In consolidating his ideas about natural selection, and in considering orchids as being “universally acknowledged to rank amongst the most singular and most modified forms in the vegetable kingdom”, Charles Darwin (1809–1882) was already making concrete observations on, and evolutionary links between, insects and plants in the first edition of his book published in early 1862:
The object of the following work is to show that the contrivances by which Orchids are fertilised, are as varied and almost as perfect as any of the most beautiful adaptations in the animal kingdom; and, secondly, to show that these contrivances have for their main object the fertilisation of the flowers with pollen brought by insects from a distinct plant.
Indeed, one can endeavour to trace the history of evolutionary biology and come to the recognition that Darwin’s book on orchids generated the impetus for all succeeding investigations into coevolution and the evolution of extreme specialization. The book was published in 1862, less than 30 months after the advent of On the Origin of Species, and its second edition in 1877, when the contemporary Victorian vogue for growing exotic orchids was well established in England and Europe. Riding on the vogue intentionally or unintentionally, the book presents Darwin’s first detailed demonstration of the potency of natural selection, and demonstrates how multifaceted ecological relationships can result in the coevolution of orchids and insects. In other words, it explains how the relationship between plants and animals can produce beautiful and complex forms, including exaggerated phenotypes with unusual traits or extreme morphologies. A famous instance is documented on page 162 of the second edition: Darwin recounted his receiving from the distinguished horticulturist Mr James Bateman (1811–1897) in 1862 a Madagascar orchid named Angraecum sesquipedale whose nectary was 11.5 inches long, and predicted that there must be a species of moth with proboscis long enough to reach the nectar at the end of the spur. It is no wonder that the orchid is given the specific epithet in Latin, “sesquipedale”, meaning “one and a half feet”. On page 165, Darwin even predicted that “[i]f such great moths were to become extinct in Madagascar, assuredly the Angræcum would become extinct.” Such a moth, named Xanthopan morgani, was discovered in 1903, validating the predictive power of (co)evolution.
Xanthopan morgani is classified under Sphingidae, a family of about 1,450 species of moths (Lepidoptera) commonly known as hawkmoths, sphinx moths and hornworms. Since nocturnal sphingids tend to be attracted to pale flowers with long corolla tubes and a sweet odour, a specific pollination syndrome has been named after the family of moths as “sphingophily”. Typical of sphingids, Xanthopan morgani has the ability to hover like hummingbirds and feed on the nectar of Angraecum sesquipedale’s flowers, which the moth identifies by scent.
Closely related to Angraecum sesquipedale is Aerangis ellisii, also known as Aerangis platyphylla, which is not only ephiphytic but also epilithic, as it is often found to be growing on the surface of rock. It is a smaller orchid endemic to central and eastern Madagascar at elevations of 1100 to 1400 meters. As shown in the photo below and according to the abstract of a 1988 paper entitled “Hawk-moth scale analysis and pollination specialization in the epilithic Malagasy endemic Aerangis ellisii (Reichenb. fil.) Schltr. (Orchidaceae)” authored by L A Nilsson and E Rabakonandrianina:
The flowers exhibit long nectariferous spurs indicative of hawk-moth pollination, the mechanism evidently involving pollinia transfer via the frons and palpi of the vectors. Analysis of hawk-moth scales on naturally pollinated stigmas showed that the principal pollinators were Agrius conuolvuli (Linnaeus) and Panogena lingens (Butler). Proboscis morphology of long-tongued Malagasy Sphingidae in relation to nectar position and spur morphology in A. ellisii also indicated that A. conuolvuli and P. lingens were best suited to interact with the plant’s floral adaptation. Aerangis ellisii seems to display a relatively moderate specialization versus the Malagasy hawk-moth guild since its nectar is accessible even to those long-proboscis hawk-moth species which are not able to act as pollinators.
Four years later, in a 1992 paper entitled “Exact tracking of pollen transfer and mating in plants”, the abovementioned two researchers in conjunction with B Pettersson concluded on the coevolutionary outcomes of animal-plant interactions in pollination biology and plant morphology as follows:
UNLIKE animals, where individuals engage in direct sexual encounters, higher plants interact sexually only through minute, usually animal-mediated pollen grains, a trait that has hampered understanding of processes that govern plant evolution. A new technique using micro-tags to mark individual orchid pollinia and monitoring of all stigmas for pollination made it possible to measure exactly pollen transfer and mating pattern in a plant species. We report here that in populations of a hawkmoth-pollinated orchid, Aerangis ellisii, pollen transfers were found to be infrequent, to involve single pollen parents, and to occur mostly within 5 metres. Pollinator-mediated patterns of disproportional reproductive success suggest that floral traits are being shaped by mutual sexual selection as proposed by Darwin.
Even Angraecum sesquipedale’s smallest South African cousin, a miniature orchid called Mystacidium capense, is also exclusively hawkmoth-pollinated, its flower having a 3.9cm spur, much shoter than the 27–43cm (10.6–16.9in) spur of Angraecum sesquipedale. That coevolution so similar in kind has left its mark in species so dissimilar in size is quite remarkable. Taxonomically, both species had crossed paths at the level of genus, given that Angraecum sesquipedale was classified as Mystacidium sesquipedale (Rolfe) in 1904, whereas Mystacidium capense was originally called Angraecum capense (Lindl.) in 1830–40. Robyn P Luyt’s Master of Science Thesis of 2002 entitled “Pollination and evolution of the genus Mystacidium (Orchidaceae)” reveals that both Mystacidium capense and Mystacidium venosum are exclusively pollinated by long-tongued hawkmoths since their spur lengths are 3.9cm and 4.7cm respectively, whereas other Mystacidium species are pollinated by settling noctuid moths (and perhaps also bees, flies or even butterflies), since their spur lengths are less than 3cm, ranging from 1.68cm in M. tanganyikense to 2.56cm in M. gracile.
In the introduction to chapter 3 of the thesis on pages 33 and 34, Luyt also mentions Darwin and explains in the context of pollination biology that long spurs are evolved traits that confer “effective pollination by long-tongued pollinators” as the result of an evolutionary race between a plant and its pollinator:
The mechanism by which long spurs evolved was suggested by Darwin (1862) and later experimentally tested by Nilsson(1988): selection for longer spurs will compel a long-tongued pollinator to insert its proboscis deep into the spur, thereby ensuring contact with the flower’s sexual organs. Conversely, longer tongues are selected when they enable pollinators to reach deeply concealed nectar. The “evolutionary race” continues as pollinators with longer mouthparts drive the selection for longer spurs, and vice versa.
In biology, coevolution happens “when changes in at least two species’ genetic compositions reciprocally affect each other’s evolution.” Coevolution is considered as one of the most defining ecological and (phylo)genetic processes that organize biodiversity in ecosystems through interspecific interactions resulting from the relationship between individuals of two or more species in a community or biocenosis. According to John N Thompson, “coevolution is a pervasive process that continually reshapes interspecific interactions across broad geographic areas. And that has important implications for our understanding of the role of coevolution in fields ranging from epidemiology to conservation biology.” Regarded as a potent evolutionary force and feedback mechanism, the process of coevolution results in a series of adaptive changes in the genotypes and associated traits of the interacting species through inherent reciprocality of coevolutionary selection such that “the fitnesses of two interacting species depend not only on their own genotypes (and associated traits), but also on each other’s genotypes (and traits).”
Coevolution can also be called reciprocal evolution, a term encapsulating the process of mutual evolutionary change that occurs in pairs or groups of species interacting with each other and applying selection pressure to one another. Furthermore, coevolution can be deemed as an example or a subset of mutualism, where “two organisms of different species exist in a relationship in which each individual benefits from the activity of the other.” Specifically, pollination mutualism is a type of service-resource relationship in which “nectar or pollen (food resources) are traded for pollen dispersal (a service)”. Both coevolution and mutualism are thought to be significantly contributing to biological diversity in many ways, including flower forms (vital for pollination mutualisms) and coevolution between groups of species.
