1

American Journal of Botany 96(1): 1–18. 2009.

I have just read Ball ’ s Essay. It is pretty bold. The rapid de-velopment 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 fi rst could live only at a high level; but until it is experimen-tally [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 astonish-ingly rapid development of the high plants, as soon [as] fl ower-frequenting insects were developed and favored 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. — Ex-cerpt 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 ra-

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diation of fl owering 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 fl ower-ing plants, his “ abominable mystery ” has captured the imagina-tions of generations of plant biologists. Beginning just months after Darwin ’ s letter of 22 July 1879 to Joseph Hooker ( Figs. 1A – G7 ) was fi rst published in More Letters of Charles Darwin ( Darwin and Seward, 1903 ), biologists have used the phrase “ abominable mystery ” unabated, through the modern synthesis and on to the current synthesis of molecular phylogenetics, de-velopmental genetics, morphology, and paleobotany (e.g., Seward, 1904 ; Grew, 1911 ; Stopes, 1913 ; Parkin, 1925 ; Scott, 1925 ; Wieland, 1929 ; Baker, 1963 ; Stebbins, 1965 ; Regal, 1977 ; Crepet, 1998 , 2000 ; Bowe et al., 2000 ; Chaw et al., 2000 ; Ma and dePamphilis, 2000 ; Davies et al., 2004 ; Feild and Arens, 2005 ; Friedman, 2006 ; Frolich and Chase, 2007 ; Theissen and Melzer, 2007 ). 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. ”

Over the course of the last century, Darwin ’ s abominable mystery has become synonymous with the complexities and of-ten seemingly impenetrable questions surrounding the origin and earliest phases of angiosperm evolutionary history. Mean-ings ascribed to Darwin ’ s abominable mystery are highly vari-able 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 pre-cursors of fl owering plants; the search for the earliest fossil fl owering plants; the evolutionary origin of the fl ower, the car-

1 Manuscript received 28 April 2008; revision accepted 11 June 2008.

The author thanks J. Browne, P. Crane, P. Diggle, S. Renner, R. Robichaux, and R. Stockey for suggestions for the improvement of the manuscript, Y. Linhart and E. Smith for assistance with French – English translation, A. Mayer for assistance with German – English translation, P. Endress for help tracking down a portrait of Oswald Heer, and A. Pearn and E. Smith of the Darwin Correspondence Project for the extraordinary measures taken to provide access to previously unpublished letters to and from Charles Darwin. This research was supported by grants from the National Science Foundation and the University of Colorado Committee on Research and Creative Works.

2 E-mail: ned@colorado.edu

doi:10.3732/ajb.0800150

THE MEANING OF DARWIN ’ S “ ABOMINABLE MYSTERY ” 1

William E. Friedman 2

Department of Ecology and Evolutionary Biology; University of Colorado; Boulder, Colorado 80309 USA

Charles Darwin ’ s “ abominable mystery ” has come to symbolize just about all aspects of the origin and early evolution of fl ow-

ering plants. Yet, there has never been an analysis of precisely what Darwin thought was so abominably mysterious. Here I expli-

cate Darwin ’ s thoughts and frustrations with the fossil record of fl owering 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 Dar-

win to write his “ abominable mystery ” letter to Hooker in July of 1879. Contrary to what is generally believed, Darwin ’ s abomi-

nable mystery has little if anything to do with the fossil prehistory of angiosperms, identifi cation of the closest relatives of

fl owering plants, questions of the homologies (and character transformations) of defi ning features of fl owering plants, or the phy-

logeny of fl owering 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 fl owering plants. Rather, Darwin was

deeply bothered by what he perceived to be an abrupt origin and highly accelerated rate of diversifi cation of fl owering plants in

the mid-Cretaceous. This led Darwin to create speculative arguments for a long, gradual, and undiscovered pre-Cretaceous history

of fl owering plants on a lost island or continent. Darwin also took refuge in the possibility that a rapid diversifi cation of fl owering

plants in the mid-Cretaceous might, if real, have a biological explanation involving coevolutionary interactions between pollinat-

ing insects and angiosperms. Nevertheless, although generations of plant biologists have seized upon Darwin ’ s abominable mys-

tery 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 fl owering 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.

