The origin of Darwin’s “abominable mystery”

The phrase “Darwin’s abominable mystery” is frequently used with reference to a range of outstanding questions about the evolution of the plant group today known as the angiosperms. Here, I seek to more fully understand what prompted Darwin to coin the phrase in 1879, and the meaning he attached to it, by surveying the systematics, paleobotanical records, and phylogenetic hypotheses of his time. In the light of this historical research, I argue that Darwin was referring to the origin only of a subset of what are today called angiosperms: a (now obsolete) group equivalent to the “dicotyledons” of the Hooker and Bentham system. To Darwin and his contemporaries, the dicotyledons’ fossil record began abruptly and with great diversity in the Cretaceous, whereas the gymnosperms and monocotyledons were thought to have fossil records dating back to the Carboniferous or beyond. Based on their morphology, the dicotyledons were widely seen by botanists in Darwin’s time (unlike today) as more similar to the gymnosperms than to the monocotyledons. Thus, morphology seemed to point to gymnosperm progenitors of dicotyledons, but this hypothesis made the monocotyledons, given their (at the time) apparently longer fossil record, difficult to place. Darwin had friendly disagreements about the mystery of the dicotyledons’ abrupt appearance in the fossil record with others who thought that their evolution must have been more rapid than his own gradualism would allow. But the mystery may have been made “abominable” to him because it was seen by some contemporary paleobotanists, most notably William Carruthers, the Keeper of Botany at the British Museum, as evidence for divine intervention in the history of life. Subsequent developments in plant systematics and paleobotany after 1879 meant that Darwin’s letter was widely understood to be referring to the abrupt appearance of all angiosperms when it was published in 1903, a meaning that has been attached to it ever since.     

Diversity in obscurity: fossil flowers and the early history of angiosperms

In the second half of the nineteenth century, pioneering discoveries of rich assemblages of fossil plants from the Cretaceous resulted in considerable interest in the first appearance of angiosperms in the geological record. Darwin''s famous comment, which labelled the ‘rapid development’ of angiosperms an ‘abominable mystery’, dates from this time. Darwin and his contemporaries were puzzled by the relatively late, seemingly sudden and geographically widespread appearance of modern-looking angiosperms in Late Cretaceous floras. Today, the early diversification of angiosperms seems much less ‘rapid’. Angiosperms were clearly present in the Early Cretaceous, 20–30 Myr before they attained the level of ecological dominance reflected in some mid-Cretaceous floras, and angiosperm leaves and pollen show a distinct pattern of steadily increasing diversity and complexity through this interval. Early angiosperm fossil flowers show a similar orderly diversification and also provide detailed insights into the changing reproductive biology and phylogenetic diversity of angiosperms from the Early Cretaceous. In addition, newly discovered fossil flowers indicate considerable, previously unrecognized, cryptic diversity among the earliest angiosperms known from the fossil record. Lineages that today have an herbaceous or shrubby habit were well represented. Monocotyledons, which have previously been difficult to recognize among assemblages of early fossil angiosperms, were also diverse and prominent in many Early Cretaceous ecosystems.     

Darwin's second 'abominable mystery': Why are there so many angiosperm species?

The rapid diversification and ecological dominance of the flowering plants beg the question "Why are there so many angiosperm species and why are they so successful?" A number of equally plausible hypotheses have been advanced in response to this question, among which the most widely accepted highlights the mutually beneficial animal-plant relationships that are nowhere better developed nor more widespread than among angiosperm species and their biotic vectors for pollination and dispersal. Nevertheless, consensus acknowledges that there are many other attributes unique to or characteristic of the flowering plants. In addition, the remarkable coevolution of the angiosperms and pollination/dispersal animal agents could be an effect of the intrinsic adaptability of the flowering plants rather than a primary cause of their success, suggesting that the search for underlying causes should focus on an exploration of the genetic and epigenetic mechanisms that might facilitate adaptive evolution and speciation. Here, we explore angiosperm diversity promoting attributes in their general form and draw particular attention to those that, either individually or collectively, have been shown empirically to favor high speciation rates, low extinction rates, or broad ecological tolerances. Among these are the annual growth form, homeotic gene effects, asexual/sexual reproduction, a propensity for hybrid polyploidy, and apparent "resistance" to extinction. Our survey of the literature suggests that no single vegetative, reproductive, or ecological feature taken in isolation can account for the evolutionary success of the angiosperms. Rather, we believe that the answer to Darwin's second "abominable mystery" lies in a confluence of features that collectively make the angiosperms unique among the land plants.     