Angraecum sesquipedale and Xanthopan morgani as well as Mystacidium capense, Aerangis ellisii and the respective hawkmoths pollinating them, are three good examples of obligatory symbiosis or obligate mutualism, which is a form of symbiosis in which a close and long-term biological interaction between two different species is so indispensable or intricate that both species become highly interdependent and cannot survive on their own. Bound by this type of symbiosis, the host plant and the specific pollinator involved are called obligate mutualists or obligate species.
In contrast, a host plant whose pollination biology is less specialized tends to have non-exclusive nectaries accessible by multiple insect (or animal) species capable of pollinating its flowers. Such a host plant and its varied pollinators represent facultative symbiosis or facultative mutualism, a type of relationship where the survival of the host plant and the pollinator involved is not dependent upon the biological interaction, such that one facultative mutualist or facultative species can survive without the other and vice versa.
Overall, mutualism is essential for the health of many ecosystems, which would deteriorate or collapse without insect- or animal-mediated pollination and seed dispersal. Mutualism is believed to be highly responsible for both reciprocal specialization and coevolutionary diversification, to the extent that there are over one hundred times more existing flowering plant species (angiosperms, including herbaceous plants, shrubs, grasses and most trees) than there are species of all other extant seed-bearing plants (gymnosperms, including the conifers, cycads and ginkgo). In other words, more than 99% of seed plants are flowering plants. Likewise, roughly 75% of all extant animal species are insects. That there are readily observable strong correlations between the number of angiosperm species, floral features and insect families is beyond any reasonable doubt. Appearing 130 million years ago, angiosperms became ubiquitous and diverse by 100 million years ago. The angiosperm radiation had been so rapid and saltational that the rise of flowering plants during the Cretaceous period was designated by Charles Darwin as the “abominable mystery” in his letter addressed to his friend Sir Joseph Hooker in July of 1879. However, the precise roles and contributions of pollinator-plant coevolution to the radiation and diversity of both insects and angiosperms require further refining to iron out the “empirical anomalies and theoretical inconsistencies” in the biotic pollination hypothesis. Moreover, the angiosperm radiation remains somewhat of an “abominable mystery” until more fossil evidence is available to adequately shed light on the rise of the flowering plants, which has also been linked to climatic change (such as increases in carbon dioxide from major geological events), the evolution of herbaceous plants, and even the coevolution with dinosaurs (the last of which was suggested by Bob Bakker in 1986, but yet to be proven with scientific evidence). Hopefully, advances in molecular genetics can contribute solid clues to, and promote more complete understanding of, the (co)evolutionary history of flowering plants and their pollinators.
In any case, insect- or animal-mediated pollination is a reproductive strategy that is not only vital to the evolutionary success and diversity of flowering plants, but also crucial to agriculture and human survival, as 75% of crop species depend on biotic pollination to disperse their pollens. Such evolutionary success and diversity are prodigiously reflected in the size of the Orchidaceae as well as the complex pollination mechanisms and fascinating pollination syndromes characteristic of the large family. Nevertheless, certain researchers in biology and environmental science propose that the taxonomic diversity of the Orchidaceae should not be overly or summarily “attributed to adaptive radiation for specific pollinators driven by selection for outcrossing”, since genetic drift, being one of the fundamental mechanisms of evolution (along with natural selection, mutation and migration) and driven by random environmental events or the vagaries of chance, invariably results in some species or individuals leaving behind a few more descendants (and thus their genes) than other species or individuals regardless of their fitness, to the extent that
orchids are primarily pollination limited, the severity of which is affected by resource constraints. Fruit set is higher in temperate than in tropical species, and in species which offer pollinator rewards than those that do not. Reproductive success is skewed towards few individuals in a population and effective population sizes are often small. Population structure, reproductive success and gene flow among populations suggest that in many situations genetic drift may be as important as selection in fostering genetic and morphological variation in this family. Although there is some evidence for a gradualist model of evolutionary change, we believe that the great diversity in this family is largely a consequence of sequential and rapid interplay between drift and natural selection.
The same researchers conclude that “pollen-limitation of both male and female reproductive success, in combination with the unique structure of the orchid flower (the column), largely explains the extravagant pollination mechanisms.… Paradoxically, it is the low reproductive success of orchids, not the opposite, that may account for both their unique pollination mechanisms and extreme diversity. The Orchidaceae is a remarkable group of plants and the fundamental processes by which the family has diversified are far more fascinating than Darwin ever suspected.”
Whilst Darwin’s evolutionary prediction of the moth’s proboscis in 1862 is remarkable, this example of specific coevolution or pairwise coevolution (such as that of host and pollinator, host and symbiont, host and parasite, or predator and prey) is the exception rather than the rule, given that strict specialization of plants relying on one species of pollinator is relatively rare, as it can lead to variable or unreliable reproductive success when pollinator populations vary significantly or unpredictably. As with many forms of specialization, the exclusivity of a service-resource relationship via pollination mutualism can be a double-edged sword. Thus, plants usually generalize on a wide range of pollinators, and many insect pollinators are generalists visiting various types of flowers, insofar as such ecological generalization is ubiquitous in nature. However, some research “results suggest that a fine-tuned one-to-one coevolutionary state between a flower species and a pollinator species might be common, but frequently overlooked, in multiple flower-pollinator interactions”, and that in stable pollination systems, “one-to-one interactions are likely to be favorable, as opposed to the one-to-many or many-to-many interactions, typical in other mutualisms.” In contrast, some researchers not only caution against assuming that coevolution and selection pressures resulting from interspecific interactions necessarily or invariably lead to specialization, but also highlight the evolutionary advantages and wider ecological implications of plant generalization and pollinator generalization:
Pollinator generalization is predicted when floral rewards are similar across plant species, travel is costly, constraints of behavior and morphology are minor, and/or pollinator lifespan is long relative to flowering of individual plant species. Recognizing that pollination systems often are generalized has important implications. In ecological predictions of plant reproductive success and population dynamics it is useful to widen the focus beyond flower visitors within the “correct” pollination syndrome, and to recognize temporal and spatial fluidity of interactions. Behavioral studies of pollinator foraging choices and information-processing abilities will benefit from understanding the selective advantages of generalization. In studies of floral adaptation, microevolution, and plant speciation one should recognize that selection and gene flow vary in time and space and that the contribution of pollinators to reproductive isolation of plant species may be overstated. In conservation biology, generalized pollination systems imply resilience to linked extinctions, but also the possibility for introduced generalists to displace natives with a net loss of diversity.
Moreover, across the vast, open systems in the ecosphere, plants and animals tend to coevolve within extended networks of multispecies ecological interactions, resulting in diffuse coevolution or guild coevolution, in which whole groups of species interact with other groups of species, leading to changes that cannot be designated as instances of specific or pairwise coevolution between two species. Throughout the expanse of coevolutionary dynamics, new modes of flower-pollinator interaction and diverse forms of insect-plant relationship can emerge and evolve, even though some of them may initially elude discovery, confound expectation, or defy conventional classification. A good example can be studied in an academic article entitled “The Pollination Ecology of an Assemblage of Grassland Asclepiads in South Africa”, available from Annals of Botany, an international plant science journal publishing novel and rigorous research. It is also cited and contextualized by Wikipedia as follows:
… new types of plant-pollinator interaction, involving “unusual” pollinating animals are regularly being discovered, such as specialized pollination by spider hunting wasps (Pompilidae) and fruit chafers (Cetoniidae) in the eastern grasslands of South Africa. These plants do not fit into the classical [pollination] syndromes, though they may show evidence of convergent evolution in their own right.
All in all, phenotype variations emerge out of the coevolutionary processes within and between ecological networks, and phenotypes (as well as extended phenotypes) appear and disappear over time. The multispecies interaction patterns and coevolutionary dynamics are determined not only by biodiversity, the abundance of individuals expressing each phenotype, but also by sustainability, the preservation of viable environments in which individuals and species can persist with ongoing evolutionary change, and in which species interactions can be maintained. In this regard, there has been a substantial shift from preserving speciﬁc phenotypic variants by deploying taxonomic data to describe the constituent species through the traditional assessment of their morphological characters, to preserving the ecological and evolutionary processes via which biodiversity is engendered. In essence, understanding these processes with respect to coevolution is essential for improving the aims, scopes and outcomes of conservation. And in turn, the concept of species as having the objective reality or embodiment of gene flow, and the assumption or assertion that species is always the preferred unit and fundamental currency of conservation, can be reassessed.