Key words: abominable mystery; angiosperms; John Ball; Charles Darwin; evolution; Oswald Heer; Joseph Hooker; radia-

tion; Gaston de Saporta

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“ 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 Amer-ica]. 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 diversifi ca-tion and biogeographical spread of angiosperms had been re-markably 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 operandus of transformation, although Darwin certainly accepted the possibility of some rapid evolutionary change ( Mayr, 1982 ; Gould and Eldredge, 1983 ; Rhodes, 1987 ; Gould, 2002 ). This, in turn, led Darwin on a six-year odyssey to ex-plain either an extremely rapid pace of evolutionary diversifi ca-tion or a strikingly long and missing fossil record of the earliest (and gradual) phases of angiosperm evolution. As Mayr has noted (1982, p. 508), “ Darwin took great pains to reconstruct a gradual evolution of phenomena that at fi rst site 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 evo-lutionary innovation led him to posit that prior to the Creta-ceous record of fl owering plants, angiosperms had slowly evolved and diversifi ed on a remote (and no longer present) landmass, perhaps in the southern hemisphere. As a conse-quence, fl owering plants were absent from the fossil record un-til the mid-Cretaceous when they fi nally 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 suc-ceeded in escaping, and spread quickly over the world ” (letter to Oswald Heer, 8 March 1875; Darwin and Seward, 1903 , p. 240). Four years later, Darwin again alluded to this idea in his abominable mystery letter to Hooker ( Darwin and Seward, 1903 , 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. ”

pel, 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 “ abomi-nable 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 fl owering plants. Given the universal inclination to quote Darwin whenever pos-sible, it seems only fi tting 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.

What was Darwin ’ s abominable mystery? — Darwin ’ s par-ticular fascination and frustration with the early evolution of angiosperms appear to have begun in earnest several years be-fore 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 perplex-ing 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 ” ( Darwin and Seward, 1903 , p. 239). Heer had been a proponent of the potential for rapid (in essence punctuational or saltational) evo-lution, much to Darwin ’ s dismay.

The early angiosperm fossil record that confronted Charles Darwin, Oswald Heer, and others (including John Ball and Gas-ton 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 fl owering plants would clearly have recognized the contrast between the virtual absence of an-giosperms 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):

Figs. 1A – 1G. Letter from Charles Darwin to Joseph Dalton Hooker, written July 22, 1879 (provenance: Cambridge University Library DAR 95: 485 – 488). In this letter, Darwin refers to the early evolution of fl owering plants as an “ abominable mystery. ” He also shows his interest in Gaston de Sa-porta ’ s idea that a coevolutionary set of interactions between angiosperms and insects may have been central to the rapid diversifi cation of fl owering plants in the mid-Cretaceous. This letter is a wonderful example of Darwin ’ s correspondence with Hooker, fi lled with the exchange of scientifi c 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 diffi cult to decipher, but the handwriting in this letter is actually quite good compared to others from this late period of Darwin ’ s 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, fi ve, and seven are the class marks associated with the archives at Cambridge University Library. On the fi rst 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.

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Fig. 1A. Letter from Charles Darwin to Joseph Dalton Hooker, written July 22, 1879 (provenance: Cambridge University Library DAR 95: 485 – 488), page 1.

My dear Hooker If my memory serves me rightly Dyer 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 fi nd

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Fig. 1B. Letter from Charles Darwin to Joseph Dalton Hooker, written July 22, 1879 (provenance: Cambridge University Library DAR 95: 485 – 488), page 2.

a support by bending toward any dark objects. — Our book on the movements of Plants 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 1st 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

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Fig. 1C. Letter from Charles Darwin to Joseph Dalton Hooker, written July 22, 1879 (provenance: Cambridge University Library DAR 95: 485 – 488), page 3.

to do. Frank comes back in the beginning of next month from W ü rzburg, where he has been working pretty hard on various subjects and practicing dissec-tion, cutting slices & c.

I have just read Balls ’ 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 abomi-nable mystery. Certainly it w d be a great step if we could believe that the higher plants at fi rst could live only at a high level; but until it is experimentally

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Fig. 1D. Letter from Charles Darwin to Joseph Dalton Hooker, written July 22, 1879 (provenance: Cambridge University Library DAR 95: 485 – 488), page 4.

that Cycade æ , 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] fl ower-frequenting insects were developed & favored 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

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Fig. 1E. Letter from Charles Darwin to Joseph Dalton Hooker, written July 22, 1879 (provenance: Cambridge University Library DAR 95: 485 – 488), 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.

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Fig. 1F. Letter from Charles Darwin to Joseph Dalton Hooker, written July 22, 1879 (provenance: Cambridge University Library DAR 95: 485 – 488), 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

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Fig. 1G. Letter from Charles Darwin to Joseph Dalton Hooker, written July 22, 1879 (provenance: Cambridge University Library DAR 95: 485 – 488), 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.

