Boveri's long experiment: sea urchin merogones and the establishment of the role of nuclear chromosomes in development

Abstract

Theodor Boveri's major intellectual contribution was his focus on the causality of nuclear chromosomal determinants for embryological development. His initial experimental attempt to demonstrate that the character of the developing embryo is determined by nuclear rather than cytoplasmic factors was launched in 1889. The experimental design was to fertilize enucleate sea urchin eggs with sperm of another species that produces a distinguishably different embryonic morphology. Boveri's "hybrid merogone" experiment provided what he initially thought was empirical evidence for the nuclear control of development. However, for subtle reasons, the data were not interpretable and the experiment was repeated and contested. At the end of his life, Boveri was finally able to explain the technical difficulties that had beset the original experiment. However, by 1902 Boveri had carried out his famous polyspermy experiments, which provided decisive evidence for the role of nuclear chromosomal determinants in embryogenesis. Here we present the history of the hybrid merogone experiment as an important case of conceptual reasoning paired with (often difficult) experimental approaches. We then trace the further history of the merogone and normal species hybrid approaches that this experiment had set in train, and review their results from the standpoint of current insights. The history of Boveri's hybrid merogone experiment suggests important lessons about the interplay between what we call "models", the specific intellectual statements we conceive about how biology works, and the sometimes difficult task of generating experimental proof for these concepts.

Fig. 1

Drawings from the initial mergon experiment. (A) Normal Echninus pluteus. (B) Normal Sphearechinus pluteus. The plutei are shown upside down, as presented in the original paper; reproduced from Boveri, 1889. (C) Dwarf pluteus formed by insemination of a nucleated egg fragment Sphaerechinus with Echinus sperm. (D) Dwarf pluteus formed by insemination of an apparently enucleated Sphaerchinus egg fragment with Echinus sperm. Drawings from Boveri 1893 [1889], English translation of this paper by T.H. Morgan, which contains additional original drawings from Boveri.

Fig. 2

Provided by Dr. Andrew Ransick. Boveri at his laboratory at the Institute of Zoology in Würzburg in 1907, reproduced from Baltzer, 1967. Boveri’s drawing at upper right shows an abnormal aneuploid gastrula stage embryo containing nuclei of two different sizes. Below is the same embryo, photographed by Dr. Andrew Ransick from one of Boveri’s original 1904 slides, which had been kindly provided to the author by Professor Ulrich Scheer, University of Würzburg. In the magnification below the smaller nuclei in the blue region to the right can clearly be distinguished. Lower left shows an approximately normal pluteus larva from the same series of experiments.