The meaning of Darwin's “abominable mystery”^†

Abstract

Charles Darwin's “abominable mystery” has come to symbolize just about all aspects of the origin and early evolution of flowering plants. Yet, there has never been an analysis of precisely what Darwin thought was so abominably mysterious. Here I explicate Darwin's thoughts and frustrations with the fossil record of flowering plants as revealed in correspondence with Joseph Hooker, Gaston de Saporta, and Oswald Heer between 1875 and 1881. I also examine the essay by John Ball that prompted Darwin to write his “abominable mystery” letter to Hooker in July of 1879. Contrary to what is generally believed, Darwin's abominable mystery has little if anything to do with the fossil prehistory of angiosperms, identification of the closest relatives of flowering plants, questions of the homologies (and character transformations) of defining features of flowering plants, or the phylogeny of flowering plants themselves. Darwin's abominable mystery and his abiding interest in the radiation of angiosperms were never driven primarily by a need to understand the literal text of the evolutionary history of flowering plants. Rather, Darwin was deeply bothered by what he perceived to be an abrupt origin and highly accelerated rate of diversification of flowering plants in the mid-Cretaceous. This led Darwin to create speculative arguments for a long, gradual, and undiscovered pre-Cretaceous history of flowering plants on a lost island or continent. Darwin also took refuge in the possibility that a rapid diversification of flowering plants in the mid-Cretaceous might, if real, have a biological explanation involving coevolutionary interactions between pollinating insects and angiosperms. Nevertheless, although generations of plant biologists have seized upon Darwin's abominable mystery as a metaphor for their struggle to understand angiosperm history, the evidence strongly suggests that the abominable mystery is not about angiosperms per se. On the contrary, Darwin's abominable mystery is about his abhorrence that evolution could be both rapid and potentially even saltational. Throughout the last years of his life, it just so happens that flowering plants, among all groups of organisms, presented Darwin with the most extreme exception to his strongly held notion natura non facit saltum, nature does not make a leap.

I have just read Ball's Essay. It is pretty bold. The rapid development as far as we can judge of all the higher plants within recent geological times is an abominable mystery. Certainly it would be a great step if we could believe that the higher plants at first could live only at a high level; but until it is experimentally [proved] that Cycadeae, ferns, etc., can withstand much more carbonic acid than the higher plants, the hypothesis seems to me far too rash. Saporta believes that there was an astonishingly rapid development of the high plants, as soon [as] flower-frequenting insects were developed and favoured intercrossing. I sh^d like to see this whole problem solved. I have fancied that perhaps there was during long ages a small isolated continent in the S. hemisphere which served as the birthplace of the higher plants—but this is a wretchedly poor conjecture. —Excerpt of a letter written by Charles Darwin on 22 July 1879 to Joseph Hooker

Charles Darwin's fascination and frustration with the epic set of evolutionary events associated with the origin and early radiation of flowering plants are legendary. Perhaps no other group of organisms merited Darwin's attention in such dramatic terms: “abominable mystery,” “most perplexing phenomenon,” “nothing... more extraordinary.” But of all of the comments made by Darwin about the early evolutionary history of flowering plants, his “abominable mystery” has captured the imaginations of generations of plant biologists. Beginning just months after Darwin's letter of 22 July 1879 to Joseph Hooker (Figs. 1A–G1B1C1D1E1F1G) was first published in More Letters of Charles Darwin (17), biologists have used the phrase “abominable mystery” unabated, through the modern synthesis and on to the current synthesis of molecular phylogenetics, developmental genetics, morphology, and paleobotany (e.g., 55; 29; 59; 45; 54; 62; 1; 58; 47; 12, 3; 3; 6; 39; 18; 22; 23; 26; 60). A Google search of the internet for “abominable mystery” and “Darwin” will yield hundreds (if not thousands) of results, often in science headlines referring to the mystery as “solved.”

Figure 1A–1G

Letter from Charles Darwin to Joseph Dalton Hooker, written 22 July 1879 (provenance: Cambridge University Library DAR 95: 485–488). In this letter, Darwin refers to the early evolution of flowering plants as an “abominable mystery.” He also shows his interest in Gaston de Saporta's idea that a coevolutionary set of interactions between angiosperms and insects may have been central to the rapid diversification of flowering plants in the mid-Cretaceous. This letter is a wonderful example of Darwin's correspondence with Hooker, filled with the exchange of scientific information and queries, updates on Darwin's writing and publications, family matters (holiday), and the mundane (problems of scale infestation on a plant lent to Darwin from Kew). Darwin's handwriting is often very difficult to decipher, but the handwriting in this letter is actually quite good compared to others from this late period of his life (E. Smith, Darwin Correspondence Project, Cambridge University Library, personal communication). A transcription of the letter follows. Note that the penciled numbers 485, 486, 487, and 488 that appear on pages one, three, five, and seven are the class marks associated with the archives at Cambridge University Library. On the first page, the “/79” after the date and the annotation at left “sent July 23/79” are in pencil and may have been added by Francis Darwin when he transcribed and published parts of this letter in 1903. On the last page of the letter, the penciled “No” may have been added by Joseph Hooker in response to Darwin's query about returning the scale-infested Smilax plant to Kew. Digital images of this letter from the Darwin collection, courtesy of Cambridge University Library.

