Arrows indicate the direction of cell divisions. Developmental sequence based on (Conklin, 1897). (B) Schematic diagram of cell divisions in the D quadrant in a lateral view (top: animal pole, bottom: vegetal pole). Cells are named with the standard spiral cleavage notation(Child, 1900; Conklin, 1897; Wilson, 1892). Representation based on Lambert (2010).

Because the cell divisions are stereotypic, individual blastomeres can be followed and compared between spiral-cleaving taxa in a fairly consistent manner. The ability to compare blastomere fates at this unprecedented cellular-resolution uncovered a surprising similarity in the fate maps of spiral-cleaving embryos (=annelids, molluscs, nemerteans and polyclad flatworms). The iconic example being the 4d mesentoblast, a well-conserved mesoderm precursor (Lambert, 2008). Overall, despite having the oblique cell divisions as an idiosyncrasy, spiral cleavage is understood today as a complex of developmental characters (Costello and Henley, 1976; Hejnol, 2010; Henry and Martindale, 1999; Lambert, 2010).

The empirical findings of cell lineage studies raised several important evolutionary questions regarding the evolution of development and the establishment of homologies (Guralnick, 2002). What are the underlying causes behind embryonic cleavage patterns—mechanical forces acting on the embryo or inherited historical factors? Are the events of early development necessary to build the adult characters? Is there an embryological criterion for homology? The ideas progressively moved towards a more evolutionary view of development, where ontogeny is not “a brief and rapid recapitulation of phylogeny” but an inherited product of evolution and subject to modification (Guralnick, 2002).

Even though most cell lineage biologists initially denied the systematic value of embryonic cleavage patterns, mainly in opposition to recapitulation (Guralnick, 2002), it was difficult to argue against the striking similarity between spiral-cleaving embryos, and dismiss their potential kinship3. Schleip (1929) was the first to propose a group to contain the animals displaying spiral cleavage—the Spiralia.

Recent metazoan-wide phylogenetic analyses corroborate the kinship between spiral-cleaving taxa, in a major protostome clade that is sister to the Ecdysozoa (e.g., insects) (Dunn et al., 2014). The latest works in protostome phylogenomics (Laumer et al., 2015; Struck et al., 2014) suggest that Spiralia (=Lophotrochozoa in some cases, see Hejnol (2010)) contains not only the typical spiral-cleaving groups, but several other taxa. Some spiralians (=animals that belong to the clade Spiralia) do not show any clear trace of spiral cleavage, such as bryozoans, brachiopods, gastrotrichs and rotifers, while others do exhibit spiral-like characters, such as gnathostomulids (Riedl, 1969), phoronids (Pennerstorfer and Scholtz, 2012) and entoprocts (Marcus, 1939; Merkel et al., 2012). What can we say about the evolution of these disparate cleavage patterns?

The spiral arrangement of embryonic blastomeres is present in the three main clades of Spiralia (Gnathifera, Lophotrochozoa and Rouphozoa), suggesting that this character is ancestral at least to the Lophotrochozoa-Rouphozoa clade. This implies the spiral cleavage pattern was lost during the evolution of gastrotrichs, brachiopods, bryozoans and maybe rotifers. How did these groups lose spiral cleavage? Which aspects of a typical spiral-cleaving embryo did they lose, in addition to the spiral arrangement of the blastomeres? Are there any remnants of spiral cleavage?

The comparison between clades that have lost spiral symmetry, like bryozoans and brachiopods, and typical spiral-cleaving clades such as annelids and molluscs, can identify the traits that were lost, or are still shared, among these groups. This comparative approach can reveal novel insights about the evolution of spiral cleavage itself, and give rise to a broader perspective of the evolutionary mechanisms underlying spiralian development.

This text is a section of my PhD thesis. Read the next section: Segmentation, a question of boundaries.


