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).
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: http://jcs.biologists.org/content/s2-14/56/323.full.pdf.
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: https://archive.org/details/treatiseoncompar02balfuoft.
Byrne, M., 2006. Life history diversity and evolution in the Asterinidae. Integrative and comparative biology, 46(3), pp.243–254. Available at: http://dx.doi.org/10.1093/icb/icj033.
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: http://www.ncbi.nlm.nih.gov/pubmed/15341151.
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: https://doi.org/10.1111/j.1096-3642.1922.tb00464.x.
Hall, B.K., 2000. Balfour, Garstang and de Beer: The First Century of Evolutionary Embryology. American zoologist, 40(5), pp.718–728. Available at: http://dx.doi.org/10.1668/0003-1569(2000)040[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: https://doi.org/10.1016/B978-012730935-4/50002-X.
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: https://www.jstor.org/stable/2411007.
Henry, J.Q. et al., 2007. Homology of ciliary bands in Spiralian Trochophores. Integrative and comparative biology, 47(6), pp.865–871. Available at: http://dx.doi.org/10.1093/icb/icm035.
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: http://dx.doi.org/10.1016/j.ydbio.2014.09.020.
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: https://doi.org/10.1002/bies.950140404.
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: http://dx.doi.org/10.1186/1741-7007-12-7.
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: http://dx.doi.org/10.1387/ijdb.140090sm.
Nielsen, C., 1998. Origin and evolution of animal life cycles. Biological reviews of the Cambridge Philosophical Society, 73(02), pp.125–155. Available at: http://journals.cambridge.org/abstract_S0006323197005136.
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: http://www.ncbi.nlm.nih.gov/pubmed/19556589.
Page, L.R., 2009. Molluscan larvae: Pelagic juveniles or slowly metamorphosing larvae? The Biological bulletin, 216(3), pp.216–225. Available at: http://www.ncbi.nlm.nih.gov/pubmed/19556590.
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: https://doi.org/10.1002/bies.950190713.
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: http://dx.doi.org/10.1098/rstb.2007.2237.
Raff, R.A. & Byrne, M., 2006. The active evolutionary lives of echinoderm larvae. Heredity, 97(3), pp.244–252. Available at: http://dx.doi.org/10.1038/sj.hdy.6800866.
Rawlinson, K.A., 2014. The diversity, development and evolution of polyclad flatworm larvae. EvoDevo, 5(1), p.9. Available at: http://dx.doi.org/10.1186/2041-9139-5-9.
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: http://dx.doi.org/10.1111/j.1095-8312.1999.tb01920.x.
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: http://www.ncbi.nlm.nih.gov/pubmed/14756338.
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: http://dx.doi.org/10.1093/icb/34.4.502.
Wray, G.A., 1995. Punctuated evolution of embryos. Science, 267(5201), pp.1115–1116. Available at: http://dx.doi.org/10.1126/science.267.5201.1115.