Fig. 1A. Letter from Charles Darwin to Joseph Dalton Hooker, written 22 July 1879, page 1. My dear Hooker If my memory serves me rightly Dyer [William Turner Thiselton-Dyer, Assistant Director of Kew Gardens] has left Kew for his holidays, and so I write to you to ask you if by any chance you have seeds of Lathyrus aphaca or any young seedlings 2 or 3 of which could be potted. If I receive no answer I shall understand that you cannot aid me. — I want to try whether the tendrils are apheliotropic, for I record that they revolve very little, I conjecture that they may find

Figure 1B

Letter from Charles Darwin to Joseph Dalton Hooker, written 22 July 1879, page 2. a support by bending toward any dark objects. — Our book on the movements of Plants [The Power of Movement in Plants, 1880, written by Charles Darwin and “assisted” by his son Francis Darwin] will, I think, contain a good deal of new matter, but will be intolerably dull. I have been working pretty hard of late & want rest & change, so we all go on August 1^st to Coniston for a month. It is an awful journey to me. — It is a long time since I have heard any news of you & yours & what you are doing & intending

Figure 1C

Letter from Charles Darwin to Joseph Dalton Hooker, written 22 July 1879, page 3. to do. Frank [Francis] comes back in the beginning of next month from Würzburg, where he has been working pretty hard on various subjects and practicing dissection, cutting slices &c. I have just read Ball's essay. It is pretty bold. The rapid development, as far as we can judge, of all the higher plants within recent geological times is an abominable mystery. Certainly it w^d be a great step if we could believe that the higher plants at first could live only at a high level; but until it is experimentally [proved]

Figure 1D

Letter from Charles Darwin to Joseph Dalton Hooker, written 22 July 1879, page 4. that Cycadeæ, ferns etc., can withstand much more carbonic acid than the higher plants, the hypothesis seems to me far too rash. Saporta believes that there was an astonishingly rapid development of the high plants, as soon [as] flower-frequenting insects were developed & favoured intercrossing. I sh^d like to see this whole problem solved. I have fancied that perhaps there was during long ages a small isolated continent in the S. hemisphere, which served as the birth place of the higher plants; but this

Figure 1E

Letter from Charles Darwin to Joseph Dalton Hooker, written 22 July 1879, page 5. is a wretchedly poor conjecture. It is odd that Ball does not allude to the obvious fact that there must have been alpine plants before the Glacial period, many of which would have returned to the mountains after the Glacial period when the climate again became warm. I always accounted to myself in this manner for the Gentians etc.

Figure 1F

Letter from Charles Darwin to Joseph Dalton Hooker, written 22 July 1879, page 6. Ball ought also to have considered the Alpine insects common to the arctic regions. I do not know how it may be with you, but my faith in the Glacial migration is not at all shaken. Ever my dear old friend yours truly Ch. Darwin

Figure 1G

Letter from Charles Darwin to Joseph Dalton Hooker, written 22 July 1879, page 7. P.S. I shall have to return some plants to Kew when we leave home. — Your plant of Smilax aspera has been injured by scale insects which were only lately detected. — Is this worth returning? It is a large bush.

Over the course of the last century, Darwin's abominable mystery has become synonymous with the complexities and often seemingly impenetrable questions surrounding the origin and earliest phases of angiosperm evolutionary history. Meanings ascribed to Darwin's abominable mystery are highly variable and include the phylogenetic relationships of angiosperms to other seed plant lineages; the phylogenetic relationships of major clades within angiosperms; the search for the fossil precursors of flowering plants; the search for the earliest fossil flowering plants; the evolutionary origin of the flower, the carpel, and myriad other questions of the homologies of unique angiosperm characteristics; and the relatively abrupt rise to ecological dominance of angiosperms during the Cretaceous.

Beyond the simple excision of this two-word phrase from Darwin's voluminous writings, it is worth asking what precisely Darwin (Fig. 2) was pondering when he wrote of an “abominable mystery.” This important question has never truly been addressed, except in the most general sense that Darwin was perplexed by the origin and early history of flowering plants. Given the universal inclination to quote Darwin whenever possible, it seems only fitting that Charles Darwin's thoughts about these seminal evolutionary events be systematically analyzed. As will be seen, from the 1870s through to the very last year of his life, Charles Darwin was fundamentally perplexed by the early evolutionary history of angiosperms—and there is quite a bit more to Darwin's abominable mystery than can be captured in a two-word phrase.

Figure 2

Charles Darwin in 1877 and 1878. Left. Darwin in 1878, photographed by his son Leonard. Right. Darwin on his horse “Tommy” at Down House in the late 1870s. Below a copy of this photograph, he wrote “Hurrah — no letters today!” His comment is a wonderful reminder of the extreme importance of the highly efficient British mail service in ensuring that his vast correspondence with colleagues around the world, including those who helped shape his views on the “abominable mystery,” made it to and from Down House. Images of Darwin from the Darwin collection, courtesy of Cambridge University Library.

What was Darwin's abominable mystery?