Epigenetic mechanisms in the endosperm and their consequences for the evolution of flowering plants

The sudden rise of angiosperms to ecological dominance was an "abominable mystery" to Charles Darwin, and understanding the underlying evolutionary driving force has remained a scientific challenge since then. The recognition of polyploidization as an important factor for plant speciation is likely to hold a key to this mystery and we will discuss possible mechanisms underlying this phenomenon. Polyploidization raises an immediate reproductive barrier in the endosperm, pointing towards an important but greatly underestimated role of the endosperm in preventing interploidy hybridizations. Parent-of-origin-specific gene expression is largely restricted to the endosperm, providing an explanation for the dosage sensitivity of the endosperm. Here, we review epigenetic mechanisms causing endosperm dosage sensitivity, their possible consequences for raising interploidy and interspecies hybridization barriers and their impact on flowering plant evolution. This article is part of a Special Issue entitled: Epigenetic Control.     

Darwin's use of the analogy between artificial and natural selection

Conclusion The central role played by Darwin's analogy between selection under domestication and that under nature has been adequately appreciated, but I have indicated how important the domesticated organisms also were to other elements of Darwin's theory of evolution-his recognition of the constant principle of change, for instance, of the imperfection of adaptation, and of the extent of variation in nature. The further development of his theory and its presentation to the public likewise hinged on frequent reference to domesticates.We have seen that Darwin's reliance on the analogy between domesticated varieties and wild species was a bold and original step, in light of contemporary views on the nature of domesticates. However, as Darwin undoubtedly foresaw, his reliance on the analogy created difficulties as well as solving problems, and these began with his Malthusian codiscoverer of the principle of natural selection, Alfred Russel Wallace. Wallace's paper On the Tendency of Varieties to Depart Indefinitely from the Original Type, presented to the Linnean Scoiety along with the first public unveiling of Darwin's theory, states: We see, then, that no inferences as to varieties in a state of nature can be deduced from the observation of those occurring among domestic animals. The two are so much opposed to each other in every circumstance of their existence, that what applies to the one is almost sure not to apply to the other. Domestic animals are abnormal, irregular, artificial; they are subject to varieties which never occur and never can occur in a state of nature.⁶² Much has been made of the similarity of views of Darwin and Wallace, but this quotation surely reveals how utterly different their views were on what to Darwin was an important matter. Several critics of the Origin saw Darwin's reliance on the domesticates as his Achilles heel. As Young has pointed out, Samuel Wilberforce included the following passage in his attack on the Origin: Nor must we pass over unnoticed the transference of the argument from the domesticated to the untamed animals. Assuming that man as the selector can do much in a limited time, Mr. Darwin argues that Nature, a more powerful, a more continuous power, working over vastly extended ranges of time, can do more. But why should Nature, so uniform and persistent in all her operations, tend in this instance to change? Why should she become a selector of varieties?⁶³ Another critic, Fleeming Jenkin, found the analogy a weakness in Darwin's theory because of the limited extent of variation in any one direction in domestic animals and plants.⁶⁴ We have already seen that Darwin had confided a similar view to his notebook thirty years earlier, but changed his mind as a result of his profound study of domesticates. De Beer's reference to an English country gentleman's knowledge of domestic plants and animals and their breeding⁶⁵ fails totally to recognize the originality and depth of Darwin's knowledge of domesticates.Why did Darwin, against the currents of his time, rely so heavily on mankind's experience with domesticated organisms to shape his theory about species in nature? On reason is that only with domesticates was an approach that came close to experimental verification possible. Darwin fully realized the inadequacies of the experiment, as is emphasized by his repeated contrasting of selection under nature and selection by man. Yet the extensive experience and data of plant and animal breeders offered the only reliable base against which Darwin could continually challenge his views. As he wrote in the introduction to Variation, with domestication, man ... may be said to have been trying an experiment on a gigantic scale.⁶⁶ Given Darwin's high opinion of the quantitative work of Malthus and Quetelet (as emphasized by Schweber),⁶⁷ and his unremitting efforts to secure data by which to test his theories, it was inevitable that he should attach high significance to domesticated varieties. John Tyndall, in his Belfast address of 1874, said: The strength of the doctrine of Evolution consists, not in experimental demonstration (for the subject is hardly accessible to this mode of proof), but in its general harmony with scientific thought.⁶⁸ Darwin would have agreed with the latter thought, but I think he would have challenged the preceding one on the grounds that long experience with domesticated varieties did provide an element of experimental demonstration. It gave him confidence in his theory, and he used his vast knowledge of artificial selection boldly and creatively.     