There has also been a corresponding shift of the intellectual kind happening in the life of a featured author at ✿❀ Queensland Orchid International ❀✿ and a featured guest at 🦅 SoundEagle : Dr Craig Eisemann is a retired biologist and entomologist who used to work for a major government organization to conduct entomological research with respect to parasite-host relationship as applicable to molecular biosciences, molecular animal genetics, and agricultural sciences in general, and more specifically to tropical animal production, tropical agriculture, insect biochemistry and immunological control, such as vaccination and antibody-mediated inhibition. Like most researchers, Dr Eisemann’s career was occupied with projects with sharply defined problems, which he and his colleagues investigated and solved with the experimental method (though researchers in other related or unrelated fields may otherwise elect to use the historical, descriptive, correlational and/or causal-comparative methods, depending on academic disciplines, research problems and relevant contexts), in addition to dealing with administration, bureaucracy and corporate culture as they arose. Unlike Charles Darwin who had substantial financial inheritance and professional freedom to pursue wide-ranging interests from biology to geology, modern-day academics and researchers are increasingly specialized or vocationalized, blindingly honing their skillsets on pinpointing minutiae to outshine others in their respective microniches. Gone are the big narratives and grand syntheses, unless one has the time and resources to go against prevailing trends to wield long and meandering strokes on the large canvass of a book, let alone a multi-chapter magnum opus. In this respect, James Stapley, a marine biologist and orchid enthusiast working in the ASCLME Project for the United Nations Development Programme, has summed up the predicament and impasse whilst guest-blogging for Linda Markovina, a freelance photography and travel journalist, about “Darwin and the Lost Art of the Naturalist”:
From an age when a naturalist would study anything and everything of interest, we now have researchers who might spend their entire career working on so small a topic as a single species or even a single enzyme system. Whilst such a depth of knowledge can be absolutely invaluable, many of the “important” questions, particularly at a societal level, are really “big picture” or “synthesis” overviews of not only many different scientific disciplines, but also benefit from the input of social, economic, political and even “humanities” disciplines. In an era where we have so many specialists, most of whom can scarcely understand the jargon of the research group down the corridor, where are the generalists who can help us [to] pull together these separate threads and weave them into a richly informative tapestry?
Even the publication style that the modern research “industry” seems to encourage increasingly drives this fragmented approach. There is little room for the grand treatise or synthesis (the odd exception, like IPCC reports, aside) – modern publication is overwhelmingly dominated by many, very short, highly focussed papers, often many from the same research team on very slightly different aspects of effectively the same research question (and often from the same data). Publish or Perish, Research Output Volume (measured by number of publications – the accountant’s metric of scientific “productivity”) encourages more and more of this “mini-paper”, “same data, slightly different angle” approach.
This fragments the research landscape still further…
Funding agencies generally like to see a depth of research (and occasionally strong citation of that research) on a particular topic, or obviously related research avenues. I strongly suspect many of them would not positively review funding requests from a researcher with as varied a research output as a modern day Darwin. This perhaps suggests that “generalist” scientists will never be those that attract high “career researcher” ratings. Perhaps they’ll be more likely to lurk on the scientific “fringe” – people like science bloggers, journalists, and “hobby” researchers. Some of them might ultimately collate a lifetime of observations into one or more significant books – but this seems a remote possibility.
Furthermore, the pressure of having to satisfy research quotas or agendas, and the stress to fulfil corporate expectations and business interests, can create or exacerbate issues about integrity, transparency and reproducibility of scientific research, and also increase the likelihood of questionable research practices involving fraud, misconduct, misrepresentation and falsification, often in an effort to obtain some desired outcomes. One can no longer automatically assume that those who have been conscientious and ethical in applying research can remain untainted or unaffected by such practices, since retractions of scientific papers and the reasons for their retractions are not always publicized. Given that the transparency of the retraction process can be dubious, other researchers as well as the media and the public unaware of the retractions may quote or broadcast invalid research findings, or even make decisions or commitments based on invalid results.
In spite of this, those who are conscientious would still like to be confident that their due diligence can be exercised to foster good understanding about various research methodologies and pitfalls, including the art and science of falsification (and of questioning), in order to gauge the validity and reliability of research findings, including their interpretations and assumptions. These abilities are not necessarily easy to cultivate by being (or functioning as) a “normal” or “regular” academic, given that the science and philosophy of research (and of knowledge) are very complex, and there are good reasons to be so. Perhaps such abilities are even more essential in analyses of, or discussions on, subject matters that are seldom or inadequately explained, debated or resolved.
Taking all of the aforementioned matters into account, one can begin to realize that this post is much more than an attempt or an opportunity for a scientist (or anyone for that matter) to ask or broach the question “Do Plants and Insects Coevolve?”, a (kind of) question that cannot always be well served or properly approached by the format and scope of a conventional scientific article or experiment. Indeed, whatever or however one would like to designate what can be amply witnessed and experienced here — a flashy webpage, a hybrid blog post, a topical assignment, an educational article, an academic paper, a literature review, or a dual-author essay — one could have qualitatively identified the pairwise coevolution, reciprocal evolution, mutualism, symbiosis and service-resource relationship between Dr Craig Eisemann and SoundEagle, all of which are rendered even more plausible or desirable when one also considers the rationale and validity of the latter’s following statement about Orchids in Perspectives commensurate with the aims and missions of ✿❀ Queensland Orchid International ❀✿:
In completing this Foreword, and before serving the , SoundEagle would like to invite all and sundry to contemplate the significance and profundity of Jason D Hoeksema’s opening statements about Geographic Mosaics of Coevolution:
Species constantly engage in strong interactions with other species — parasites, predators, prey, and mutualists. As a result, their traits may coevolve and diversify in geographic mosaics.… Since Darwin and Wallace, studies on coevolution have shown that species interactions can drive rapid and sustained evolutionary change in species at multiple spatial and temporal scales, generating genetic diversity within populations, leading to adaptive differentiation among populations, and often leading to ecological speciation (Schluter 2009). It has been argued that much of the diversity on earth is a consequence of coevolutionary diversification in species interactions (Thompson 1994, 2005, Ehrlich & Raven 1964). Clearly, studies of coevolution in species interactions can lend insight into the fundamental processes generating and maintaining biodiversity, including genetic and phenotypic diversity within and between species.
Orchid (Dracula lafleurii) flower with pollinator flies, Ecuador
ೋღஜஇ CRAIG EISEMANN at SoundEagle🦅 இஜღೋ
Coevolution is usually defined as a reciprocal influence of at least two interacting species on each other’s evolution. For insect–host plant interactions, possible examples include the development of toxic or at least distasteful chemical constituents in plants as an evolutionary response to insect attack and the evolutionary response of some plant-feeding insects to these, and various adaptations found in flowers and pollinating insects which combine to permit and enhance a mutually beneficial relationship. It remains a matter for debate whether such developments truly exemplify coevolution as defined above; the evidence in favour of this interpretation appears most persuasive for flowers and their pollinators and at least some symbiotic relationships between ants and plants, in view of the multiple apparent adaptations seen on both sides of these relationships. In some instances, such as the development of long nectaries in flowers and correspondingly long sucking tubes in their specialized pollinators, attempts to model the evolutionary processes involved mathematically may strengthen the evidential basis for deciding whether a true coevolutionary process has occurred. A presumed coevolutionary relationship between two species or groups of species may be extended by the intrusion of other species not originally involved in the relationship, as in the case of aggressive flower mimicry by predatory insects that prey on pollinators of the mimicked flowers. Another kind of extension of a putative coevolutionary relationship is exemplified by Mullerian mimicry, in which insect species that have evolved to tolerate and sequester toxic or distasteful chemical compounds from their food plants have also coevolved to resemble each other visually, and yet another by Batesian mimicry, in which a palatable species, which does not feed on a toxic host plant, has evolved to resemble visually a toxic insect that does. The association between plants and plant-feeding insects is one of great antiquity, and it is suggested that coevolutionary relationships in their broadest sense should be conceived as occurring between whole evolutionary lineages over long periods of geological time.
