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

Larvae as the epitome of evolution

Read the previous section: What a larva is.

Francis M. Balfour set the pace on discussions about the evolutionary importance of larvae by addressing many of the fundamental questions regarding larval evolution (Balfour, 1874; Balfour, 1880; Balfour, 1881). He wondered about the ancestry of larvae. Can larvae reveal the ancestral forms of metazoans? He indicated tests to the predictions of recapitulation. Can we find a larva that corresponds to the adult of a related group? He asked whether larvae changed during evolution. How often do larval organs evolve? And what might be the underlying mechanisms for the evolution of development. What guides the maintenance or atrophy of larval organs in adult stages? (Hall and Wake, 1999).

Perhaps, the greatest conceptual advance initiated by Balfour is that larvae are subject to variation and natural selection in the same manner as the adult stage (Balfour, 1874; Balfour, 1881). In other words, he articulated the realization that evolution can occur at any developmental stage. However, if not all embryonic features represent ancestors (or ancestral traits), the foundation of the recapitulation theory is compromised. The evolutionary debate caused by larvae influenced a more informed way to make extrapolations from ontogeny to phylogeny (Hall, 2000; Hall and Wake, 1999). It was no coincidence that one of the most vehement opponents of Haeckel’s recapitulation theory was a larvae affectionate, the biologist Walter Garstang who boldly concluded that “ontogeny does not recapitulate phylogeny, it creates it” (Garstang, 1922).

Larvae of different marine invertebrates.
Larvae of a brachiopod (left), a nemertean (center) and a bryozoan (right).

Present-day research shows that larval traits are evolutionary labile, and often correlate to ecological, developmental and other life-history factors (Strathmann and Eernisse, 1994). Evidence from diverse taxa, including gastropods (Collin, 2004), sea urchins (Raff and Byrne, 2006), ascidians (Jeffery and Swalla, 1992), sea stars (Byrne, 2006; Hart et al., 1997), nemerteans (Maslakova and Hiebert, 2014) and polyclad flatworms (Rawlinson, 2014), indicates that larval forms were modified, gained or lost in different lineages independently, and that the observed similarities are likely the result of convergent evolution.

These observations undermine scenarios about animal evolution that require the homology of larval characters (Jägersten, 1972; Nielsen, 1998; Nielsen, 2001; Nielsen, 2009; Peterson and Cameron, 1997) and are more consonant with the multiple independent evolution of metazoan larvae from a direct-developing ancestor (Page, 2009; Raff, 2008; Sly et al., 2003; Wray, 1995). Yet, the homology of larval characters such as the apical organ (e.g., Hunnekuhl and Akam, 2014; Marlow et al., 2014) or ciliated bands (e.g., Henry et al., 2007; Rouse, 1999) continues to be a central and lively discussed topic. For all the reasons above, larvae are a scandalous epitome of evolution, and the diversity of larval body patterns in marine invertebrates continue to provide a rich framework for evolutionary studies.

This text is a section of my PhD thesis. Read the next section: Spiral cleavage, an oblique matter.


Balfour, F.M., 1874. Memoirs: A Preliminary Account of the Development of the Elasmobranch Fishes. The Quarterly journal of microscopical science. Available at:

Balfour, F.M., 1880. A Treatise on Comparative Embryology, Macmillan and Company.

Balfour, F.M., 1881. A Treatise on Comparative Embryology, Macmillan and Company. Available at:

Byrne, M., 2006. Life history diversity and evolution in the Asterinidae. Integrative and comparative biology, 46(3), pp.243–254. Available at:

Collin, R., 2004. Phylogenetic effects, the loss of complex characters, and the evolution of development in calyptraeid gastropods. Evolution; international journal of organic evolution, 58(7), pp.1488–1502. Available at:

Garstang, W., 1922. The Theory of Recapitulation: A Critical Re-statement of the Biogenetic Law. Journal of the Linnean Society of London, Zoology, 35(232), pp.81–101. Available at:

Hall, B.K., 2000. Balfour, Garstang and de Beer: The First Century of Evolutionary Embryology. American zoologist, 40(5), pp.718–728. Available at:[0718:BGADBT]2.0.CO;2.