Darwin's particular fascination and frustration with the early evolution of angiosperms appear to have begun in earnest several years before his oft-quoted letter (22 July 1879) to Joseph Hooker (Fig. 3). In correspondence (8 March 1875) with the Swiss botanist, entomologist, and paleontologist Oswald Heer (Fig. 3), Darwin went so far as to note that the “sudden appearance of so many Dicotyledons in the Upper Chalk appears to me a most perplexing phenomenon to all who believe in any form of evolution, especially to those who believe in extremely gradual evolution, to which view I know that you are strongly opposed” (17, p. 239). Heer had been a proponent of the potential for rapid (in essence punctuational or saltational) evolution, much to Darwin's dismay.

Figure 3

The key correspondents with Charles Darwin in his discussions of the early evolution of flowering plants. Top left. Joseph Dalton Hooker in 1877 at La Veta Pass in Colorado, USA. Top right. Oswald Heer (1809–1883), date unknown. Reproduced from Oswald Heer: Lebensbild eines schweizerischen Naturforschers (53). Bottom left. John Ball (1818–1889), date unknown. John Ball was an avid naturalist, who studied with Henslow at Cambridge. As Under-Secretary of State at the Colonial Office, he promoted the botanical interests of the Royal Botanic Gardens at Kew (34; 19) and was an alpine expert and botanist. An obituary notice by 34 provides an excellent sketch of his life. Reproduced from Sir Joseph Dalton Hooker, Traveler and Plant Collector (19). Bottom right. Gaston de Saporta (1823–1895), between 1880 and 1885.

The early angiosperm fossil record that confronted Charles Darwin, Oswald Heer, and others (including John Ball and Gaston de Saporta as discussed later) in the mid-1870s was rich in terms of the mid to Late Cretaceous radiation of angiosperms, but virtually devoid of representation of the Early Cretaceous beginnings of angiosperm evolution. Although stratigraphic resolution at the time was rudimentary, anyone interested in the early evolutionary history of flowering plants would clearly have recognized the contrast between the virtual absence of angiosperms in the Early Cretaceous and their clear ascension to ecological and biogeographical dominance by the Late Cretaceous.

In dramatic terms, Oswald Heer explicitly discussed the early angiosperm fossil record with Darwin in a letter dated 1 March 1875 (at the time, Heer was in the midst of publishing a seven volume series, Flora Fossilis Arctica, 1868–1883). Heer wrote (provenance: Cambridge University Library, DAR 166: 130): “In Europe, the Dicotyledons of the Lower Cretaceous are also missing; they do however occur in great profusion in the Upper Cretaceous…both in Europe and America… [I]t is possible that some of these kinds [dicotyledonous angiosperms] may yet be discovered there [in the Lower Cretaceous of Europe and America]. Even so, if we say that the Dicotyledons begin with the Upper Cretaceous, we must still concede that this section of the vegetable kingdom, which forms the bulk of modern vegetation, appears relatively late and that, in geological terms, it underwent a substantial transformation within a brief period of time.”

Charles Darwin's understanding of the fossil record, as it was known in 1875, was absolutely clear: the early diversification and biogeographical spread of angiosperms had been remarkably rapid. This abrupt and relatively widespread appearance of apparently near-modern angiosperm diversity in the mid-Cretaceous, with little if any antecedent fossil record, placed Darwin in a most uncomfortable position. Should the fossil record be an accurate indicator of past events, it presented a strong challenge to his general notion of gradualism as the modus operandi of transformation, although Darwin certainly accepted the possibility of some rapid evolutionary change (42; 28; 48; 27). This, in turn, led Darwin on a six-year odyssey to explain either an extremely rapid pace of evolutionary diversification or a strikingly long and missing fossil record of the earliest (and gradual) phases of angiosperm evolution. As Mayr has noted (1982, p. 509), “All of his life Darwin took great pains to reconstruct a gradual evolution of phenomena that at first sight seemed clearly the result of sudden origins.”

Darwin's solution to the abominable mystery

Darwin's tendency to hew to a gradualist perspective on the pace of evolutionary innovation led him to posit that prior to the Cretaceous record of flowering plants, angiosperms had slowly evolved and diversified on a remote (and no longer present) landmass, perhaps in the southern hemisphere. As a consequence, flowering plants were absent from the fossil record until the mid-Cretaceous when they finally expanded beyond this limited territory. As Darwin put it to Heer, “plants of this great division must have been largely developed in some isolated area, whence owing to geographical changes, they at last succeeded in escaping, and spread quickly over the world” (letter to Oswald Heer, 8 March 1875; 17, p. 240). Four years later, Darwin again alluded to this idea in his abominable mystery letter to Hooker (17, pp. 21, 22): “I have fancied that perhaps there was during long ages a small isolated continent in the S. Hemisphere which served as the birthplace of the higher plants—but this is a wretchedly poor conjecture.”

Nearing the end of his life, Darwin returned to the notion of a lost fossil record of the earliest phases of angiosperm diversification (16, p. 248) in a letter to Hooker (6 August 1881). “Nothing is more extraordinary in the history of the Vegetable Kingdom, as it seems to me, than the apparently very sudden or abrupt development of the higher plants. I have sometimes speculated whether there did not exist somewhere during long ages an extremely isolated continent, perhaps near the South Pole.” Darwin's stress on the word “apparently” reveals his deeply rooted recognition that the fossil record could be remarkably incomplete, as well as his continuing skepticism that a major evolutionary radiation of the magnitude seen (as of 1881) with mid-Cretaceous angiosperms could really be so abrupt.