Plants and the insects and other animals that interact with them can obviously each influence the ability of the other to survive and reproduce. For example, plant-feeding insects grow and develop by destroying a plant’s stem, leaf or root tissue, or its seeds, or else suck its sap, while insects that collect nectar or pollen from flowers may perform a crucial role in spreading pollen between plants (or individual flowers) and hence facilitate reproduction by plants of the species used in this way. Therefore, a clear potential exists for plants and the insects and other organisms associated with them to influence each other’s evolution, by selecting for traits that may confer some protection for plants against insect attack, facilitate insects’ exploitation of plants or enhance a mutually beneficial relationship. Some biologists have developed this concept further by suggesting that plants and plant-utilizing insects (as well as pairs of other interacting species) often cause reciprocal evolutionary change in each other, a process usually termed “coevolution”.
The term “coevolution” was popularized in a well-known paper by P R Ehrlich and P Raven, published in 1964, in which butterflies and the host plants fed on by their caterpillars were discussed as an example of mutual evolutionary change in two interacting groups of organisms. The authors demonstrated a broadly consistent pattern of association between taxonomic groups of butterflies and particular taxonomic groups of plants. Their discussion centred around the chemical constituents of the plants, in particular their “secondary” compounds. These are a complex mixture of various classes of chemicals, including alkaloids, terpenoids and glucosinolates, which are often produced in specialized epidermal cells and are commonly assumed to have no direct role in plant structure or physiology. The occurrence of these compounds varies widely among taxonomic groups of plants; many plant groups are characterized by the presence of particular classes of secondary compounds. These authors, like other investigators before them, suggested that the presence of secondary compounds evolved as a defence against plant-feeding insects, as many are known to be toxic, in some degree, to various organisms.
The argument presented in the above paper depended upon the concepts that insects feeding on plants do indeed exert significant “selective pressure” on them. In essence, the damage they cause significantly reduces the plant’s ability to survive and reproduce, and that the presence of secondary compounds is an evolutionary response of the plant to this pressure, conferring a degree of immunity to insect attack and hence improving the plant’s ability to survive and leave viable offspring. An “immune” plant species could then perhaps more easily colonize new habitats or ecological niches, giving rise to additional species in the process and resulting in the eventual appearance of a group of species, constituting a genus, family or even higher classification, characterized by the presence of one or more classes of secondary compounds. This process is sometimes described as “escape and (evolutionary) radiation” or “escape-and-radiate coevolution”.
Some insect species may in turn evolve to tolerate the toxic constituents of certain plants, often by evolving the capacity for biochemical detoxification of the compounds involved; this development would allow them to exploit these plants as food. The insects may in fact go further, evolving the ability to use these originally protective secondary compounds as “token” attractants (in the case of volatile compounds) or stimulants of feeding or egg-laying to assist their utilization of plants to which they have become adapted. Insects that have adapted to a plant species or group of species having a similar chemical constitution could then, in the absence of competition from other plant-feeding species, readily give rise to new species adapted to related plants having a generally similar, though not necessarily identical, suite of secondary chemical compounds. In this way, taxonomically-related groups of butterflies (and other plant-feeding insects) could come to use as their food plants, particular taxonomically-related groups of plants containing generally similar secondary compounds. The processes described above may be repeated with the appearance of novel plant defences (not only chemical; see below) and subsequent insect adaptations to them, resulting in a parallel proliferation of new plant and insect taxonomic groups. A hypothetical illustration of this is presented in the following figure.
However, other researchers have argued that the above and other examples have not demonstrated conclusively the occurrence of coevolution, that is, of mutual evolutionary change in at least two interacting species, resulting from their interaction over time. For example, the Hungarian entomologist Tibor Jermy, in a series of papers published from 1976, contended that, in most natural ecosystems, plant-feeding (“phytophagous”) insects have a very much smaller biomass than their food plants and therefore inflict only minor damage on them. This means that the insects exert very little selective pressure on their host plants, so that there will be little tendency for the plants to evolve protective adaptations to their insect “predators”. Secondary chemicals, Jermy asserts, occur in plants because they perform functions unconnected with deterring herbivore attack — they may be intermediate metabolites or simply waste products of biochemical processes. Therefore, the process involved is not one of coevolution but of one-way “sequential evolution” — plants produce secondary chemicals for their own purposes and insects and other herbivores adapt to them.
A further objection to the idea that plant chemistry is, in part, an evolutionary response to insect attack is that many non-host plants are not in fact toxic to many phytophagous insect species and even specific chemicals known to deter feeding and egg-laying may not be toxic, at least at the concentrations occurring in plants: insects’ host plant specificity is determined not by avoidance of toxicity but by other factors. These may include the presence or absence of sensory cues such as constituent volatile or non-volatile chemical compounds, and visual and tactile characteristics, all of which can mediate acceptance or avoidance of particular plant species. The original selective pressure that led insects to specialize in using certain host plants may have come from factors such as competition with other plant-feeding species and avoidance of predators, and the responses to specific sensory stimuli evolved by insects in identifying and locating their host plants may then have the effect of limiting them to host plants having the required presence or absence of sensory cues, irrespective of the potential suitability of other plants as sources of food.
These objections may be answered, to some degree, by noting firstly that even relatively slight selective pressure can, over many generations, result in significant evolutionary change and secondly that patterns of utilization of plants by insects that are in evidence at present are the product of an evolutionary association between the two that has continued for tens or even hundreds of millions of years. During this long association, many insects may have evolved to acquire a tolerance to many originally toxic plant chemicals that appeared as defences against insect attack in the remote past and persist, for various reasons, in a wide variety of present-day species. In any case, the fairly high degree of host-plant specificity observed in present-day insects will have the effect of limiting the abundance of most phytophagous insects because of the difficulty of finding suitable host plants scattered among many others in the ecosystem during the (usually short) lifetime of a searching insect. Such a constraint may have operated less strongly at an earlier stage in the evolutionary association between insects and plants when many insects may have been able to use a higher proportion of available plants, hence increasing the selective pressure on plants to evolve chemical and other defences. In any case, it is important to recognize that, as for other characters, plant chemistry may result from a variety of selective influences; even if defence against phytophagous insects and other herbivores is accepted as being important among these, it is not necessary to attribute the entire suite of plant secondary chemicals to this cause.
Current plant defences are not limited to toxic secondary chemicals, and may include such characters as fine hairs (trichomes) on leaves and stems and latex circulating in plant conductive tissues that may immobilize and kill small larvae. An interesting example is the ocurrence of small yellow structures on leaves and stems of Passiflora species (passion vines) that resemble visually the eggs of butterflies of the genus Heliconius that feed on Passiflora as larvae. This apparent adaptation is illustrated in the following article.
These structures tend to deter the butterflies from laying eggs on these plants, as they normally avoid laying eggs near existing eggs, thereby minimizing overcrowding and cannibalism among larvae. This example may show evidence of a “coevolutionary arms race”, in which a plant has responded to insect attack by evolving toxic chemical constituents (in this case including cyanogenic glucosides) that deter most herbivores from feeding on them, a group of insect species has in turn evolved a biochemical tolerance for these compounds, allowing them to feed on an otherwise toxic plant, and the plant has in turn responded to this further challenge by evolving deterrent structures specific to these insects.
