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Embryos in evolution: evo-devo at the Naples Zoological Station in 1874

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Abstract

Eighteen seventy-four was a high point in evolutionary embryology. Thanks to Charles Darwin, the theory of evolution by natural selection provided a revolutionary new way of viewing the relationships and origins of organisms on Earth. Thanks to Ernst Haeckel, embryos were the way to study evolution (Haeckel in Generelle morphologie der organismen, vols 1, 2. Verlag Georg Reimer, Berlin, 1866)—it really was embryos in evolution—and recapitulation was in the air. Thanks to Anton Dohrn, a new research facility was on the ground, designed, located and structured to facilitate the study of embryos in evolution. Anton Dohrn devised, designed, financed, supervised the construction and then administered the Naples Zoological Station specifically so that researchers from all nations would have a facility where Darwin’s theory of evolution by natural selection could be tested. The zoologists who took advantage of the brand new facility within weeks of its opening late in 1873 established lines of research into evolutionary embryology, the field we now know as evolutionary developmental biology (evo-devo), the study of embryos in evolution. I examine the approach taken by Ambrosius Hubrecht, the first Dutch embryologist to undertake research at the station, and then evaluate the research of three British zoologists—E. Ray Lankester, Albert Dew-Smith, and Francis Maitland (Frank) Balfour. All four sought insights into origins, especially vertebrate origins that rested on comparative embryology, homology, germ layers, and a Darwinian approach to origins.

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Notes

  1. See Groeben and Müller (1975), Groeben (1985), Monroy and Groeben (1985), Heuss (1991) and Hall (2007a) for Anton Dohrn and analyses of the founding of the station.

  2. The 1887 paper is based on specimens collected during the Challenger expedition.

  3. See Macleod (1994) for those who went out to seek such embryos funded by the Balfour Studentship from Cambridge university, Hall (1999) for William Caldwell and the search for platypus embryos, Hall (2001) for John Budgett and the search for lungfish embryos (and Blackman 2007, for why Balfour did not investigate lungfish embryos.

  4. Richard Assheton, himself a worker on mammalian embryology and a former student of Balfour's, published a biographical evaluation of Hubrecht (Assheton 1915).

  5. For a later summary of Lankester's view on germ layers see his presidential address to the BAAS delivered in 1906 (Lankester 1911, pp. 112–113). See Hall (1994, 1995, 2003a, 2007b) for discussions of the relationships between homology and embryonic development.

  6. A short visit to Naples (September and October 1873) by the German anatomist Wilhelm Waldeyer (1836–1921), who went on to become a brilliant teacher of Anatomy at Breslau, Strasbourg, and Berlin, makes him the first to work at the (unfinished) station. We owe to Waldeyer our basic ideas about the relationships between numbers of germ cells and major stages of the reproductive life cycle in women. Waldeyer coined the terms ‘chromosome’ and ‘neuron.’ Balfour was aware of Waldeyer's work before they met in Naples. In his first paper on germ layers in the embryonic chick published in 1873, Balfour cited an 1869 paper of Waldeyer's on the origin of the mesoblast (Balfour disagreed with Waldeyer's interpretation: “his drawings of the derivation of the mesoblast from the epiblast are not very correct”) and cites an 1870 paper on the origin of the Wolffian duct from the epiblast. In his second paper on disappearance of the primitive groove in chick embryos, Balfour referred to Waldeyer's views without citing any references (Balfour 1873a, pp. 270, 272, 1873b, pp. 276–7), a pattern he would adopt when referring to earlier work in much of his later writing.

  7. See Russell (1916), Desmond (1982), Hall (1994, 1995, 1998, 2003b, 2004a, b), Nyhart (1995) and Bowler (1996) for discussions of these issues.

  8. Groeben (1982), p. 54, 57, 58, 59, 62.

  9. Michael Foster, in his biographical introduction to The Works of Francis Maitland Balfour states that Balfour arrived at the station at Christmas 1873 (Foster 1885, p. 9). It is clear from the letters of Charles Darwin and records of the station itself that he did not arrive until February 1874.

  10. Letters of Darwin to Dohrn of 13 February 1874 and 29 July 1875; cited from Groeben (1982), pp. 54, 66.

  11. Darwin, F. (1887), vol 3, pp. 250–251.

  12. Cited from Groeben (1982), p. 54. (Sir) Francis Darwin (1848–1925) was a botanist, trained in natural sciences at Trinity and in medicine at St. George's Hospital in London. For 7 years from 1875 until his father's death he acted as Charles Darwin’s secretary and assistant. He lived at Down House after the death of his first wife in 1876, but returned to Cambridge where from 1888 to 1904 he was Reader in Botany and a very effective teacher of that subject. Francis Darwin is most remembered as his father's biographer and editor (The Life and Letters and More Letters) and for his research in plant physiology.

  13. F. Darwin and A. C. Seward (1903), vol 2, p. 44. Frank Balfour's mother was Lady Blanche Mary Harriet Gascoyne-Cecil (1825–1872), second daughter of James Brownlow Cecil (1791–1868) created 2nd Marquis of Salisbury in 1823.

  14. Darwin, F. (1950), p. 100.

  15. See Balfour (1876a, b, 1876–1878) for his other studies on sharks and dogfish.

  16. Early development to the germ layers accounts for one quarter of the paper. Somitic mesoderm or the somites from which axial structures such as vertebrae, muscle and dermis arise, are referred to by Balfour as protovertebrae. Balfour first uses the term somites for these structures in his 1879 paper on early development in lizards (Balfour 1879, p. 423).

  17. Balfour would later argue that the gills of amphibian tadpoles exist because the tadpole is an aquatic ancestral stage. Physiological arguments associated with tadpole respiration are not mentioned at all. Later, workers such as Nikolaus Kleinenberg (Dohrn’s first but short-lived assistant in Naples from 1874–1875) posited a second alternative reasons for the retention of such structures – they provided the stimulus for the development of other organs—notochord for the vertebral column, cartilage for bone.

  18. Letter from Thomas Huxley to Anton Dohrn, 24 September, 1882; cited in Huxley, L. (1900). vol. 2, p. 38.

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Acknowledgments

I am grateful to Prof. Lennart Olsson for the invitation to contribute to this issue. Research support from the Natural Sciences and Engineering Council of Canada (Grant A5056) is gratefully acknowledged, as is the School of Life Sciences at Arizona State University for providing such a conducive environment in which to read, write and think.

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  1. School of Life Sciences, College of Liberal Arts and Sciences, Arizona State University, Tempe, AZ, 85287-3301, USA

    Brian K. Hall

  2. Department of Biology, Dalhousie University, Halifax, NS, B3H 4J1, Canada

    Brian K. Hall

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Hall, B.K. Embryos in evolution: evo-devo at the Naples Zoological Station in 1874. Theory Biosci. 128, 7–18 (2009). https://doi.org/10.1007/s12064-009-0057-0

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