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Fig. 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 effi cient 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 Cam-bridge University Library.

Nearing the end of his life, Darwin returned to the notion of a lost fossil record of the earliest phases of angiosperm diversi-fi cation ( Darwin, 1887 , 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 ” re-veals his deeply rooted recognition that the fossil record could be remarkably incomplete and 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; Darwin and Seward, 1903 , 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 im-mense 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 — Dar-win ’ s 22 July 1879 abominable mystery letter to Hooker di-rectly relates to his keen desire to moderate the perceived rapid rate of early angiosperm diversifi cation. The stimulus for this letter was Darwin ’ s reading of the essay “ On the origin of the

fl ora 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 (Ball, 1879). In this paper, which is largely concerned with biogeo-graphical aspects of alpine fl oras, 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 exoge-nous plants [dicotyledonous angiosperms] is not disclosed by direct evidence until about the middle of the [C]retaceous pe-riod. Then all at once, in deposits widely spread over the north-ern hemisphere, we encounter a crowd of species, belonging to very different types, but for the most part so nearly resembling living plants, that pal æ ontologists do not hesitate to refer many of them to existing genera. ” Ball (p. 580) then posed the ques-tion succinctly. “ But if, at the commencement of the earliest chapter of the history accessible to us, the evolution of the fl ow-ering plants, and especially of the exogens [dicotyledonous an-giosperms], 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 inter-

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An alternative solution to the abominable mystery — In contrast to Darwin ’ s view that the initial diversifi cation of an-giosperms had been gradual, but unrecorded in the fossil re-cord, an alternative explanation of the mid-Cretaceous fl owering 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; Conry, 1972 , p. 93) that with “ respect to the sudden development of dicotyledinous [sic] plants, which view Heer likewise main-tains, 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 specifi c changes. ”

Saporta, like Darwin, was perplexed by the seemingly abrupt origin and rapid diversifi cation of angiosperms, as manifest in the fossil record ( “ un ph é nomene des plus curieux ” ). Unlike Darwin, however, Saporta began with the premise that a rapid rate of diversifi cation of angiosperms in the mid-Cretaceous was real and could be explained on biological principles. Im-portantly, Saporta ’ s hypothesis did not require a long unre-corded history of angiosperms prior to the Cretaceous.

Saporta had already developed a general theory that could provide a biological basis for the rapid diversifi cation of fl ow-ering plants. In the second section of the introduction to Pal é ontologie Fran ç aise, Plantes Jurassiques, Saporta (1873) 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 ( Conry, 1972 ). Specifi cally, 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 Conry (1972) and Crepet (2000) have noted, Saporta (1873) was the fi rst to suggest a critical and interde-pendent role of insects in the emergence and diversifi cation of angiosperms.

In his correspondence with Charles Darwin, Saporta elabo-rated on the theme of coevolutionary interdependence between insects and fl owering plants — and this time, he tied his reading of the fossil record to issues associated with rates of diversifi ca-tion , the very essence of Darwin ’ s “ abominable mystery. ” In a letter that is notable for its brilliance and insights, Saporta ex-plicitly 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 Conry 1972 , pp. 98 – 99) that the rapid diversifi cation of an-giosperms 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 for-merly 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 in-sects, to anemophilous plants alone, whose number and diver-

val, so perplexing to the botanist, between the endogens [mono-cots] and the exogens? ”

Perhaps unwittingly, Ball captured the essence of Darwin ’ s angiosperm dilemma. “ To my mind there is no alternative be-tween abandoning the doctrine of evolution and admitting that the origin of the existing types of fl owering plants is enormously more remote than the period as to which we have direct evi-dence. The diffi culty to be got over is the utter absence of such evidence ” (Ball, 1879, p. 580). As Darwin had confessed to Heer four years earlier (and noted above), the “ sudden appear-ance 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 ” ( Darwin and Seward, 1903 , p. 239).

Ball reasoned that angiosperms fi rst evolved in the alpine. Critically, he argued (Ball, 1879, 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 angio-sperms was entirely absent from the fossil record until fl ower-ing 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 addition-ally speculated that carbon dioxide levels decrease with eleva-tion. Finally, Ball conjectured that fl owering plants were unable to withstand high levels of atmospheric carbon dioxide (in con-tradistinction to other groups of plants). Thus, a long period of angiosperm evolution (dating to the Carboniferous) would have been confi ned to the alpine until global atmospheric carbon di-oxide levels dropped signifi cantly ( Darwin and Seward, 1903 ).

