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Prior to the theory of symbiogenesis (heralded especially by Lynn Margulis in the late 60s), how did people explained the presence of chlorophyll in various, separate groups such as cyanobacteria, land plants, chromists and a variety of small separate groups of eukaryots (namely, if I don't forget anyone: euglens, chlorarachniophyceae, cryptophytes, haptophytes and dinoflagellates)?

Did people think that chlorophyll-based photosynthesis appeared once and that all those groups were descendants of the same ancester?

Or did they think it appeared multiple times, using basically the same structure, by convergence?

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  • $\begingroup$ @terry-s You can always see the complete revision history of a post by clicking on the "edited Jul 5 at 21:22" link. Here BenCrowell only changed the title from "Theories on the apparition of photosynthesis, prior to Lynn Margulis work on symbiogenesis" to "Theories on the beginning of photosynthesis, prior to Lynn Margulis work on symbiogenesis". $\endgroup$ – plannapus Aug 31 '17 at 7:55
  • $\begingroup$ thanks for that, I took, at least, the reference to Margulis as indicating that the question was intended to be about the chloroplast/plastid origins, did I mistake your intent? $\endgroup$ – terry-s Aug 31 '17 at 8:27
  • $\begingroup$ No at all, this is exactly what the question is about. $\endgroup$ – plannapus Aug 31 '17 at 9:21
  • $\begingroup$ @ben-crowell : (Please ignore my earlier query about how the original question had been edited, Plannapus has explained that and confirmed that the intended subject of the question was indeed about the chloroplast/plastid origins - thanks.) $\endgroup$ – terry-s Sep 1 '17 at 9:30
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The question implicitly assumes that other theoretical explanations had been offered before the theory of symbiogenesis. I believe the truth is that up to a certain point around the later 60s, those active in the field were still too busy identifying constituents and properties of the plastids to think that the time was ripe to offer separate (scientifically-testable) theories of their origin: it does not seem that there were yet any theories of that kind.

Many of the analytical tools and methods of molecular biology that are well-known now did not even exist then. Much of the confidence in evolutionary pathways that exists now comes from nucleic acid sequences, which did not then yet exist. Classical taxonomy without genetic sequence information was an uncertain business.

References that support that the idea was old, but that the questions of evolutionary origin were for a long time untestable and undecidable, include: Schimper A F W (1883) Über die Entwicklung der Chlorophyllkörner und Farbkörner, Botanische Zeitung 41: 105-114 (for a scientifically prudent and restrained mention in a footnote that if it became definitely established that the plastids did not arise anew in the egg-cells (but propagated independently) then 'their relationship to the organism containing them would somewhat remind one of a symbiosis'); Mereschkowsky, C. (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche, Biologisches Centralblatt 25 593-604 (pointing out the lack of evidence supporting the old idea that the green particles arose under control of the cell nucleus from the cytoplasm, but going further and proposing their separate origin); and the same author (1910), in Biologisches Centralblatt, Band 30 (1910), (pages 277-303, 321-347, 353-367) gave an extensive elaboration with his idea of a Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis (theory of two kinds of plasma as a basis of symbiogenesis), but still there was no feasible way to test it.

Heavy disapproval of the idea in the period from about 1925 to the later 1960s is shown first by E B Wilson, The Cell in Development and Heredity (3rd ed. 1925 and 1928 -- described by J T Bonner (The Ideas of Biology, 1962) as 'one of the great books of biology'); and its continuing disrepute can be seen confirmed & reiterated by J T Bonner (in 'The Ideas of Biology', 1962); and by R M Klein & A Cronquist (in Quarterly Review of Biology, vol.42(2), 108-296 at p.167).

The unusually emphatic terms in which the idea was condemned are themselves a noteworthy piece of background to the current question.