A seemingly less controversial example of plant-insect coevolutionary relationships is provided by flowering plants and nectar- and pollen-feeding insects. Pollination of flowering plants by insects may have originated in early angiosperms, which were all initially wind-pollinated. It has been suggested that, as in extant gymnosperms such as conifers, droplets of sap were secreted by the ovule to catch pollen grains floating in the air. Insects began to use this sap as a food resource, incidentally transferring pollen grains between plants. As both “partners” benefitted from this relationship, natural selection acted on both groups of organisms to produce, on the one hand, more “attractive”, easily-located flowers, and on the other, specific structural, physiological and behavioural adaptations to allow the insects to better locate the flowers and to exploit their contained nectar and/or pollen. In general terms, this may constitute an example of “guild” or “diffuse” coevolution, which occurs between groups of species, rather than individual species. Different plant species may nevertheless evolve to target particular groups of pollinators or even individual species. For example, flowers pollinated by diurnal insects (those active during daylight) such as butterflies or wasps, which are often strongly visually-oriented, are frequently brightly-coloured, whereas flowers pollinated by nocturnal insects (such as most moths) tend to be pale-coloured and hence more visible in low light. Flowers visited predominantly by nocturnal foragers also produce more odourous chemicals, this characteristic being more suited to these insects, which tend to be more dependent upon responses to odours. Some additional information about flowers and pollinators is available on the following webpage.
A strikingly close evolutionary relationship between a single species (or group of closely-related species) of plant and a single species of pollinator is exemplified by the Madagascan Star Orchid Angraecum sesquipedale and its pollinator, the hawkmoth Xanthopan morgani. In this orchid, the nectar is produced at the end of a remarkable corolla tube in the form of a spur some 20 to 35 cm long. In his book on pollination of orchids, published in 1862, Charles Darwin predicted that some moth with a haustellum (specialized sucking tube) sufficiently long to reach the nectar at the end of this spur must exist in the orchid’s geographical range. Subsequently, Darwin’s contemporary and fellow evolutionary theorist Alfred Russel Wallace suggested that this moth would probably be a hawkmoth (family Sphingidae). In 1903, X. morgani, which was already known from Africa, was found to occur in Madagascar as well, but it was not until 1997 that it was shown to pollinate A. sesquipedale and other members of its genus. The orchid and its pollinator are illustrated below.
A video of the moth visiting this orchid in its natural environment can be viewed below.
In this mutualistic association between species, the coexistence of an unusually long nectary in the orchid and an unusually long haustellum in the moth has the effect of limiting pollination of these orchids to the one species of pollinator. This situation has the potential advantage for the orchid, which is said to be quite rare in its natural forest habitat, of ensuring that its pollen is transferred preferentially to other individuals of this species rather than being “wasted” by transfer to flowers of other species. Whilst having a long haustellum does not necessarily preclude access to nectar in species that do not have a long corolla tube, there may be an advantage to the moth (which is apparently also rare in its natural habitat) in specializing in collecting nectar from a particular species (or group of related species) for which it has no competitors, and hence a more assured supply of nectar. For the success of this relationship, it is important that the nectary be long enough to exclude other nectar-feeding species but not too long to be reached by X. morgani. Further, it is important for the orchid that the moth’s haustellum be only just sufficiently long to reach the nectar at the tip of the corolla tube, so that the head of the moth rubs against the anthers of the flower, collecting pollen that can subsequently be transferred to other flowers of the same species.
Angraecum sesquipedale (Darwin’s orchid, Christmas orchid, Star of Bethlehem orchid, Madagascan Star orchid, Comet orchid, King of the Angraecums, The One and a Half Foot Long Angraecum), Madagascar
Much commentary about the causes of particular evolutionary events is necessarily speculative, concerning as it does events and conditions that occurred in the remote past. In some cases, mathematical modelling may help to put such speculations on a somewhat firmer basis. Deep corolla tubes and long sucking tubes in pollinators appear to have evolved repeatedly in orchids and hawkmoths as well as in other groups of organisms, the pollinators including hummingbirds, nectar-feeding bats and certain species of flies. A group of researchers have attempted to model the evolution of these adaptations in general terms. Their models have shown firstly that, in the presence of pollinators with long and short tongues that are competing for nectar, coexisting plant species will evolve corolla tubes of different lengths, as this will increase the proportion of their pollen grains being deposited on flowers of the same species. Secondly, for two plant and two pollinator species, all having a similar range of corolla tube depth or tongue length, variability in corolla tube depth within the two species will result in the evolution of different tongue lengths in the two pollinator species, provided that it is not equally costly in terms of energy for the two species to increase their tongue length, and that scarcity of nectar is a limiting factor for the survival of the pollinators. Once a difference in tongue length between the two pollinator species has become established, a divergence in corolla tube depth between the two plant species will develop. These conclusions hold for a wide range of assumptions about prevailing conditions, and therefore provide evidence that coevolution of these characters in interacting species can indeed occur. In explaining how “Resource Competition Triggers the Co-Evolution of Long Tongues and Deep Corolla Tubes”, Miguel A Rodríguez-Gironés and Ana L Llandres Resource demonstrate their main model components as follows.
The associations that have developed between certain species of ant and particular plants provide further likely examples of coevolutionary relationships. More than 100 genera of plants are known to be “myrmecophytes” — plants that live in a mutualistic relationship with a colony of ants. The plants provide food for their associated ants in the form of sugars and amino acids secreted from extrafloral nectaries or via sap-sucking insects that first obtain them from the plant, and in some cases in the form of specialized structures rich in proteins and lipids. Myrmecophytes also provide “domatia” — specialized plant structures containing cavities that can be occupied as nesting sites by their ant symbionts.
Several species of acacia (the “swollen thorn” acacias native to the tropical Americas) have evolved strong mutualistic relationships with ants of the genus Pseudomyrmex. The association between Vachellia (formerly Acacia) cornigera and Pseudomyrmex ferruginea has been studied in detail by Daniel Janzen. This species of tree has evolved a number of adaptations, not shared with non-myrmecophytic acacias, that foster this relationship: enlarged thorns in which the ants find shelter (domatia), enlarged leaf nectaries from which the ants obtain sugars and amino acids, modified leaflet tips (“Beltian bodies”) rich in proteins and lipids that are consumed by the ants and their larvae, and year-round production and maintenance of leaves, even in dry seasons.
Occupation of a Vachellia cornigera plant by Pseudomyrmex ferruginea begins with a dispersing mated Queen attracted by the odour of the acacia. She then cuts her way into a hollow thorn or uses an existing entrance hole; inside the thorn she lays eggs and rears the first brood of workers. As the colony expands, the workers eventually occupy all of the thorns on the plant and sometimes spread to neighbouring plants of the same species; the population of a colony may reach as many as 30,000 workers. The ants, which are highly aggressive and possess, to human perception, an especially painful sting, patrol the host tree, killing most intruding insects, deterring browsing mammals and even pruning encroaching plants of other species to maintain a clear space around it. (However, the ants protect scale insects feeding on the host tree, as these are a source of honeydew consumed by the ants). The following illustration and video show some activities of P. ferruginea on its host tree:
The relationship is essentially an obligate one on both sides: the occupying ants obtain the great majority of their food from the tree and have adapted many aspects of their behaviour to occupy, exploit and protect their symbiotic plant; on the other hand, the benefits to the acacia from the association are shown by the fact that individuals of V. cornigera deprived of their ant symbionts are severely damaged by phytophagous insects and browsing goats and rodents, and in many environments tend to become overgrown by competing plant species. An interesting observation made by Janzen is that this species of acacia appears to have lost its ability to resist attack by insects and mammals as well as competition from other plants. Its leaves are not bitter to human taste, unlike those of non-myrmecophytic acacias, and are preferred to them by browsing mammals if the tree is not occupied by P. ferruginea. This species seems to have ceased using energy to produce feeding-deterrent chemical compounds; these are presumably not necessary since their protective functions have been assumed by the ant symbionts. Instead, V. cornigera has diverted energy towards producing outsized thorns, large extrafloral nectaries and Beltian bodies as supports for its myrmecine defence system.
A further example of a mutualistic relationship between a plant and an attendant ant species is provided by the carnivorous fanged pitcher plant Nepenthes bicalcarata and a species of carpenter ant, Colobopsis (formerly Camponotus) schmitzi. The pitcher plant inhabits mainly peat forests in north-western Borneo. N. bicalcarata is unique among some 120 species of its genus in in being a myrmecophyte; it is also unusual in lacking a waxy layer on the peritreme (the “lip” of the insect-capturing “pitcher”), and in having a fluid inside its pitchers that is less acidic and viscoelastic than that of other Nepenthes species. In addition, it may lack the digestive enzymes that occur in the pitcher fluid of other species of its genus.