Less than a week later (letter of 11 August 1881; 17, p. 26), Darwin reiterated these same points to Hooker. “I have been so astonished at the apparently sudden coming in of the higher phanerogams, that I have sometimes fancied that development might have slowly gone on for an immense period in some isolated continent or large island, perhaps near the South Pole.” This letter appears to contain Darwin's last recorded words on the early evolution of angiosperms.

How Darwin came to write of the abominable mystery

Darwin's 22 July 1879 abominable mystery letter to Hooker directly relates to his keen desire to moderate the perceived rapid rate of early angiosperm diversification. The stimulus for this letter was Darwin's reading of the essay “On the origin of the flora of the European Alps,” delivered by John Ball (Fig. 3) to a meeting of the Royal Geographical Society on 9 June 1879 and subsequently published in September of that year (2). In this paper, which is largely concerned with biogeographical aspects of alpine floras, Ball also directly addressed the question of the early evolutionary history of angiosperms. In a letter to Darwin dated 8 August 1879, Ball noted he had arranged for a preprint of this publication to be sent to Darwin earlier that summer. Thus, we can safely assume that Darwin had this manuscript in hand no later than June or July of 1879.

Ball's essay (1879, p. 579) provides an important window into the fossil record of angiosperms that confronted Darwin in the late 1870s. “[T]he appearance of the higher type of exogenous plants [dicotyledonous angiosperms] is not disclosed by direct evidence until about the middle of the [C]retaceous period. Then all at once, in deposits widely spread over the northern hemisphere, we encounter a crowd of species, belonging to very different types, but for the most part so nearly resembling living plants, that palæontologists do not hesitate to refer many of them to existing genera.” Ball (p. 580) then posed the question succinctly. “But if, at the commencement of the earliest chapter of the history accessible to us, the evolution of the flowering plants, and especially of the exogens [dicotyledonous angiosperms], had already proceeded so far, where, I would ask, must we look for the earlier forms, the ancestral types from which our present groups have sprung? And where again for the much more remote forms which served to bridge over the interval, so perplexing to the botanist, between the endogens [monocots] and the exogens?”

Perhaps unwittingly, Ball captured the essence of Darwin's angiosperm dilemma. “To my mind there is no alternative between abandoning the doctrine of evolution and admitting that the origin of the existing types of flowering plants is enormously more remote than the period as to which we have direct evidence. The difficulty to be got over is the utter absence of such evidence” (2, p. 580). As Darwin had confessed to Heer four years earlier (and noted above), the “sudden appearance of so many Dicotyledons in the Upper Chalk appears to me a most perplexing phenomenon to all who believe in any form of evolution, especially to those who believe in extremely gradual evolution” (17, p. 239).

Ball reasoned that angiosperms first evolved in the alpine. Critically, he argued (2, p. 579) that since “only by the rarest of chances can a plant from the upper mountain region be preserved [fossilized],” a long pre-Cretaceous history of angiosperms was entirely absent from the fossil record until flowering plants later descended to lower elevations (where fossilization would be common). Ball's hypothesis began with the insight that atmospheric carbon dioxide levels during the Carboniferous were exceedingly high (Ball claimed 20 times greater than present) and subsequently declined, largely as a result of coal formation (carbon burial). To this, Ball additionally speculated that carbon dioxide levels decrease with elevation. Finally, Ball conjectured that flowering plants were unable to withstand high levels of atmospheric carbon dioxide (in contradistinction to other groups of plants). Thus, a long period of angiosperm evolution (dating to the Carboniferous) would have been confined to the alpine until global atmospheric carbon dioxide levels dropped significantly (17).

As Hooker remarked to Darwin, in a letter dated 26 July 1879 (provenance: Cambridge University Library, DAR 104: 128–130), “I think it very unsatisfactory in more ways than one… & I am sure you have had enough of Ball whom we will discuss when we meet.” In print, Hooker was far more diplomatic (in the published written comments by Hooker following the paper by 2): “[Ball's] speculations on the origin of the Floras in question, as affected by the presence of that gas under former conditions of the globe, had really taken his [Hooker's] breath away.” Darwin too was skeptical, as he made clear to Hooker in his abominable mystery letter. “Certainly it would be a great step if we could believe that the higher plants at first could live only at a high level; but until it is experimentally [proved] that Cycadeae, ferns, etc., can withstand much more carbonic acid than the higher plants, the hypothesis seems to me far too rash.” Nevertheless, there is a bit of wishful thinking on the topic of a missing early angiosperm fossil record because Darwin notes that it “would be a great step” if Ball's hypothesis could be proven.

Ball's hypothesis of an alpine origin of angiosperms intrigued Darwin. It represented the exact same line of argumentation found in his private letters: (1) that the abrupt appearance of diverse angiosperms in the mid-Cretaceous was illusory; (2) that a long period of angiosperm evolution preceded what was then known from the mid-Cretaceous; and (3) that there was no fossil record of the gradual diversification of angiosperms prior to the Cretaceous. The only real difference between Ball and Darwin was that Ball assumed a long early history of angiosperms had never entered the fossil record, whereas Darwin posited it had been preserved geologically on a remote island or continent, but that the land mass had disappeared from the face of the earth.