The vascular plants of Joseph Dalton Hooker's An enumeration of the plants of the Galapagos Archipelago; with descriptions of those which are new

The first floristic work on the Galápagos Islands was published by J. D. Hooker in 1847. It was based mainly on the Beagle collections of Charles Darwin, but those of James McRae, John Scouler. Hugh Cuming, David Douglas, Thomas Edmonston, Abel Du Petit-Thouars and John Goodridge were also used, though those of Archibald Menzies, the first botanist to visit the archipelago, were not. The visits of these naturalists and their collections are discussed. Darwin's field notes on Galápagos plants, hitherto unpublished, are given, and most of the species identified. In the taxonomic portion of the paper, each taxon included by Hooker is discussed, the nomenclaturally or-taxonomically correct name is indicated, specimens examined by Hooker are enumerated, and additional specimens presumably seen but not cited by him are given. Hooker wrote before our present type concept had evolved, and consequently 51 of his 114 new names needed to be typified, as did four others based on Darwin Galápagos collections. In addition, examination of these specimens revealed one species not yet reported from the archipelago ( Galium canescens ), one new island record ( Chamaesyce hirta on James Island), and one deletion from the flora ( Malachra capitala )     

被子植物花的起源:假说和证据

达尔文的 令人讨厌之谜 ,即被子植物的起源和早期演化 ,一直是植物系统学研究领域的热点 .被子植物区别于其它植物类群的一个显著特征就是花 ,因此 ,解决被子植物的起源之谜很大程度上取决于对被子植物花器官起源的研究 .对被子植物花器官的详尽研究已经在形态、解剖、古植物、形态发生、分子等方面积累了大量的证据 ,植物学家基于这些证据为被子植物花器官的起源提出了各种各样的解释 .综述了迄今为止被子植物花器官起源的主要学说流派 ,如 :真花学说、假花学说、生殖叶学说、生殖茎节学说、生花植物学说、新假花学说、古草本学说和 ANITA学说等 .根据研究手段和获得证据的方式 ,作者将被子植物花器官起源研究划分为 5个阶段 ,并简要阐述了各个阶段的代表学说和主要研究特点     

Timing in the evolution of derived floral characters: upper cretaceous (turonian) taxa with tricolpate and tricolpate-derived pollen

Various hypotheses that seek to explain the rich species diversity of angiosperms relative to other seed plants are briefly mentioned or reviewed. Of these, the subset that relates angiosperm diversity in some way to the relationship between angiosperms and insects, particularly anthophilous insects, is here the object of attention. Specifically, I address and reject the possibility that the relationship between angiosperm diversification and insects, particularly those demonstrating a preference for flowers with derived floral characteristics associated with insect pollination, may be ruled out because of asynchronous patterns of diversification in the fossil record. New data on floral structure from the Turonian of the Atlantic Coastal Plain reveal a surprising diversity of floral characters in taxa bearing tricolpate and tricolporate-derived pollen. The characters and taxa that appear in these Turonian sediments suggest that rather specific modes of insect pollination, perhaps involving highly derived insect pollinators, already existed at 90 Ma. Given the observed rate of diversification of angiosperms during that time and the pattern of evolution in insects, including what can be inferred about the history of the Apidae, these new floral data suggest that hypotheses relating angiosperm diversity to highly specific pollinators are still valid in the context of fossil evidence. Even so, consistency with fossil evidence is not necessarily proof of these relationships. In any case, there may well be multiple causes of relatively high angiosperm species diversity and understanding the relative importance of each of these requires neontological as well as paleontological investigations. One promising approach is to work within the context of phylogenetic patterns with more fossil data.     