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 diplo-matic (in the published written comments by Hooker following the paper by Ball, 1879): “ [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 fi rst could live only at a high level; but until it is experimen-tally [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 think-ing 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 di-verse 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 diversifi cation 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.

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ond volume of L ’ É volution du R è gne V é g é tal (Saporta and Marion, 1885).

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 fl owering plants, namely, their coevolution with insects (for ongoing discussions of angio-sperm – insect coevolution, see Ehrlich and Raven, 1964 ; Raven, 1977 ; Regal, 1977 ; Crepet, 1984 , 1996 ; Midgley and Bond, 1991 ; Labandeira and Sepkoski, 1993 ; Ricklefs and Renner, 1994 ; Farrell, 1998 ; Grimaldi, 1999 ; Gorelick, 2001 ; Sargent, 2004 ). Moreover, Saporta ’ s solution to Darwin ’ s skepticism about the “ sudden development ” of fl owering plants was the only explanation Darwin ever embraced to potentially explain a rapid diversifi cation of early angiosperms as real .

Does the abominable mystery include the origin of angio-sperms? — 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 diversifi cation) of fl owering plants from their nonangiosperm ancestors. As Stebbins (1965, p. 457) put the case (refl ecting a viewpoint that dates to the early 1900s): “ About a hundred years ago, Charles Darwin referred to the origin of the Angio-sperms 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 inter-ested in evolution, to their bewilderment and frustration. The reasons for this diffi culty are manifold, but lie chiefl y 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 struc-tures connecting the most primitive angiosperms with non-an-giospermous seed plants [italics added] … ”

Although Darwin was clearly perplexed by a seemingly abrupt origin and rapid rate of diversifi cation of angiosperms, he does not appear to have explicitly considered the evolution of the many unique characteristics of fl owering plants (ques-tions of homology) from their nonangiosperm ancestors. Un-derlying his sense of bewilderment with the origin and early evolution of angiosperms certainly lay a problem with the pre-angiosperm fossil record and the phylogeny of seed plants. Dar-win ’ s extensive correspondence with paleobotanists describing the Jurassic and Cretaceous plant record makes clear that the immediate prehistory of fl owering plants was, at least tangen-tially, of interest to him. Nevertheless, Darwin does not appear to have pondered specifi c character transformations that would have been central to the establishment of defi ning features of fl owering plants (e.g., the fl ower, carpel, embryo sac, and so forth) — nor is there evidence that he worried about the identifi -cation of the ancestors of fl owering plants. In view of Darwin ’ s longstanding recognition of the inadequacies of the fossil

sity were never able to exceed a certain limit, and in which nutritive and succulent substances were never very abundant nor well diversifi ed. 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 fl ora, vol. 1, pp. 53 and 54 …

“ Now one can conceive very well that the angiosperms, whose fl oral combinations and crossings of individuals to in-dividuals and of fl ower to fl ower depend on the role of in-sects, 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 favored their existence; insects and plants have therefore been simultane-ously 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 ar-rangements and was composed almost exclusively of anemo-philous plants. ”

Darwin responded immediately to Saporta (letter of 24 De-cember 1877; Conry, 1972 , p. 109). “ Your idea that dicotyle-donous 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 fi rst 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 hy-pothesis and was thus provided with a plausible, indeed power-ful, mechanism to explain the rapid pace of early (meaning mid-Cretaceous, as of 1877) angiosperm diversifi cation: the ac-celerating effects of the coevolution of pollinating insects and fl owers, and the potential benefi ts of enhanced outcrossing as-sociated with entomophily.

Darwin did not forget Saporta ’ s ideas. A year and half later, in his abominable mystery letter to Joseph Hooker, Darwin re-lated, “ Saporta believes that there was an astonishingly rapid development of the high plants, as soon [as] fl ower-frequenting insects were developed and favored intercrossing. ” In 1881 (6 August letter to Joseph Hooker; Darwin and Seward, 1903 , 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 fl ower-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 be-ing thus suddenly formed. ” It is worth noting that in these two letters, Darwin focused on the presumed benefi ts of outcrossing to promote diversifi cation, while Saporta had primarily empha-sized the coevolutionary dynamics of anthophilous insects and fl owering plants. Saporta would go on to elaborate considerably on the early coevolution of insects and angiosperms in the sec-

Fig. 3. The key correspondents with Charles Darwin in his discussions of the early evolution of fl owering 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 ( Schr ö ter and Heer, 1885 ). 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 Offi ce, he promoted the botanical interests of the Royal Botanic Gardens at Kew ( Hooker, 1890 ; Desmond, 1999 ) and was an alpine expert and botanist. The obituary notice by Hooker (1890) provides an excellent sketch of his life. Reproduced from Sir Joseph Dalton Hooker, Traveler and Plant Collector ( Desmond, 1999 ). Bottom right. Gaston de Saporta (1823 – 1895), between 1880 and 1885.

