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:

biology articles

Endless larval forms most beautiful: what a larva is

This text is a section of my PhD thesis.

The Latin word lārva means evil spirit, ghost or mask1. In the 18th century, the naturalist Carolus Linnaeus was the first to employ the word larva to describe a stage in the life of an animal in which its adult form is still hidden or masked (Linnaeus, 1767, p. 534). An exemplar case of this new biological meaning is the maggot—the larval stage of a fly—whose wormy form and life style truly differs from its flying adult stage.

Not all larvae, however, are masked forms. The larval body of some marine snails2, for example, is very similar to its adult body, except for the dazzling presence of a ciliated velum, used by the larva to swim and gather food (Collier, 1997). In more general terms, larval stages are considered to be a modification of embryonic development usually characterized by a morphology and habitat that are disparate from the adult stage (Hall and Wake, 1999). Because embryonic development can change in a multitude of ways, as evidenced by the great diversity of larval forms in nature (see below), there is no precise definition of larva (Hickman, 1999; Strathmann, 1993). Thus in practice, what a larva is, is defined case by case according to the organism and to one’s research background.

The majority of animals on this planet have a complex life cycle with one or more larval stages. Collectively, marine invertebrates represent a great part of the observed larval diversity. Molluscs have the veliger, a shelled larva with the ciliated velum mentioned above; echinoderms have the pluteus, a spaceship-like larva with eight food-capturing arms, and the brachiolaria, a free-swimming larva driven by body-length dancing arms; bryozoans have the cyphonautes, a paper-thin triangular larva that sails over kelp blades; crustaceans have the zoea, an armored larva that swims as if using a jet pack; nemerteans have the pilidium, a larva with lobes and lappets in the form of a deerstalker cap… and this list goes on. The diversity of larval forms is astonishing.

Sample of the diversity of metazoan larval forms. Larvae are not to scale. Photos from the Cifonauta marine biology image database (Migotto and Vellutini, 2011).
Sample of the diversity of metazoan larval forms. Larvae are not to scale. Photos from the Cifonauta marine biology image database (Migotto and Vellutini, 2011).

Most of these charismatic larval figures were discovered in the 19th century by the naturalist founders of comparative embryology (Hall and Wake, 1999). At the time, the ideas of Karl Ernst von Baer and Ernst Haeckel had great influence on the understanding of embryonic development (Guralnick, 2002; Hall, 2000). Ontogeny was seen as the unfolding of an immutable process that represents the evolutionary history of an organism—an idea known as recapitulation or Haeckel’s biogenetic law: “ontogeny is a rapid and shortened recapitulation of phylogeny.” (Gould, 1977; Haeckel, 1866).

These influential ideas were directly challenged by the mere existence of larvae. Or more generally, challenged by the existence of differentiated developmental stages that are, at the same time, functionally adapted to their environment and morphologically diverse. Such impressive variety of larval forms instigated questions about the relationship between the embryonic development of an individual (ontogeny) and the evolutionary history of a lineage (phylogeny).

Do larvae represent ancestral adult forms? How many times have larvae evolved? Are larval structures homologous or independently evolved? Soon, there was an urge to rationalize the diversity of larval forms into an evolutionary context.

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


Collier, J.R., 1997. Gastropods, the Snails. In S. F. Gilbert & A. M. Raunio, eds. Embryology: constructing the organism. Sinauer Associates, Inc., pp. 189–217.

Gould, S.J., 1977. Ontogeny and phylogeny, Harvard University Press.

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:

Haeckel, E., 1866. Generelle Morphologie der Organismen, Georg Reimer, Berlin. 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:

Hickman, C.S., 1999. Chapter 2 – Larvae in Invertebrate Development and Evolution. In B. K. H. H. Wake, ed. The Origin and Evolution of Larval Forms. San Diego: Academic Press, pp. 21–59. Available at:

Linnaeus, C., 1767. Systema Naturæ, Impensis direct. Laurentii Salvii. 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].

Sars, M., 1837. Beitrag zur Entwicklungsgeschichte der Mollusken und Zoophyten. Archiv für Naturgeschichte, 3, pp.402–407. Available at:

Strathmann, R.R., 1993. Hypotheses on the Origins of Marine Larvae. Annual review of ecology and systematics, 24, pp.89–117. Available at:

Young, C.M., 1990. Larval ecology of marine invertebrates: A sesquicentennial history. Ophelia, 32(1-2), pp.1–48. Available at:

  1. American Heritage® Dictionary of the English Language, Fifth Edition. (2011). Accessed November 13 2015 at
  2. Michael Sars, one of the Norwegian biologists giving the name to the Sars Centre, was among the first to describe the development of molluscs from a swimming larva (Sars, 1837; Young, 1990).
notes science

My PhD thesis in the blog post format

I miss blogging. I began in 2006 and did it quite actively until 2011—when my posting frequency declined. During my PhD I was still drafting several posts, but ended up only publishing a few. I missed the sharing of ideas and the open discussion that a blog post can give. And this is why I decided to write the introduction of my PhD thesis as a series of blog posts.

Now that I have defended my PhD, I’ll post some sections of the text here. The thesis is accessible at the Bergen Open Research Archive (BORA – UiB):

Bruno C. Vellutini PhD Thesis

Vellutini, B.C., 2016. Comparative development of spiralian larvae. The University of Bergen. Available at:

The first section is online. I’ll post the remaining in the coming weeks. Enjoy, comment, disagree, re-use, etc 🙂

  1. Endless larval forms most beautiful: what a larva is (also at The Winnower)
  2. Larvae as the epitome of evolution (also at The Winnower)
  3. Spiral cleavage, an oblique matter (also at The Winnower)
  4. Segmentation, a question of boundaries (also at The Winnower)
notes personal science


Congratulations Andreas Hejnol for debutting as a Doktorvater (doctorfather) yesterday! It is an honor to be the first of many more to come. And thank you for being the most awesome PhD supervisor I could have ever envisioned! <3