An alternative solution to the abominable mystery

In contrast to Darwin's view that the initial diversification of angiosperms had been gradual, but unrecorded in the fossil record, an alternative explanation of the mid-Cretaceous flowering plant radiation was developed and brought to his attention by the French paleontologist Gaston de Saporta (Fig. 3). Darwin revealed to Saporta (10 September 1876; 7, p. 93) that with “respect to the sudden development of dicotyledinous [sic] plants, which view Heer likewise maintains, I confess that I am sceptical.” In this letter, Darwin went on to repeat his default explanation: “It is of course a mere conjecture, but I imagine that this great group of plants must have been slowly developed in some part of the globe which was formerly more completely isolated from all other regions than any part of the land now is. I have always felt the keenest interest in your observations on the very gradual change of species during the later Tertiary periods, and I observe that A. de Candolle has likewise been struck with these observations which are strongly opposed to Heer's belief of great and abrupt specific changes.”

Saporta, like Darwin, was perplexed by the seemingly abrupt origin and rapid diversification of angiosperms, as manifest in the fossil record (“un phénomène des plus curieux”). Unlike Darwin, however, Saporta began with the premise that a rapid rate of diversification of angiosperms in the mid-Cretaceous might be real and could be explained on biological principles. Importantly, Saporta's hypothesis did not require a long unrecorded history of angiosperms prior to the Cretaceous.

Saporta had already developed a general theory that could provide a biological basis for the rapid diversification of flowering plants. In the second section of the introduction to Paléontologie Française, Plantes Jurassiques, 50 argued that the strong interdependence of animals and plants required an understanding of their various linked phases of evolutionary history and he described a ratcheting mechanism of coevolution between animals and plants (7). Specifically, Saporta reasoned that the essential absence of angiosperms from the Jurassic made it impossible for many forms of animals, particularly those that were phytophagous, to evolve. As 7 and 13 have noted, 50 was the first to suggest a critical and interdependent role of insects in the emergence and diversification of angiosperms.

In his correspondence with Charles Darwin, Saporta elaborated on the theme of coevolutionary interdependence between insects and flowering plants—and this time, he tied his reading of the fossil record to issues associated with rates of diversification, the very essence of Darwin's “abominable mystery.” In a letter that is notable for its brilliance and insights, Saporta explicitly proposed to Darwin (16 December 1877; provenance: Cambridge University Library, DAR 177: 34; also note that the transcription used for this translation differs from that published by 7, pp. 98–99) that the rapid diversification of angiosperms was, in essence, a coevolutionary story tied to the origin of many major groups of insects: “You know how the delayed evolution of Dicotyledons has always preoccupied me, as one of the most curious phenomena, as much by its immense importance, as by the apparent speed with which it was formerly manifest. Now, the role that you attribute to Insects in fertilization [pollination], coupled with the need for crossing, explains everything: the earlier poverty of the plant kingdom, reduced for so long in the absence of certain categories of insects, to anemophilous plants alone, whose number and diversity were never able to exceed a certain limit, and in which nutritive and succulent substances were never very abundant nor well diversified. The absence of sucking insects during the Jurassic had struck me as well as Mr. Heer. I mentioned this absence or its rarity in my introduction to the Jurassic flora, vol. 1, pp. 53 and 54…

“Now one can conceive very well that the angiosperms, whose floral combinations and crossings of individuals to individuals and of flower to flower depend on the role of insects, could only appear and increase under the impetus of the latter, and the latter for their part, could become numerous and active [as pollinators], and cling to a certain determined type, for which reason the appearance of plants favoured their existence; insects and plants have therefore been simultaneously cause and effect through their connection with each other, plants not being able to diversify without insects and the latter not being able to provide many pollen and nectar feeders so long as the plant kingdom remained poor in arrangements and was composed almost exclusively of anemophilous plants.”

Darwin responded immediately to Saporta (letter of 24 December 1877; 7, p. 109). “Your idea that dicotyledonous plants were not developed in force until sucking insects had been evolved seems to me a splendid one. I am surprised that the idea never occurred to me, but this is always the case when one first hears a new and simple explanation of some mysterious phenomenon… [Y]our idea, which I hope you will publish, goes much further and is much more important…” Darwin recognized the seminal importance of Saporta's hypothesis and was thus provided with a plausible, indeed powerful, mechanism to explain the rapid pace of early (meaning mid-Cretaceous, as of 1877) angiosperm diversification: the accelerating effects of the coevolution of pollinating insects and flowers, and the potential benefits of enhanced outcrossing associated with entomophily.

Darwin did not forget Saporta's ideas. A year and half later, in his abominable mystery letter to Joseph Hooker, Darwin related, “Saporta believes that there was an astonishingly rapid development of the high plants, as soon [as] flower-frequenting insects were developed and favoured intercrossing.” In 1881 (6 August letter to Joseph Hooker; 17, p. 248), Darwin again returned to Saporta's ideas: “Hence I was greatly interested by a view which Saporta propounded to me, a few years ago, at great length in MS, and which I fancy he has since published, as I urged him to do—viz., that as soon as flower-frequenting insects were developed, during the latter part of the secondary period, an enormous impulse was given to the development of the higher plants by cross-fertilization being thus suddenly formed.” It is worth noting that in these two letters, Darwin focused on the presumed benefits of outcrossing to promote diversification, while Saporta had primarily emphasized the coevolutionary dynamics of anthophilous insects and flowering plants. Saporta would go on to elaborate considerably on the early coevolution of insects and angiosperms in the second volume of L’Évolution du Règne Végétal (51).