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14 American Journal of Botany [Vol. 96

record (discussed later) and his embrace of the hypothesis that fl owering plants may have been evolving for an extended pe-riod 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 defi ning angiosperm characteristics.

The abominable mystery has also been invoked in modern times in reference to the relationships among extant seed plants and specifi cally 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 relation-ships within seed plants and acknowledged this late in 1861 in a letter to Joseph Hooker ( Darwin and Seward, 1903 , 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 ( Hooker, 1863 ), Darwin took note (letter of 6 October 1862; Burkhardt et al., 1997) 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 inten-sively ponder the question of hypothesized angiosperm rela-tives and their potential evolutionary signifi cance. While the origin of angiosperms from nonangiosperm seed plants remains problematic, even to this day (e.g., Friedman and Floyd, 2001 ; Magall ó n and Sanderson, 2002 ; Burleigh and Mathews, 2007 ), questions of homology and character transformation, and issues of the identifi cation of angiosperm ancestors and closest rela-tives, were not a central part of Darwin ’ s curiosity and frustra-tion with the evolutionary history of fl owering plants.

Natura non facit saltum, the heart of Darwin ’ s abominable mystery — Over the course of the last century, Darwin ’ s “ abom-inable mystery ” has become broadly synonymous with the complexities and often seemingly impenetrable questions sur-rounding the prehistory, origin, and early phases of angiosperm evolutionary history. Nevertheless, few, if any, of these topics, as they relate specifi cally to fl owering plants, appear to have been uppermost in Darwin ’ s mind at any point in his life. And this leads to a fi nal 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, favorable variations, it can produce no great or sudden modifi -cation; 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 … ” ( Darwin, 1859 , fi rst edition, p. 471; essentially similar in Darwin, 1872 , 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 fi rst group to confront Darwin with a stark absence of paleontological data for a gradual diver-sifi cation phase antecedent to a seemingly abrupt morphologi-cal 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 argu-ments 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 pal æ on-tologists, 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, be-longing 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 modifi cation through natural selection. For the devel-opment of a group of forms, all of which have descended from some one progenitor, must have been an extremely slow pro-cess; and the progenitors must have lived long ages before their modifi ed descendants ” ( Darwin, 1859 , fi rst edition, p. 302; es-sentially similar in Darwin, 1872 , sixth edition, p. 282).

In a deft tactical maneuver, Darwin set the stage for a solu-tion to this perceived “ fatal ” challenge to his theory of evolu-tion by descent with gradual modifi cation. “ [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 care-fully examined; we forget that groups of species may elsewhere have long existed and have slowly multiplied before they in-vaded the ancient archipelagoes of Europe and of the United States ” ( Darwin, 1859 , fi rst edition, p. 302; essentially similar in Darwin, 1872 , sixth edition, p. 282). Darwin continues, “ I will now give a few examples to illustrate the foregoing re-marks, and to show how liable we are to error in supposing that whole groups of species have suddenly been produced ” ( Darwin, 1859 , fi rst edition, p. 302; identical in Darwin, 1872 , sixth edition, p. 283). With this, Darwin launches an empirical counterattack against the vagaries of the fossil record by describ-ing 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 fi shes, and trilo-bites. 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 signifi cant prior record of transitional fossils compatible with his gradualist views of transmutation.

These passages from the Origin of Species presage the strat-egy Darwin later employed to attack the abominable mystery of the seemingly sudden and geographically widespread appear-ance of diverse angiosperms in the fossil record. Darwin ’ s ideas in the Origin of Species are clearly predicated on the assump-tion that biological innovation and diversifi cation are gradual,

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Darwin could not accept that the pace of evolutionary innova-tion could be so very rapid — and angiosperms (as known in the 1870s and 1880s) presented a signifi cant exception to this deeply held notion.