Bonner, J.T. & Bell, W.J., Jr., 1984. “What Is Money for?”: An Interview with Edwin Grant Conklin, 1952. Proceedings of the American Philosophical Society, 128(1), pp.79–84. Available at:

Child, C.M., 1900. The early development of Arenicola and Sternaspis. Wilhelm Roux’ Archiv fur Entwicklungsmechanik der Organismen, 9(4), pp.587–723. Available at:

Conklin, E.G., 1897. The embryology of Crepidula, A contribution to the cell lineage and early development of some marine gasteropods. Journal of morphology, 13(1), pp.1–226. Available at:

Costello, D.P. & Henley, C., 1976. Spiralian Development: A Perspective. American zoologist, 16(3), pp.277–291. Available at:

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:

Guralnick, R., 2002. A Recapitulation of the Rise and Fall of the Cell Lineage Research Program: The Evolutionary-Developmental Relationship of Cleavage to Homology, Body Plans and Life History. Journal of the history of biology, 35(3), pp.537–567. Available at:

Heath, H., 1899. The development of Ischnochiton. Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere Abteilung für Anatomie und Ontogenie der Tiere., 12, pp.567–656. Available at:

Hejnol, A., 2010. A twist in time—the evolution of spiral cleavage in the light of animal phylogeny. Integrative and comparative biology, 50(5), pp.695–706. Available at:

Henry, J. & Martindale, M.Q., 1999. Conservation and innovation in spiralian development. Hydrobiologia, pp.255–265. Available at:

Lambert, J.D., 2008. Mesoderm in spiralians: the organizer and the 4d cell. Journal of experimental zoology. Part B, Molecular and developmental evolution, 310(1), pp.15–23. Available at:

Lambert, J.D., 2010. Developmental patterns in spiralian embryos. Current biology: CB, 20(2), pp.R72–7. Available at:

Laumer, C.E. et al., 2015. Spiralian phylogeny informs the evolution of microscopic lineages. Current biology: CB, 25(15), pp.2000–2006. Available at:

Lillie, F.R., 1895. The embryology of the Unionidae. A study in cell-lineage. Journal of morphology, 10(1), pp.1–100. Available at:

Maienschein, J., 1978. Cell lineage, ancestral reminiscence, and the biogenetic law. Journal of the history of biology, 11(1), pp.129–158. Available at:

Marcus, E., 1939. Bryozoarios Marinhos Brasileiros III. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia, 3, pp.113–299.

Mead, A.D., 1897. The early development of marine annelids. Journal of morphology, 13(2), pp.227–326. Available at:

Merkel, J. et al., 2012. Spiral cleavage and early embryology of a loxosomatid entoproct and the usefulness of spiralian apical cross patterns for phylogenetic inferences. BMC developmental biology, 12(1), p.11. Available at:

Pennerstorfer, M. & Scholtz, G., 2012. Early cleavage in Phoronis muelleri (Phoronida) displays spiral features. Evolution & development, 14(6), pp.484–500. Available at:

Riedl, R.J., 1969. Gnathostomulida from America. Science, 163(3866), pp.445–452. Available at:

Schleip, W., 1929. Die Determination der Primitiventwicklung, ein zusammenfassende Darstellung der Ergebnisse über das Determinationsgeschehen in den ersten Entwicklungsstadien der Tiere, Leipzig: Akademische Verlagsgesellschaft m.b.h. Available at:

Struck, T.H. et al., 2014. Platyzoan paraphyly based on phylogenomic data supports a noncoelomate ancestry of Spiralia. Molecular biology and evolution, 31(7), pp.1833–1849. Available at:

Wilson, E.B., 1892. The cell-lineage of Nereis. A contribution to the cytogeny of the annelid body. Journal of morphology, 6(3), pp.361–466. Available at:

  1. Also nicknamed cellular bookkepping, as recalled by E.G. Conklin: “…I followed individual cells through the development, followed them until many people laughed about it; called it cellular bookkeeping.” (Bonner and Bell, 1984, p. 81).
  2. “What a wonderful parallel is this between animals so unlike in their end stages! How can such resemblances be explained?” (Conklin, 1897, p. 195).
  3. “…if these minute and long-continued resemblances are of no systematic worth, and are merely the result of extrinsic causes, as is implied, then there are no resemblances between either embryos or adults that may not be so explained.” (Conklin, 1897, p. 195).