Thus, in ways that have previously not been appreciated, Darwin was at least partially responsible for stimulating the publication of the single most accepted hypothesis as to the cause of the rapid radiation of flowering plants, namely, their coevolution with insects (for ongoing discussions of angiosperm–insect coevolution, see 20; 46; 47; 10, 9; 43; 36; 49; 21; 31; 30; 52). Moreover, Saporta's solution to Darwin's skepticism about the “sudden development” of flowering plants was the only explanation Darwin ever embraced to potentially explain a rapid diversification of early angiosperms as real.

Does the abominable mystery include the origin of angiosperms?

Darwin's abominable mystery has commonly, throughout the 20th and nascent 21st centuries, been interpreted to include questions of character evolution or transformation associated with the origin (as contrasted with their subsequent diversification) of flowering plants from their nonangiosperm ancestors. As 58, p. 457) put the case (reflecting a viewpoint that dates to the early 1900s): “About a hundred years ago, Charles Darwin referred to the origin of the Angiosperms as an ‘abominable mystery.’ Modern research, although it has shed light on many of the problems which in Darwin's day were mysterious and unsolved, has done little to clarify this problem. It still occupies the thoughts of many botanists interested in evolution, to their bewilderment and frustration. The reasons for this difficulty are manifold, but lie chiefly in the imperfection of the fossil record. Clear evidence regarding the origin and early evolutionary history of angiosperms would need to consist of a series of well preserved reproductive structures connecting the most primitive angiosperms with non-angiospermous seed plants [italics added]…”

Although Darwin was clearly perplexed by a seemingly abrupt origin and rapid rate of diversification of angiosperms, he does not appear to have explicitly considered the evolution of the many unique characteristics of flowering plants (questions of homology) from their nonangiosperm ancestors. Underlying his sense of bewilderment with the origin and early evolution of angiosperms certainly lay a problem with the preangiosperm fossil record and the phylogeny of seed plants. Darwin's extensive correspondence with paleobotanists describing the Jurassic and Cretaceous plant record makes clear that the immediate prehistory of flowering plants was, at least tangentially, of interest to him. Nevertheless, Darwin does not appear to have pondered specific character transformations that would have been central to the establishment of defining features of flowering plants (e.g., the flower, carpel, embryo sac, and so forth)—nor is there evidence that he worried about the identification of the ancestors of flowering plants. In view of Darwin's longstanding recognition of the inadequacies of the fossil record (discussed later) and his embrace of the hypothesis that flowering plants may have been evolving for an extended period of time in a remote area of the southern hemisphere, it is fair to conclude that he simply did not look to the fossil record for data that could speak to the homologies and transformations that gave rise to defining angiosperm characteristics.

The abominable mystery has also been invoked in modern times in reference to phylogenetic relationships among extant seed plants and specifically to the identity of the closest living relatives of angiosperms. Although the analysis of seed plant phylogeny was well underway during Darwin's later years (e.g., Ernst Haeckel, writing in the 1870s and 1880s in his seminal work The History of Creation: Or the Development of the Earth and Its Inhabitants, viewed Gnetales as being most closely related to angiosperms), his writings and correspondence do not dwell on this topic.

Darwin was essentially agnostic on the question of relationships within seed plants and acknowledged this late in 1861 in a letter to Joseph Hooker (17, p. 281; letter of 28 December 1861): “I wrote carelessly about the value of Phanerogams; what I was thinking of was that the sub-groups seemed to blend so much more one into another than with most classes of animals.” In 1862 and 1863, when Joseph Hooker was in the midst of an intensive examination of the vegetative, reproductive and embryological features of Welwitschia (33), Darwin took note (letter of 6 October 1862; 4) of Hooker's belief that the Gnetales (and Welwitschia in particular) could be viewed as intermediate in character between the gymnosperms and angiosperms (“it does seem a most grand case to connect two such groups”).

The evidence strongly suggests that Darwin did not intensively ponder the question of hypothesized angiosperm relatives and their potential evolutionary significance. While the origin of angiosperms from nonangiosperm seed plants remains problematic, even to this day (e.g., 24; 41; 5), questions of homology and character transformation, and issues of the identification of angiosperm ancestors and closest relatives, were not a central part of Darwin's curiosity and frustration with the evolutionary history of flowering plants.

Natura non facit saltum, the heart of Darwin's abominable mystery

Over the course of the last century, Darwin's “abominable mystery” has become broadly synonymous with the complexities and often seemingly impenetrable questions surrounding the prehistory, origin, and early phases of angiosperm evolutionary history. Nevertheless, few, if any, of these topics, as they relate specifically to flowering plants, appear to have been uppermost in Darwin's mind at any point in his life. And this leads to a final and critical set of considerations: is Darwin's abominable mystery really about angiosperms?