Concluding remarks — When Darwin went to his grave (ac-tually, 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 ori-gin and extremely rapid evolutionary and biogeographic diver-sifi cation of fl owering plants. Thus, it is worth briefl y addressing whether Darwin ’ s “ abominable mystery, ” specifi cally with re-spect to angiosperms, has been “ resolved ” in the interim be-tween 1882 and the present.

We now know that the earliest phases of angiosperm diversi-fi cation, as witnessed in the fossil record, demonstrate a period of relatively gradual and orderly diversifi cation prior to the mid-Cretaceous (see Friis et al., 2006 for review). This Early Cretaceous record of angiosperms, with its fl oras dominated by small-fl owered species, was entirely unknown to the paleon-tologists of Darwin ’ s time (or even 30 years ago). As such, the earliest manifestation of angiosperms, as now understood, ap-pears to be signifi cantly 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 con-forms to the patterns that Darwin took comfort in as he em-braced the discoveries of early transitional fossils for mammals, birds, sessile barnacles, teleost fi shes, and trilobites in the Ori-gin of Species . Obviously, such speculations are open to debate, but Darwin might well have been satisfi ed 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 Cre-taceous fl owering plants.

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

Despite the vagaries of mid-19th century stratigraphy, the es-sence 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 diversifi cation within angiosperms during the mid through Late Cretaceous and Early Tertiary were high ( Niklas et al., 1983 ; Crane, 1987 ; Upchurch and Wolfe, 1987 ; Lidgard and Crane, 1988 ; Crane and Herendeen, 1996 ; Crepet, 1996 , 2000 ; Lupia et al., 1999 ; Magall ó n and Sanderson, 2001 ; Friis et al., 2006 ). It has been suggested that the profound expansion of the mid to Late Creta-ceous and Early Tertiary angiosperm fossil record over the course of the last century might have exacerbated the “ prob-lem ” of high rates of diversifi cation that confronted Darwin ( Crepet, 2000 ). However, it is worth bearing in mind that in the 1860s and 1870s, the dominant view, as advanced by Lord Kel-vin (William Thomson) was that the Earth was between tens and hundreds of millions of years old ( Knell and Lewis, 2001 ).

as he would later argue in the case of fl owering plants. More-over, 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, and this led him to seek explanations for seemingly abrupt origins and diversifi cations of major lineages of animals and plants as pre-sented in the known fossil record of his times. Yet, in each in-stance, but one , Darwin ’ s geological and evolutionary “ problems ” were resolved as paleontological exploration suc-ceeded in fi lling 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 di-versifi cation of fl owering plants prior to their abrupt and di-verse 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 fl owering plants (provenance: Cambridge University Library, DAR 177: 35), “ Since there are no traces of Dicotyledons before the mid-Cre-taceous … the fi rst defi nable types seem from this time adorned with their discriminating characteristics and fi xed 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 diffi culty 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 defi ni-tive group. ” Darwin came to his abominable mystery, not be-cause of a specifi c or programmatic curiosity about the broad scale evolutionary history of fl owering plants, but rather, be-cause angiosperms, among all groups of living organisms, pre-sented 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 ad-aptation 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 fl owering plants. There is no indication that Darwin concerned himself with the homologies of the fl ower and its organs (as, for example, had Goethe in 1790).

Charles Darwin ’ s abominable mystery was never truly about fl owering plants per se. Charles Darwin ’ s abominable mystery was, in essence, one of rate : how to explain periods of seem-ingly abrupt and highly accelerated diversifi cation 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.

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16 American Journal of Botany [Vol. 96

Given that the Cretaceous alone is now known to be on the or-der of 80 million years in length, it is unclear whether Darwin would or would not have viewed the mid to Late Cretaceous diversifi cation of angiosperms (as now understood) as particu-larly 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 various groups of metazoans, as well as angiosperms, were topics hotly de-bated 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 mis-take to infer from Darwin ’ s excised words “ abominable mys-tery, ” as made in reference to the origin and rapid diversifi cation of fl owering plants, that he was specifi cally and programmati-cally interested in the evolutionary history of angiosperms. Darwin ’ s abominable mystery is not, in the fi nal analysis and as his correspondence and publications demonstrate, about angio-sperms per se. Darwin ’ s abominable mystery is about his ab-horrence that evolution could be both rapid and potentially even saltational; it is about his concerns that seemingly abrupt ap-pearances of well-differentiated members of a group of organ-isms could be used to support a creationist agenda; and it is truly a refl ection of the limitations that Darwin and other evolu-tionists of his era faced when attempting to read an as yet very incomplete fossil record of life on Earth.

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