Evolution in fossil lineages: paleontology and The Origin of Species

Of all of the sources of evidence for evolution by natural selection, perhaps the most problematic for Darwin was the geological record of organic change. In response to the absence of species-level transformations in the fossil record, Darwin argued that the fossil record was too incomplete, too biased, and too poorly known to provide strong evidence against his theory. Here, this view of the fossil record is evaluated in light of 150 years of subsequent paleontological research. Although Darwin's assessment of the completeness and resolution of fossiliferous rocks was in several ways astute, today the fossil record is much better explored, documented, and understood than it was in 1859. In particular, a reasonably large set of studies tracing evolutionary trajectories within species can now be brought to bear on Darwin's expectation of gradual change driven by natural selection. An unusually high-resolution sequence of stickleback-bearing strata records the transformation of this lineage via natural selection. This adaptive trajectory is qualitatively consistent with Darwin's prediction, but it occurred much more rapidly than he would have guessed: almost all of the directional change was completed within 1,000 generations. In most geological sequences, this change would be too rapid to resolve. The accumulated fossil record at more typical paleontological scales (10(4)-10(6) years) reveals evolutionary changes that are rarely directional and net rates of change that are perhaps surprisingly slow, two findings that are in agreement with the punctuated-equilibrium model. Finally, Darwin's view of the broader history of life is reviewed briefly, with a focus on competition-mediated extinction and recent paleontological and phylogenetic attempts to assess diversity dependence in evolutionary dynamics.     

Comparative embryology of basal angiosperms

Recent phylogenetic analyses of basal angiosperms have identified those lineages central to the study of the origin and early diversification of flowering plants. As we begin to understand the early evolution of endosperm developmental patterns in flowering plants, it is apparent that we know little about the other basic embryological features of basal angiosperms, such as the nature of the female gametophyte and even whether a process of double fertilization occurs.     

From Charles Darwin's botanical country-house studies to modern plant biology

As a student of theology at Cambridge University, Charles Darwin (1809–1882) attended the lectures of the botanist John S. Henslow (1796–1861). This instruction provided the basis for his life-long interest in plants as well as the species question. This was a major reason why in his book On the Origin of Species , which was published 150 years ago, Darwin explained his metaphorical phrase 'struggle for life' with respect to animals and plants. In this article, we review Darwin's botanical work with reference to the following topics: the struggle for existence in the vegetable kingdom with respect to the phytochrome-mediated shade avoidance response; the biology of flowers and Darwin's plant–insect co-evolution hypothesis; climbing plants and the discovery of action potentials; the power of movement in plants and Darwin's conflict with the German plant physiologist Julius Sachs; and light perception by growing grass coleoptiles with reference to the phototropins. Finally, we describe the establishment of the scientific discipline of Plant Biology that took place in the USA 80 years ago, and define this area of research with respect to Darwin's work on botany and the physiology of higher plants.     

Darwin's evolutionary philosophy: The laws of change

The philosophical or metaphysical architecture of Darwin's theory of evolution by natural selection is analyzed and diflussed. It is argued that natural selection was for Darwin a paradigmatic case of a natural law of change — an exemplar of what Ghiselin (1969) has called selective retention laws. These selective retention laws lie at the basis of Darwin's revolutionary world view. In this essay special attention is paid to the consequences for Darwin's concept of species of his selective retention laws. Although Darwin himself explicity supported a variety of nominalism, implicit in the theory of natural selection is a solution to the dispute between nominalism and realism. It is argued that, although implicit, this view plays a very important role in Darwin's theory of natural selection as the means for the origin of species. It is in the context of these selective retention laws and their philosophical implications that Darwin's method is appraised in the light of recent criticisms, and the conclusion drawn that he successfully treated some philosophical problems by approaching them through natural history. Following this an outline of natural selection theory is presented in which all these philosophical issues are highlighted.     