In the concluding chapter to every edition of the Origin of Species (with only a word change or two), Darwin wrote: “As natural selection acts solely by accumulating slight, successive, favourable variations, it can produce no great or sudden modification; it can act only by very short and slow steps. Hence, the canon of ‘Natura non facit saltum [nature does not make a leap],’ which every fresh addition to our knowledge tends to make more strictly correct…” (14, first edition, p. 471; essentially similar in 15, sixth edition, pp. 413–414). The emerging fossil record of angiosperms in the decades of the 1860s and 1870s, however, presented Darwin with the most explicit contravening evidence to his gradualist perspective on macroevolutionary change.

Angiosperms were not the first group to confront Darwin with a stark absence of paleontological data for a gradual diversification phase antecedent to a seemingly abrupt morphological and biogeographical radiation. In every edition of the Origin of Species, Darwin devoted two sections in the chapter “On the Imperfection of the Geological Record” to this very topic: “On the sudden appearance of whole groups of Allied Species” and “On the sudden appearance of groups of Allied Species in the lowest known fossiliferous strata.” Darwin realized that, if seemingly abrupt origins of diverse members of whole groups of organisms were in fact real, this could (and indeed would) be taken as evidence concordant with a creationist (supernatural) mode of species formation. Thus, it is essential to understand that Darwin's gradualist sympathies and his general rejection of saltationism, beyond their obvious resonance with his view of the process of natural selection, were also central to his arguments against a creationist explanation of the fossil record. “The abrupt manner in which whole groups of species suddenly appear in certain formations, has been urged by several palæontologists, for instance, by Agassiz, Pictet, and by none more forcibly than by Professor Sedgwick, as a fatal objection to the belief in the transmutation of species. If numerous species, belonging to the same genera or families, have really started into life all at once, the fact would be fatal to the theory of descent with slow modification through natural selection. For the development of a group of forms, all of which have descended from some one progenitor, must have been an extremely slow process; and the progenitors must have lived long ages before their modified descendants” (14, first edition, p. 302; essentially similar in 15, sixth edition, p. 282).

In a deft tactical maneuver, Darwin set the stage for a solution to this perceived “fatal” challenge to his theory of evolution by descent with gradual modification. “[W]e continually over-rate the perfection of the geological record, and falsely infer, because certain genera or families have not been found beneath a certain stage, that they did not exist before that stage. We continually forget how large the world is, compared with the area over which our geological formations have been carefully examined; we forget that groups of species may elsewhere have long existed and have slowly multiplied before they invaded the ancient archipelagoes of Europe and of the United States” (14, first edition, p. 302; essentially similar in 15, sixth edition, p. 282). Darwin continues, “I will now give a few examples to illustrate the foregoing remarks, and to show how liable we are to error in supposing that whole groups of species have suddenly been produced” (14, first edition, p. 302; identical in 15, sixth edition, p. 283). With this, Darwin launches an empirical counterattack against the vagaries of the fossil record by describing what had been viewed (prior to the publication of Origin of Species) as the seemingly abrupt origins of diverse representatives of mammals, birds, sessile barnacles, teleost fishes, and trilobites. In every instance, he argued that what had, only years earlier, appeared as a sudden origin of diverse members of each group, could now be shown to have a significant prior record of transitional fossils compatible with his gradualist views of transmutation.

These passages from the Origin of Species presage the strategy Darwin later employed to attack the abominable mystery of the seemingly sudden and geographically widespread appearance of diverse angiosperms in the fossil record. Darwin's ideas in the Origin of Species are clearly predicated on the assumption that biological innovation and diversification are gradual, as he would later argue in the case of flowering plants. Moreover, Darwin notes that the early evolution of a lineage may be geographically restricted (remote from Europe and North America, where most paleontology was then being undertaken), and as such, undiscovered in the fossil record. The parallel with a lost island or continent in the southern hemisphere, in the case of angiosperms, is exact.

By the 1870s, Darwin had experienced a series of intellectual and tactical battles over various groups of metazoans that had seemingly appeared suddenly in the fossil record. Critically, his bias in favor of gradualist explanations of transmutation emerged during a period marked by a burgeoning, yet highly incomplete, fossil record for most groups of organisms. This led him to seek explanations for seemingly abrupt origins and diversifications of major lineages of animals and plants as presented in the known fossil record of his times. Yet, in each instance, but one, Darwin's geological and evolutionary “problems” were resolved as paleontological exploration succeeded in filling the missing gaps. Darwin had every reason to believe that time was on his side.

When Darwin began to critically examine (and correspond about) the angiosperm fossil record, evidence for a gradual diversification of flowering plants prior to their abrupt and diverse appearance (as known in the 1870s) in the mid-Cretaceous eluded him. As late as 1878 (16 February), Saporta reiterated to Darwin, in reference to the fossil record of flowering plants (provenance: Cambridge University Library, DAR 177: 35), “Since there are no traces of Dicotyledons before the mid-Cretaceous… the first definable types seem from this time adorned with their discriminating characteristics and fixed in their main features. This absence of primordial [transitional] forms makes a passage to the stem [group]–mothers from which the whole class had to emerge… a problem all the more obscure—The difficulty is all the greater and the less easy to grasp, that it is not the same for mammals where one can observe almost every transition and sequence leading from one type to another definitive group.” Darwin came to his abominable mystery, not because of a specific or programmatic curiosity about the broad scale evolutionary history of flowering plants, but rather, because angiosperms, among all groups of living organisms, presented the greatest continuing challenge to his views on the pace of evolutionary innovation and his clear recognition that the fossil record remained substantially incomplete.