Hall, B.K. & Wake, M.H., 1999. Chapter 1 – Introduction: Larval Development, Evolution, and Ecology. In B. K. H. H. Wake, ed. The Origin and Evolution of Larval Forms. San Diego: Academic Press, pp. 1–19. Available at:

Hart, M.W., Byrne, M. & Smith, M.J., 1997. Molecular Phylogenetic Analysis of Life-History Evolution in Asterinid Starfish. Evolution; international journal of organic evolution, 51(6), pp.1848–1861. Available at:

Henry, J.Q. et al., 2007. Homology of ciliary bands in Spiralian Trochophores. Integrative and comparative biology, 47(6), pp.865–871. Available at:

Hunnekuhl, V.S. & Akam, M., 2014. An anterior medial cell population with an apical-organ-like transcriptional profile that pioneers the central nervous system in the centipede Strigamia maritima. Developmental biology, 396(1), pp.136–149. Available at:

Jeffery, W.R. & Swalla, B.J., 1992. Evolution of alternate modes of development in ascidians. BioEssays: news and reviews in molecular, cellular and developmental biology, 14(4), pp.219–226. Available at:

Jägersten, G., 1972. Evolution of the Metazoan Life Cycle First Printing edition., Academic Press Inc.

Marlow, H. et al., 2014. Larval body patterning and apical organs are conserved in animal evolution. BMC biology, 12(1), p.7. Available at:

Maslakova, S.A. & Hiebert, T.C., 2014. From trochophore to pilidium and back again – a larva’s journey. The International journal of developmental biology, 58(6-8), pp.585–591. Available at:

Nielsen, C., 1998. Origin and evolution of animal life cycles. Biological reviews of the Cambridge Philosophical Society, 73(02), pp.125–155. Available at:

Nielsen, C., 2001. Phylum Ectoprocta. In Animal Evolution: Interrelationships of the Living Phyla. Oxford University Press, pp. 244–263.

Nielsen, C., 2009. How did indirect development with planktotrophic larvae evolve? The Biological bulletin, 216(3), pp.203–215. Available at:

Page, L.R., 2009. Molluscan larvae: Pelagic juveniles or slowly metamorphosing larvae? The Biological bulletin, 216(3), pp.216–225. Available at:

Peterson, K.J. & Cameron, R.A., 1997. Set-aside cells in maximal indirect development: Evolutionary and developmental significance. BioEssays: news and reviews in molecular, cellular and developmental biology, 19(7), pp.623–631. Available at:

Raff, R.A., 2008. Origins of the other metazoan body plans: the evolution of larval forms. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 363(1496), pp.1473–1479. Available at:

Raff, R.A. & Byrne, M., 2006. The active evolutionary lives of echinoderm larvae. Heredity, 97(3), pp.244–252. Available at:

Rawlinson, K.A., 2014. The diversity, development and evolution of polyclad flatworm larvae. EvoDevo, 5(1), p.9. Available at:

Rouse, G.W., 1999. Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. Biological journal of the Linnean Society. Linnean Society of London, 66(4), pp.411–464. Available at:

Sly, B.J., Snoke, M.S. & Raff, R.A., 2003. Who came first–larvae or adults? origins of bilaterian metazoan larvae. The International journal of developmental biology, 47(7-8), pp.623–632. Available at:

Strathmann, R.R. & Eernisse, D.J., 1994. What Molecular Phylogenies Tell Us about the Evolution of Larval Forms. Integrative and comparative biology, 34(4), pp.502–512. Available at:

Wray, G.A., 1995. Punctuated evolution of embryos. Science, 267(5201), pp.1115–1116. Available at:

articles biology

Turtles, embryos, and fossils

I wrote a text about the development and evolution of the turtle shell on The Node: Turtles in a nutshell.

800px TurtleOmaha
Turtle at Henry Doorly Zoo, Omaha. Photo by Algy3289.

It shows the beginning of shell formation in embryos and how this can help us understand the evolution of such unique body pattern. 3D animations and fossils are included!

Never thought I would post a vertebrate on this website… but having shoulders inside the rib cage made me make an exception, poor things :p