The associated ants nest in domatia formed in swollen, hollow tendrils; worker ants also conceal themselves underneath the peritreme, from where they “ambush” insects landing on the peritreme. They also appear to clean the peritreme of debris and fungal growth. The ants can swim actively in the pitcher fluid, from which they remove the larger prey items that fall into it, as well as some of the infauna of insect larvae (such as mosquito larvae) that normally inhabit the pitcher fluid. The low viscoelasticity of the fluid enhances the ability of the ants to remove prey from it, and the low acidity and possible lack or inactivity of digestive enzymes permit both ants and infauna to survive in it. The next illustration and video show some of the details of the relationship.
The ants obviously consume part of the prey (and infauna) found in the pitchers; on the other hand, they benefit the plant by increasing the capture rate of prey through ambush and the preservation of a smooth peritreme surface, by digesting prey and making part of it available to the plant by depositing faeces into the pitchers, by providing ant carcasses which fall into the pitchers and by protecting the plant from phytophagous insects, in particular from a species of weevil that attacks growing shoots. They may also assist the plant by preventing accumulation of organic material in the pitchers to the point where putrefaction occurs, an event that would probably be deleterious to the plant, as well as to its possibly beneficial infauna.
In return, N. bicalcarata provides C. schmitzi with nesting sites in the form of domatia, prey occurring in and around the pitchers, sugar and amino acids from the large nectaries in the “fangs” that are located above the mouth of each pitcher. The net effect of the association on the plant seems to be definitely beneficial: N. bicalcarata plants inhabited by C. schmitzi have more leaves, a greater total leaf area, less abortive pitcher development (as a result of protection from weevil attack) and larger pitchers. Plants colonized by C. schmitzi have been shown to have more nitrogen available to them than those not colonized, and more of this nitrogen is of insect origin.
The relationship for N. bicalcarata is, however, facultative rather than obligate, as the plant can survive in the absence of its ant symbiont. Nevertheless, plants without C. schmitzi colonies appear to derive no net benefit from their pitchers; the adaptations that foster the mutualistic relationship with this ant species (such as low acidity and viscoelasticity of its pitcher fluid and the possible lack of digestive enzymes) appear to have reduced its ability to derive nutrients from its pitchers in the absence of its ant symbiont. N. bicalcarata has adopted an alternative strategy for obtaining supplementary nutrients from its prey as compared with other species of its genus. For C. schmitzi, the relationship with N. bicalcarata appears to be an obligate one: it is totally dependent on its partner for nutrients and nest sites and apparently rarely leaves its plant host.
In some cases, an established interaction between two species or groups of species may be intruded upon by other species in their community which act as “free-riders” on a mutualistic relationship. An example is provided by the orchid mantis Hymenopus coronatus which has evolved to exploit the relationship between flowers and the various pollinators that visit them. These pollinator insects are preyed upon by the mantid when they are attracted to it because of its strong visual resemblance to flowers (in terms of insect perception, probably to a “generalized” flower rather than specifically to an orchid), despite the strong visual similarity (to human perception) to some orchids that is shown on the webpage below.
A presumed coevolutionary relationship has therefore strongly influenced the evolution of an organism that was not originally part of the relationship. Whether the mantid has itself entered into a coevolutionary relationship with either the flowers or their pollinators (or both) is unclear, and would depend largely upon whether it exerts any significant selective pressure on them, that is, by preying on the pollinators and thereby having an incidental disruptive effect upon pollination.
A different kind of “third party” effect, in which a putative coevolutionary relationship has become extended to affect indirectly one or more additional species can be seen in mimicry involving toxic or distasteful insects. As discussed above, some insects have evolved to tolerate particular toxic secondary chemical constituents of plants, and hence can use plants containing these as food. Such toxic substances can in some cases be stored in the feeding insects and even transferred to later life stages. In other words, toxins accumulated by a caterpillar feeding on a host plant that is toxic to most other animals can be passed on to the later adult stage, such as a butterfly or moth that does not itself feed on the plant. Such insects may then be protected against predators by their stored toxic compounds.
Toxic or distasteful insects and other animals frequently display aposematic (warning) colouration, typically involving a prominent combination of black with yellow, orange or red. This is of advantage to the toxic animals as vertebrate predators, in particular, can learn to avoid prey showing this colouration after having a few unpleasant experiences with them. Often two or more such toxic species, which may or may not be closely related or feed on the same plant species, will evolve to resemble each other visually, so that fewer members of each species will be sacrificed in “educating” predators about the undesirability of eating them: a lesson learned from one such species will apply equally (or nearly so) to the other species in this “mimetic complex”. This condition is referred to as “Mullerian mimicry”. A striking example of this is provided by species of the tropical American butterfly genus Heliconius, the larvae of which feed on species of Passiflora containing highly toxic cyanogenic glucosides, and accumulate these compounds in their tissues and in those of subsequent life stages. The species H. erato and H. melpomene occupy similar geographic ranges in Central and South America, and both show remarkable variation in the colour patterns of their wings among subspecies occupying different areas within their ranges. As is shown in the figure below, there is a high degree of concordance in the wing patterns of subspecies of the two species that occur in the same areas: in each geograpical area, the locally occurring subspecies of these two unpalatable Heliconius species have evolved to resemble each other much more than either resembles other subspecies of its own species occurring elsewhere. In this and other cases, a presumed coevolutionary relationship between plants and phytophagous insects has led to a further coevolutionary relationship between the insects involved, with the effect of maximizing the survival benefit to them of storing plant-derived predator-deterring chemical compounds.
It may also occur that an insect that is not itself toxic or distasteful will evolve to resemble one that is, thereby acquiring some protection from predators (“Batesian mimicry”). In this case the mimic is a “free-rider” on the beneficial relationship that its model has developed with the latter’s host plant. Normally, the mimic is much less abundant than its model, so that the latter’s “lessons” to predators are not counteracted unduly by the presence of the palatable mimic.
In some species of mimic, a similar effect is achieved through polymorphism, whereby different forms occur (often in the same geographical area) resembling different distasteful model species of widely differing appearance. A remarkable instance of this is provided by the African Mocker Swallowtail butterfly Papilio dardanus, the female of which has more than 12 different forms of wing shape and colour, several of which mimic diverse toxic species of butterfly. Some females of P. dardanus closely resemble the males of this species, which are not mimics. In the illustration in the webpage below, various model species from another butterfly family are shown above the line, and corresponding mimetic (and non-mimetic) forms of P. dardanus are shown below it.
In answering the question “Do plants and insects coevolve?”, it is crucial to establish whether each partner in a relationship has influenced the evolution of the other. In some instances, such as that of flowers and their insect pollinators, as well as that of certain plants and their ant symbionts, it appears highly probable that this has occurred. The presence of specializations such as, on the one side, visually conspicuous petals and the production of energy-rich nectar and specialized volatile chemical compounds, and on the other, of specialized mouthparts for obtaining nectar together with sensory and behavioural capabilities attuned to locating flowers using visual and chemical cues seems difficult to account for without invoking reciprocal evolutionary change. In other instances, such as that of plant chemistry, the picture is more equivocal: it is often difficult to prove that insect adaptations to the presence of particular chemical compounds are not purely unilateral ones to characters that evolved in plants for reasons unrelated to insect attack. Even the existence of a mutualistic relationship is not in itself sufficient evidence that a coevolutionary process has occurred; again, it is possible that characters in an organism that are of benefit to its partner may have evolved originally for reasons unrelated to this partner.
It is also important to recognize that many evolutionary adaptations may have occurred not in extant species but in ancestral forms (perhaps distantly ancestral) and have been preserved in their descendants through natural selection because of their continuing usefulness (perhaps not for the original reason). The biological agent that applied the selective pressure resulting in the original adaptation may not have been the same as or even directly ancestral to that which presently interacts with the species concerned. Plants and phytophagous insects have coexisted and interacted over vast periods of time. The main insect orders (including grasshoppers, bugs, beetles, butterflies and moths, and wasps, bees and ants) that contain numerous plant-feeding species are known to have existed since at least the Jurassic period (circa 210 to 145 million years ago) and often considerably earlier than this, antedating the appearance of flowering plants. In considering plant-insect coevolution, it is necessary to take into account events occurring over deep time.