Adaptation and the origin of species

As reflected in the title of his masterwork On the Origin of Species, Darwin proposed that adaptation is the primary mechanism of speciation. On this, Darwin was criticized for his neglect of reproductive isolation, his lack of appreciation for the role of geographic barriers, his failure to distinguish varieties from species, and his typological species concept. Two developments since Darwin, the biological species concept of Ernst Mayr and the methods of Coyne and Orr for estimating the contribution of different barriers to the total reproductive isolation, provide a framework for reconciling Darwin's view on the primacy of adaptation in speciation with later proposals that emphasize reproductive isolation. A review of the few studies that have estimated the contributions of multiple isolating barriers suggests that habitat isolation and other barriers that operate before hybrid formation are much stronger than intrinsic postzygotic isolation. In light of these data, I suggest that Darwin's focus on adaptation in the origin of species was essentially correct, a conclusion that calls for future studies that explore the links between adaptation and speciation, in particular, ecogeographic isolating barriers that result from adaptive divergence in habitat use. The recent revival in thinking about ecological factors and adaptive divergence in the origin of species echoes Darwin's much-criticized "principle of divergence" and suggests that the emerging views from today's naturalists are not so different from those espoused by Darwin some 150 years ago.     

Darwin's explanation of races by means of sexual selection

In Darwin's Sacred Cause, Adrian Desmond and James Moore contend that "Darwin would put his utmost into sexual selection because the subject intrigued him, no doubt, but also for a deeper reason: the theory vindicated his lifelong commitment to human brotherhood" (2009: p. 360). Without questioning Desmond and Moore's evidence, I will raise some puzzles for their view. I will show that attention to the structure of Darwin's arguments in the Descent of Man shows that they are far from straightforward. As Desmond and Moore note, Darwin seems to have intended sexual selection in non-human animals to serve as evidence for sexual selection in humans. However, Darwin's account of sexual selection in humans was different from the canonical cases that Darwin described at great length. If explaining the origin of human races was the main reason for introducing sexual selection, and if sexual selection was a key piece of Darwin's anti-slavery arguments, then it is puzzling why Darwin would have spent so much time discussing cases that did not really support his argument for the origin of human races, and it is also puzzling that his argument for the origin of human races would be so (atypically) poor.     

Nietzsche's aesthetic critique of Darwin

Despite his position as one of the first philosophers to write in the "post-Darwinian" world, the critique of Darwin by Friedrich Nietzsche is often ignored for a host of unsatisfactory reasons. I argue that Nietzsche's critique of Darwin is important to the study of both Nietzsche's and Darwin's impact on philosophy. Further, I show that the central claims of Nietzsche's critique have been broadly misunderstood. I then present a new reading of Nietzsche's core criticism of Darwin. An important part of Nietzsche's response can best be understood as an aesthetic critique of Darwin, reacting to what he saw as Darwin having drained life of an essential component of objective aesthetic value. For Nietzsche, Darwin's theory is false because it is too intellectual, because it searches for rules, regulations, and uniformity in a realm where none of these are to be found - and, moreover, where they should not be found. Such a reading goes furthest toward making Nietzsche's criticism substantive and relevant. Finally, I attempt to relate this novel explanation of Nietzsche's critique to topics in contemporary philosophy of biology, particularly work on the evolutionary explanation of culture.     

Darwin and the origin of interspecific genetic incompatibilities

Darwin's Origin of Species is often criticized for having little to say about speciation. The complaint focuses in particular on Darwin's supposed failure to explain the evolution of the sterility and inviability of interspecific hybrids. But in his chapter on hybridism, Darwin, working without genetics, got as close to the modern understanding of the evolution of hybrid sterility and inviability as might reasonably be expected. In particular, after surveying what was then known about interspecific crosses and the resulting hybrids, he established two facts that, while now taken for granted, were at the time radical. First, the sterility barriers between species are neither specially endowed by a creator nor directly favored by natural selection but rather evolve as incidental by-products of interspecific divergence. Second, the sterility of species hybrids results when their development is "disturbed by two organizations having been compounded into one." Bateson, Dobzhansky, and Muller later put Mendelian detail to Darwin's inference that the species-specific factors controlling development (i.e., genes) are sometimes incompatible. In this article, I highlight the major developments in our understanding of these interspecific genetic incompatibilities--from Darwin to Muller to modern theory--and review comparative, genetic, and molecular rules that characterize the evolution of hybrid sterility and inviability.     