Throughout his life, Darwin was obsessively interested in adaptation and in the cumulative small changes that create new innovations of biology. Questions of the evolutionary history (e.g., homology and character transformation) of particular groups of organisms, while certainly of general concern to Darwin, were rarely, if ever, the motivating features of his inquiries. His letters clearly show that he was not particularly interested in angiosperm or seed plant phylogeny, nor was he obsessed with tracking the fossil prehistory of flowering plants. There is no indication that Darwin concerned himself with the homologies of the flower and its organs (as, for example, had Goethe in 1790).

Charles Darwin's abominable mystery was never truly about flowering plants per se. Charles Darwin's abominable mystery was, in essence, one of rate: how to explain periods of seemingly abrupt and highly accelerated diversification associated with the origins of major groups of organisms—and in this case, and only incidentally, for angiosperms. This is precisely why Darwin returned to the topic of Heer's saltationist views in his correspondence, both with Heer himself, and with Saporta. Darwin could not accept that the pace of evolutionary innovation could be so very rapid—and angiosperms (as known in the 1870s and 1880s) appeared to present a significant exception to this deeply held notion.

Concluding remarks

When Darwin went to his grave (actually, not the grave where he expected to be buried in Downe churchyard with his family, but rather Westminster Abbey) the fossil record still presented evidence of a seemingly abrupt origin and extremely rapid evolutionary and biogeographic diversification of flowering plants. Thus, it is worth briefly addressing whether Darwin's “abominable mystery,” specifically with respect to angiosperms, has been “resolved” in the interim between 1882 and the present.

We now know that the earliest phases of angiosperm diversification, as witnessed in the fossil record, demonstrate a period of relatively gradual and orderly diversification prior to the mid-Cretaceous (see 25 for review). This Early Cretaceous record of angiosperms, with its floras dominated by small-flowered species, was entirely unknown to the paleontologists of Darwin's time (or even 30 years ago). As such, the earliest manifestation of angiosperms, as now understood, appears to be significantly less abrupt than that of the fossil record Heer and Saporta described in the 1870s and 1880s. In many ways, the recently unearthed record of early angiosperms conforms to the patterns that Darwin took comfort in as he embraced the discoveries of early transitional fossils for mammals, birds, sessile barnacles, teleost fishes, and trilobites in the Origin of Species. Obviously, such speculations are open to debate, but Darwin might well have been satisfied to add angiosperms to his list of examples “to show how liable we are to error in supposing that whole groups of species have suddenly been produced” had he had access to our current record of Early Cretaceous flowering plants.

It is notable that both Darwin and Ball were correct in concluding that the early fossil record of angiosperms, as it stood in the 1870s, was fundamentally incomplete. Both keenly understood that the seemingly abrupt origins of many differentiated (derived) members of a large group of organisms, without a fossil record of transitional ancestors, was not concordant with an evolutionary schema of species origin and higher level diversification. In essence, both predicted that there must have been a period of angiosperm diversification antecedent to the mid-Cretaceous. Their predictions, with respect to angiosperms, have been borne out perfectly.

Despite the vagaries of mid-19th century stratigraphy, the essence of the mid through Late Cretaceous (and Early Tertiary) radiations of various angiosperm clades was apparent to Darwin. Current qualitative measures continue to indicate that rates of morphological, ecological, and taxonomic diversification within angiosperms during the mid through Late Cretaceous and Early Tertiary were high (44; 8; 61; 37; 9; 11, 3; 38; 40; 25). It has been suggested that the profound expansion of the mid to Late Cretaceous and Early Tertiary angiosperm fossil record over the course of the last century might have exacerbated the “problem” of high rates of diversification that confronted Darwin (13). However, it is worth bearing in mind that in the 1860s and 1870s, the dominant view, as advanced by Lord Kelvin (William Thomson) was that the Earth was between tens and hundreds of millions of years old (35). Given that the Cretaceous alone is now known to be on the order of 80 million years in length, it is unclear whether Darwin would or would not have viewed the mid to Late Cretaceous diversification of angiosperms (as now understood) as particularly troublesome to his gradualist views. In either case, this is an issue fundamentally separate from that of the “apparently very sudden or abrupt development of the higher plants” that confronted Darwin and motivated his correspondence with Hooker, Heer, and Saporta.

In summary, the seemingly abrupt origins of different groups of metazoans, as well as angiosperms, were topics hotly debated between 19th century creationists and evolutionists. Darwin keenly understood the intellectual dilemma posed by the appearance of diverse members of various groups of organisms without a transitional fossil prehistory. Nevertheless, it is a mistake to infer from Darwin's excised words “abominable mystery,” as made in reference to the origin and rapid diversification of flowering plants, that he was specifically and programmatically interested in the evolutionary history of angiosperms. Darwin's abominable mystery is not, in the final analysis and as his correspondence and publications demonstrate, about angiosperms per se. Darwin's abominable mystery is about his abhorrence that evolution could be both rapid and potentially even saltational; it is about his concerns that seemingly abrupt appearances of well-differentiated members of a group of organisms could be used to support a creationist agenda; and it is truly a reflection of the limitations that Darwin and other evolutionists of his era faced when attempting to read an as yet very incomplete fossil record of life on Earth.