The causes of evolutionary events often remain speculative and controversial, having occurred mostly in the remote past, when conditions may have differed markedly from those prevailing at present. As a result, it is not surprising that it is often difficult to decide whether a true coevolutionary relationship has existed, especially for associations of great antiquity. For more recent associations, a strong indication of coevolution exists if both species or groups of species in an association show characters that are not shared by closely related species. The existence of exaggeratedly long corolla tubes in flowers and commensurately long sucking organs in their pollinators would appear to exemplify this situation. Other likely examples are provided by the physiological and behavioural adaptations on both sides of the mutualistic ant-plant relationships discussed above. Coevolution in its fullest sense, however, should perhaps be conceived as occurring over whole evolutionary lineages, including organisms not necessarily contemporary with each other, and not merely between pairs of extant species. The complexities of such considerations are likely to remain a matter for experiment and speculation by evolutionary theorists far into the future.
- ^ Janzen, D H (1980) When Is It Coevolution? Evolution 34: 611-612. Available at http://www.bio.miami.edu/horvitz/Plant-animal%20interactions%202013/coevolution/required%20readings/Janzen%201980.pdf
- ^ Ehrlich, P R and Raven, P (1964) Butterflies and Plants: A study in coevolution. Ecology 18: 586-608. Available at http://www.esf.edu/efb/parry/Insect%20Ecology%20Reading/Ehrlich_Raven_1964.pdf
- ^ Jermy, T (1976) Insect-Host Plant Relationship — Co-Evolution or Sequential Evolution? Symp. Biol. Hung. 16: 109-113
- ^ Common, I F B and Waterhouse, D F (1981) Butterflies of Australia (2nd Edition). Sydney and Melbourne: Angus and Robertson
- ^ Bernays, E and Graham, M (1988) On the Evolution of Host Specificity in Phytophagous Arthropods. Ecology 69: 886-892
- ^ Thompson, J N (1988) Coevolution and Alternative Hypotheses on Insect/Plant Interactions. Ecology 69: 893-895
- ^ Kulakova-Peck, J (1991) Fossil History and the Evolution of Hexapod Structures. in CSIRO, The Insects of Australia (2nd Edition). Melbourne: Melbourne University Press, pp. 141-179
- ^ Darwin, C (1862) On the Various Contrivances by Which British and Foreign Orchids are Fertilized by Insects, and on the Good Effects of Intercrossing. London: John Murray
- ^ Rodriguez-Girones, M A and Santamaria, L (2007). Resource Competition, Character Displacement and the Evolution of Deep Corolla Tubes. Am. Nat. 170: 455-464
- ^ Rodriguez-Girones, M A and Llandres, A L (2008) Resource Competition Triggers the Co-Evolution of Long Tongues and Deep Corolla Tubes. Available at http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0002992
- ^ Myrmecophytes https://en.wikipedia.org/wiki/Myrmecophyte
- ^ Vachellia cornigera https://en.wikipedia.org/wiki/Vachellia_cornigera
- ^ Pseudomyrmex ferruginea https://en.wikipedia.org/wiki/Pseudomyrmex_ferruginea
- ^ Janzen D.H. (1966) Coevolution of Mutualism Between Ants and Acacias in Central America. Evolution 20: 249-275. Available at http://www.jstor.org/stable/2406628
- ^ Nepenthes bicalcarata https://en.wikipedia.org/wiki/Nepenthes_bicalcarata
- ^ Colobopsis schmitzi https://en.wikipedia.org/wiki/Camponotus_schmitzi
- ^ Bazile V, Moran J A, Le Moguedec G, Marshall D J and Gaume L (2012) A Carnivorous Plant Fed by Its Ant Symbiont: A Unique Multi-Faceted Nutritional Mutualism PLoS ONE 7(5): e36179. Available at https://doi.org/10.1371/journal.pone.0036179
- ^ O’Hanlon J C, Holwell G I, and Herberstein M E (2014) Predatory Pollinator Deception: Does the Orchid Mantis Resemble a Model Species? Current Zoology 60: 90-103. Available at http://www.currentzoology.org/temp/%7B3E2BECB0-59F7-49BD-8B76-4D2B221A61E1%7D.pdf [Note: The link seems to be defunct.]
Evolution, Coevolution, Insect-Plant Relationship, Flower-Pollinator Relationship, Mullerian mimicry, Batesian mimicry, Xanthopan morgani, Angraecum sesquipedale, Heliconius, Hymenopus coronatus, Papilio dardanus, Vachellia cornigera, Acacia cornigera, Pseudomyrmex ferruginea, Nepenthes bicalcarata, Colobopsis schmitzi, Camponotus schmitzi, Myrmecophyte, Domatia, Beltian Bodies, Extrafloral Nectaries, P R Ehrlich, P Raven, D H Janzen, E Bernays, M Graham, T Jermy, J N Thompson, C Darwin, A R Wallace, M A Rodriguez-Girones, L Santamaria, A L Llandres
King Spider Orchid (Caladenia pectinata) being visited by male parasitic wasp pollinator which is attracted to the flower by faux female wasp pheromone, Australia
King Spider Orchid (Caladenia pectinata) being visited by male parasitic wasp which is attracted to the flower by faux female wasp pheromone, western Australia
King Spider Orchid (Caladenia pectinata) flower swarmed by male parasitic wasps who interpret the flower’s red lip as female wasp, western Australia
Warty Hammer Orchid (Drakaea livida) flower has hinge mechanism to manipulate its pollinator into just the right position to receive its pollen, south of Perth, western Australia
Zebra Orchid (Caladenia cairnsiana) flower being pollinated by male parasitic wasp which is attracted to the flower by faux female wasp pheromone, western Australia
Orchid Bee (Euglossa sp) male visiting Orchid (Mormodes sp) flower
Orchid Bee (Euglossa sp) male visiting Orchid (Mormodes sp) flower, Santa Rita, Panama
Orchid Bee (Euglossa sp) male with orchid pollinia attached to its back, Barro Colorado Island, Panama
Bucket Orchid (Coryanthes panamensis) flower attracting male Bee (Apidae) with sweet scent showing pollenia on its back, Gamboa, central Panama
Orchid (Catasetum viridiflavum) with male orchid bee approaching, Barro Colorado Island, Panama
Orchid (Masdevallia caloptera) flower with its pollinator Blue Bottle Fly (Calliphoridae) carrying yellow pollinium on its back, Finca Dracula Orchid Sanctuary, western Panama
Bumblebee Orchid (Ophrys bombyliflora) flower and its male Longhorn Bee (Eucera sp) pollinator, Sardinia, Italy
Bumblebee Orchid (Ophrys bombyliflora) flower and its male Longhorn Bee (Eucera sp) pollinator, Sardinia, Italy
Brown Bee Orchid (Ophrys iricolor) flower mimics female bee with male solitary bee engaged in pseudocopulation, Sardinia, Italy
Orchid (Himantoglossum robertianum) flowers with bee pollinator, Sardinia, Italy
Olive Skipper (Pyrgus serratulae) butterfly on orchid, Hohe Tauern National Park, Austria
Brimstone butterfly (Gonepteryx rhamni) feeding on Fragrant Orchid, UK
Bee pollinating a common spotted orchid (Dactylorhiza fuchsii). This process of pollination is called Entomophily, whereby pollen is inadvertently distributed by insects to other flowers. Photographed in Kent, UK.
Common blue butterfly (Polyommatus icarus) feeding on a fragrant orchid (Gymnadenia conopsea). Photographed in June in Kent, UK.
Female common blue butterfly (Polyommatus icarus) resting on a southern marsh orchid (Dactylorhiza praetermissa), Dawlish Warren Nature Reserve, Devon, England
Pair of marsh fritillary butterflies (Euphydrayas aurinia) resting on a heath orchid flower (Dactylorhiza fuchsii) in the countryside of Devonshire.
