American Journal of Botany 96(1): 5–21. 2009.

THE MEANING OF DARWIN’S “ABOMINABLE MYSTERY”1

William E. Friedman2
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 flow-
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 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 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, identification of the closest relatives of
flowering plants, questions of the homologies (and character transformations) of defining features of flowering plants, or the phy-
logeny 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 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 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.

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

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 first 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] flower-
frequenting insects were developed and favoured intercrossing.
I shd 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
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. To B.L.F., whose love of literature and
history inspired this.
2 E-mail: ned@colorado.edu
doi:10.3732/ajb.0800150
5
Charles Darwin’s fascination and frustration with the epic set
of evolutionary events associated with the origin and early radia-
tion of flowering plants are legendary. Perhaps no other group of
organisms merited Darwin’s attention in such dramatic terms:
“abominable mystery,” “most perplexing phenomenon,” “noth-
ing... 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 gen-
erations of plant biologists. Beginning just months after Dar-
win’s letter of 22 July 1879 to Joseph Hooker (Figs. 1A–G) was
first 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, developmental ge-
netics, 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;
Frohlich 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 flowering plants; the search for the earliest fossil
6 American Journal of Botany [Vol. 96

flowering plants; the evolutionary origin of the flower, the car-
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 flowering plants.
Given the universal inclination to quote Darwin whenever pos-
sible, 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.
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 flowering plants would clearly have
recognized the contrast between the virtual absence of angio-
sperms in the Early Cretaceous and their clear ascension to eco-
logical 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 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 diversifica-
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 operandi 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 diversifica-
tion 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 evo-
lutionary innovation led him to posit that prior to the Creta-
ceous 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 conse-
quence, flowering plants were absent from the fossil record un-
til 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 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.”

Figs. 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 Sa-
porta’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.
January 2009] Friedman—Darwin’s abominable mystery 7

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
8 American Journal of Botany [Vol. 96

Fig. 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 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
January 2009] Friedman—Darwin’s abominable mystery 9

Fig. 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 abomi-
nable mystery. Certainly it wd 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]
10 American Journal of Botany [Vol. 96

Fig. 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 shd 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
January 2009] Friedman—Darwin’s abominable mystery 11

Fig. 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.
12 American Journal of Botany [Vol. 96

Fig. 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
January 2009] Friedman—Darwin’s abominable mystery 13

Fig. 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.
14 American Journal of Botany [Vol. 96

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 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 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 diversifi-
cation (Darwin, 1887, p. 248) in a letter to Hooker (6 August
1881). “Nothing is more extraordinary in the history of the Veg-
etable Kingdom, as it seems to me, than the apparently very
sudden or abrupt development of the higher plants. I have some-
times 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 re-
markably 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; 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 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 (Ball,
1879). In this paper, which is largely concerned with biogeo-
graphical 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 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 palæontologists 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 flow-
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 interval,
January 2009] Friedman—Darwin’s abominable mystery
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 be-
tween 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 evi-
dence. The difficulty 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 first 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 flower-
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 flowering 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 confined to the alpine until global atmospheric carbon di-
oxide levels dropped significantly (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 first 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 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.
15
An alternative solution to the abominable mystery— In
contrast to Darwin’s view that the initial diversification of an-
giosperms had been gradual, but unrecorded in the fossil re-
cord, 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; 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
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 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 diversification of flow-
ering plants. In the second section of the introduction to
Paléontologie Française, 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).
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 Conry (1972) and Crepet (2000) have noted,
Saporta (1873) was the first to suggest a critical and interde-
pendent role of insects in the emergence and diversification of
angiosperms.
In his correspondence with Charles Darwin, Saporta elabo-
rated 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 diversifica-
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 diversification 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 diversity
16 American Journal of Botany [Vol. 96

Fig. 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 (Schröter 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 Office, he promoted the botanical interests of the Royal Botanic Gardens at Kew (Hooker, 1890;
Desmond, 1999) and was an alpine expert and botanist. An 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.
January 2009] Friedman—Darwin’s abominable mystery
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 in-
dividuals and of flower to flower 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 favoured 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 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 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 diversification: the ac-
celerating effects of the coevolution of pollinating insects and
flowers, and the potential benefits 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] flower-frequenting
insects were developed and favoured 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
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 be-
ing 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 empha-
sized 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 sec-
ond volume of L’Évolution du Règne Végétal (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 flowering 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,
17
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 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 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
diversification) of flowering plants from their nonangiosperm
ancestors. As Stebbins (1965, 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 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 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 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 diversification of angiosperms,
he does not appear to have explicitly considered the evolution
of the many unique characteristics of flowering 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 flowering plants was, at least tangen-
tially, 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 identifi-
cation 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 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 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 an-
giosperms. 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;
18 American Journal of Botany
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 significance. While the
origin of angiosperms from nonangiosperm seed plants remains
problematic, even to this day (e.g., Friedman and Floyd, 2001;
Magallón and Sanderson, 2002; Burleigh and Mathews, 2007),
questions of homology and character transformation, and issues
of the identification of angiosperm ancestors and closest rela-
tives, were not a central part of Darwin’s curiosity and frustra-
tion 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 “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 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 modi-
fication; 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, first 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 first group to confront Darwin
with a stark absence of paleontological data for a gradual diver-
sification 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
[Vol. 96
appear in certain formations, has been urged by several palæon-
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 modification 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
modified descendants” (Darwin, 1859, first 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 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 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, first 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, first 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 fishes, 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 significant 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 diversification are gradual,
as he would later argue in the case of flowering 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. This
led him to seek explanations for seemingly abrupt origins and
diversifications 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 succeeded in filling
January 2009] Friedman—Darwin’s abominable mystery
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-
versification of flowering 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 flowering plants
(provenance: Cambridge University Library, DAR 177: 35),
“Since there are no traces of Dicotyledons before the mid-Cre-
taceous… 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 defini-
tive group.” Darwin came to his abominable mystery, not be-
cause of a specific or programmatic curiosity about the broad
scale evolutionary history of flowering 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 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 seem-
ingly 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 innova-
tion 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 (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-
sification of flowering plants. Thus, it is worth briefly addressing
whether Darwin’s “abominable mystery,” specifically 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-
fication, as witnessed in the fossil record, demonstrate a period
of relatively gradual and orderly diversification prior to the
mid-Cretaceous (see Friis et al., 2006 for review). This Early
19
Cretaceous record of angiosperms, with its floras dominated by
small-flowered 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 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 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 fishes, and trilobites in the Ori-
gin 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 Cre-
taceous flowering 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-
fication. In essence, both predicted that there must have been a
period of angiosperm diversification 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 diversification
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;
Magallón 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 diversification 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).
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
diversification 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 different 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 diversification
of flowering plants, that he was specifically and programmatically
20 American Journal of Botany
interested in the evolutionary history of angiosperms. Darwin’s
abominable mystery is not, in the final analysis and as his cor-
respondence and publications demonstrate, about angiosperms
per se. Darwin’s abominable mystery is about his abhorrence
that evolution could be both rapid and potentially even salta-
tional; it is about his concerns that seemingly abrupt appear-
ances 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 incom-
plete fossil record of life on Earth.
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