The identification of fossil angiosperm pollen and its bearing on the time and place of the origin of angiosperms

Studies in the 1970's reporting the occurrence of fossil pollen types in the Cretaceous, coupled with surveys of extant pollen morphology of primitive flowering plants, laid the foundation for proposing a Lower Cretaceous origin of angiosperms. Over the last 30 years, morphological, ultrastructural, and ontogenetic studies of both extant and fossil pollen have provided an array of new characters, as well as greater resolution in defining character polarities. Moreover, a range of fossil pollen types exhibiting angiosperm characters occur in low frequency within Triassic and Jurassic sediments. The pollen data provide evidence of a pre-Cretaceous origin of angiosperms. Speciation and extinction rates were likely equal during the Triassic and Jurassic, resulting in the paucity of angiosperm pollen types from different geographic areas in the Atlantic – South American/African rift zone. It was not until the Lower Cretaceous that origination rates exceed extinction rates, resulting in the subsequent diversification of angiosperms and the origin of the eudicots.     

Humboldt,Darwin, and population

Conclusions I have attempted to clarify some of the pathways in the development of Darwin's thinking. The foregoing examples of influence by no means include all that can be found by comparing Darwin's writings with Humboldt's. However, the above examples seem adequate to show the nature and extent of this influence. It now seems clear that Humboldt not only, as had been previously known, inspired Darwin to make a voyage of exploration, but also provided him with his basic orientation concerning how and what to observe and how to write about it. An important part of what Darwin assimilated from Humboldt was an appreciation of population analysis as a tool for assessing the state of societies and of the benefits and hardships which these societies can expect to receive from the living world around them.Darwin exhibited in his Journal of Researches a casual interest in the economic and political conditions of the countries he visited, but these considerations were much less important to him than to Humboldt. Instead, Darwin, with the assistance of Lyell's Principles of Geology, shifted from Humboldt's largely economic framework to a biological one built around the species question. This shift led Darwin away from a consideration of how the population biology of animals was related to man's economy to focus instead upon how population biology fitted into the economy of nature.Humboldt's Personal Narrative served very well as a model for Darwin's Journal of Researches, thereby helping Darwin gain scientific eminence. The Journal of Researches, like virtually all of Humboldt's writings, was a contribution to scientific orthodoxy. But Darwin had, along the way, acquired an urge to do more than just add his building blocks to the orthodox scientific edifice. He decided to rearrange those blocks of knowledge into a different structure, and for that task neither Humboldt's Personal Narrative nor any other of his works could serve as a model. Humboldt had lacked the confidence which Darwin needed that biogeography and the origin of species could be understood. Humboldt had not explored very far the possible connections between biology and geology. Nor had he provided a general synthetic account of population biology. Had he done so, he might have been more explicit about the extent of his endorsement of Malthus. But even if he had, Humboldt's strong orientation toward cooperation would probably have inhibited his recognition of the importance of competition in nature.Lyell, who had also benefited from reading Humboldt, gave Darwin insights that were lacking in Humboldt's Personal Narrative. Lyell admirably demonstrated how stratigraphy, paleontology, biogeography, and population biology could be interrelated, and his reasons for doing so were essentially the same as Darwin's. Lyell's understanding of biogeography and ecology came from the writings of Augustin-Pyramus de Candolle as much as from Humboldt's, and from the former Lyell derived an appreciation for the importance of competition and also a confidence that the mysteries of biogeography could be explained.¹¹⁷ Furthermore, Lyell's discussion of all these subjects and also of evolution in his Principles of Geology is a good synthetic argument that was the ideal model for Darwin's greatest book.Darwin, having become convinced that species change through time, was able to synthesize in his mind the contributions which he had derived from the writings of Humboldt and Lyell as they applied to the species question. When Darwin wrote his Journal of Researches there were two large gaps in his thinking about evolution that bothered him—the mechanism of evolution and the causes of extinction. It was only after reading Malthus in 1838 that he realized, as Lyell had more or less pointed out, how important was competition in nature. He now had the general outlines for his theory, and in the 1845 abridged edition of his Journal, now retitled The Voyage of the Beagle, he inserted a fuller discussion of competition in nature which showed his awareness of its importance as an ecological factor.¹¹⁸ An abridged version of this paper was presented at the meeting of the History of Science Society in Washington, D.C., on 29 December 1969.