For E B Wilson (1925 & 1928) there were already too many unprovable biological conjectures, and he expressed reluctance to create or to entertain any more of them: thus, his preface (p.viii) quoted a predecessor's report, that although a certain biologist had 'rejected two hundred and sixty-two' "groundless hypotheses of development", "nothing is more certain than that [his] own theory formed the two hundred and sixty-third." Wilson then wrote "I have no wish to add another to this list". When he then went on to review Mereschkowsky's theory, he called it an "entertaining fantasy" with "flights of the imagination" (Wilson, 3rd ed., pp.738-9). He qualified that somewhat, acknowledging that "the ... speculation [about chloroplasts] cannot be considered totally baseless in view of the symbiotic union of unicellular green algae with fungi in the lichens", and added that while "many" would rate the speculations "too fantastic for present mention in polite biological society; nevertheless it is within the range of possibility that they may some day call for more serious consideration". In spite of these somewhat positive qualifications, the negative part of Wilson's appraisal seems to have made more impact and to have contributed to adding the endosymbiotic idea to the already-long list of unprovable and disreputable biological conjectures. For a long time it remained out of favor: thus, as late as the 1960s the endosymbiotic idea was described as a "never well-regarded hypothesis" (by J T Bonner, in 'The Ideas of Biology', 1962), and even in 1967, R M Klein & A Cronquist offered reasons for likening the endosymbiotic idea to a "bad penny" (Qtrly Review of Biology, vol.42(2), 108-296 at p.167).

In the face of this weight of professional disapproval it would clearly have been a bold and risky move by anybody to revive the idea without the backup of new and at least potentially weighty and decisive evidence. When Lynn Margulis (previously Lynn Sagan) did reintroduce and revitalize the endosymbiotic idea in her publications of 1967 (L Sagan, The Origin of Mitosing Cells, J Theoret. Biol. 14, 225-274) and 1970 (Origin of Eukaryotic Cells, Yale Univ Press) she did not claim to introduce something quite new; rather, she was proposing ways to make out of the old idea a scientifically testable theory, thus distinguishing her contribution from the ideas that had gone before. For example, the prominent subtitle of her book, with the words "evidence and research implications" emphasized the new and hopefully persuasive means of theory-testing that she proposed.

There is probably no need here to go into the details of those areas where modern techniques have provided decisive evidence and those where they have not, except for one point: at least until recently (2008) there still existed some questions on this topic that arguably still could not be effectively tested even by any of the modern types of evidence. Thus, a review from 2008 (C J Howe, et al., 'The Origins of Plastids', Philosophical Transactions of the Royal Society B 363, 2675-2685), which acknowledges, of course, that the general question whether chloroplasts first arose through symbiosis has been tested, with an affirmative answer now beyond serious doubt. But it also gives reasoned consideration to the question "Can we actually prove (or disprove) anything?" about a still-open problem, whether the different known plastids descend from a single line of organisms that acquired the common endosymbiotic ancestor of all (monophyly). (The alternative possibility would be that there was an independent endosymbiosis for at least one of the current plastid types, thus with different ancestry than the rest (polyphyly).) The limits on testability arise (in the reviewers' prudent and probable opinion) from unavoidable uncertainties, e.g. about limits to the comprehensiveness of achievable taxon sampling, and the narrow effect of any evidence that could be obtained to bear on the problem.

Much of the history has been described by Jan Sapp (1994), in 'Evolution by Association: A History of Symbiosis'.

Finally, to be more specific about the questions originally asked, the original old idea up to the 1880s was that the green particles of plant cells arose from the cytoplasm under control of the nucleus, and by implication shared the same ancestry as the cells in which they occurred.

I do not know whether there is any evidence bearing decisively on the question of a single or multiple origin of photosynthesis in prokaryotes, but the 2008 review mentioned above shows that the question so far as it may be applied to single or multiple evolutionary origin of chloroplasts, actually remained arguably untestable at least as of 2008 (showing that some questions in this field may even indefinitely remain undecidable).

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  • $\begingroup$ Thanks for all those great sources! (For those interested, Schimper (1883) can be found here). $\endgroup$ – plannapus Jul 7 '17 at 11:13
  • $\begingroup$ @plannapus : glad they are of interest! $\endgroup$ – terry-s Jul 7 '17 at 11:37

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