Five-spot burnet moths (Zygaena trifolii) mating on Pyramidal orchid (Anacamptis pyramidalis) in Cornish countryside
- Do Plants and Insects Coevolve? 🥀🐝🌺🦋 (queenslandorchid.wordpress.com)
- Flowers and insects: an ancient alliance (rcannon992.com)
- ‘Good Heavens what insect can suck it’- Charles Darwin, Angraecum sesquipedale and Xanthopan morganii praedicta (academia.edu) Joseph Arditti, John Elliott, Ian J. Kitching, and Lutz T. Wasserthal (2012). ‘Good Heavens what insect can suck it’- Charles Darwin, Angraecum sesquipedale and Xanthopan morganii praedicta. Botanical Journal of the Linnean Society, 169, 403–432.
- “The Orchids Have Been A Splendid Sport” — An Alternative Look at Charles Darwin’s Contribution to Orchid Biology (academia.edu) Tim Wing Yam, Joseph Arditti, and Kenneth M. Cameron (2009). “The Orchids Have Been A Splendid Sport” — An Alternative Look at Charles Darwin’s Contribution to Orchid Biology. American Journal of Botany 96(12): 2128–2154.
- The Origin of Modern Biodiversity: Coevolution of Flowers and Insects (bioteaching.wordpress.com)
- Fine-tuned Bee-Flower Coevolutionary State Hidden within Multiple Pollination Interactions (nature.com) Akira Shimizu, Ikumi Dohzono, Masayoshi Nakaji, Derek A. Roff, Donald G. Miller III, Sara Osato, Takuya Yajima, Shûhei Niitsu, Nozomu Utsugi, Takashi Sugawara and Jin Yoshimura (2014). Fine-tuned Bee-Flower Coevolutionary State Hidden within Multiple Pollination Interactions. Scientific Reports 4, Article number: 3988. doi:10.1038/srep03988
- Coevolution (lifeofplant.blogspot.com.au)
- Interplay between insects and plants: dynamic and complex interactions that have coevolved over millions of years but act in milliseconds (jxb.oxfordjournals.org) Also available at http://jxb.oxfordjournals.org/content/66/2/455.full.pdf+html
- Did insect pollination cause increased seed plant diversity? (wolfweb.unr.edu) Root Gorelick (2001). Did insect pollination cause increased seed plant diversity? Biological Journal of the Linnean Society, 74: 407-427.
- Coevolution and Pollination (wnps.org)
- Interactions between Herbivorous Insects and Plant-Insect Coevolution (sites.biology.duke.edu)
- Coevolution (en.wikipedia.org)
- Mutualism (biology) (en.wikipedia.org)
- What is a mutualism? (standingoutinmyfield.wordpress.com)
- Coevolution of Mutualism Between Ants and Acacias in Central America. (jstor.org) Janzen D.H. (1966) Coevolution of Mutualism Between Ants and Acacias in Central America. Evolution 20: 249-275.
- Coevolution (britannica.com)
- Coevolution (bio.miami.edu)
- Lecture 9. Plant-Insect Interactions (ag.arizona.edu)
- Geographic mosaic theory of coevolution (britannica.com)
- Orchid (britannica.com)
- Mimicry (britannica.com)
- The Geographic Mosaic of Coevolution (thompsonlab.sites.ucsc.edu)
- Geographic mosaic theory of coevolution (nature.com) Hoeksema, J. D. (2012) Geographic Mosaics of Coevolution. Nature Education Knowledge 3(10):19
- Coevolution: The Geographic Mosaic of Coevolutionary Arms Races (sciencedirect.com) John N Thompson. Coevolution: The Geographic Mosaic of Coevolutionary Arms Races. Current Biology, Volume 15, Issue 24, 24 December 2005, Pages R992–R994
- The Geographic Mosaic of Coevolution (scielo.org.ar)
- Plant-insect interactions: an evolutionary arms race between two distinct defense mechanisms (scielo.org.br)
- Research proposal: Predicting coevolutionary patterns on a global scale (spsasevo.wikidot.com)
- Evolution for beginners 2: coevolution (allyouneedisbiology.wordpress.com)
- Plants and animals can also live in marriage (allyouneedisbiology.wordpress.com)
- Orchids: different colours and shapes for everyone (allyouneedisbiology.wordpress.com)
- When Is It Coevolution? (bio.miami.edu) Janzen, D H (1980) When Is It Coevolution? Evolution 34: 611-612″. Also available from biologia.bio.br
- Resource Competition Triggers the Co-Evolution of Long Tongues and Deep Corolla Tubes (journals.plos.org)
- Book review: “Pollination and Floral Ecology” by Pat Willmer (researchspace.ukzn.ac.za)
- Pollinators and pollination – something for the weekend #9 (researchspace.ukzn.ac.za)
- Fossil Focus: Arthropod–plant interactions (palaeontologyonline.com)
- Orchid Mantis: Imitation and Disguise (queenslandorchid.wordpress.com)
- Secrets of the orchid mantis revealed – it doesn’t mimic an orchid after all (jdjgilbert.wordpress.com)
- Secrets of the orchid mantis revealed – it doesn’t mimic an orchid after all (theconversation.com)
- Pollinator Deception in the Orchid Mantis (jstor.org) O’Hanlon, J., Holwell, G., Herberstein, M., & Natural History Editor: Mark A. McPeek (2014). Pollinator Deception in the Orchid Mantis. The American Naturalist, 183(1), 126-132. doi:1. Retrieved from http://www.jstor.org/stable/10.1086/673858 doi:1
- Predatory pollinator deception: Does the orchid mantis resemble a model species (currentzoology.org) [Note: The link seems to be defunct.] J. C. O’Hanlon, G. I. Holwell, M. E. Herberstein (2014). Predatory pollinator deception: Does the orchid mantis resemble a model species. Current Zoology 60(1): 90–103.
- The evolution of imperfect mimicry in hoverflies (eprints.nottingham.ac.uk) Gilbert, Francis (2004). The evolution of imperfect mimicry in hoverflies. Insect Evolutionary Biology. CABI. (In Press)
- The Roles of Colour and Shape in Pollinator Deception in the Orchid Mantis Hymenopus coronatus (onlinelibrary.wiley.com)
- Orchid Mantis Perfectly Mimics Flowers In Order To Lure Prey [VIDEO] (isciencetimes.com)
- Mantis: las reinas del mimetismo (allyouneedisbiology.wordpress.com)
- Mimicry (en.wikipedia.org)
- Batesian mimicry (en.wikipedia.org)
- Müllerian mimicry (en.wikipedia.org)
- Aggressive mimicry (en.wikipedia.org)
- New paper: genetics of red pattern elements in Heliconius erato and Heliconius melpomene (heliconius.org)
- Butterfly Genetics Group: Martin Thompson (heliconius.zoo.cam.ac.uk)
- Darwin, C. R. 1862. On the various contrivances by which British and foreign orchids are fertilised by insects, and on the good effects of intercrossing. London: John Murray. (darwin-online.org.uk)
- Darwin, C. R. (1877). The various contrivances by which orchids are fertilised by insects. London: John Murray. 2d edition. (darwin-online.org.uk)
- Guest Blog: Darwin and the Lost Art of the Naturalist (movingsushi.com)
- Angraecum sesquipedale (en.wikipedia.org)
- Angraecum sesquipedale (Christmas star orchid) (kew.org)
- Darwin’s orchid (Angraecum sesquipedale) (arkive.org)
- Xanthopan morgani (en.wikipedia.org)
- Moth tongues, orchids and Darwin – the predictive power of evolution (theguardian.com)
- Hawk-moth scale analysis and pollination specialization in the epilithic Malagasy endemic Aerangis ellisii (Reichenb. fil.) Schltr. (Orchidaceae) (onlinelibrary.wiley.com) Nilsson, L. A. and Rabakonandrianina, E. (1988). Hawk-moth scale analysis and pollination specialization in the epilithic Malagasy endemic Aerangis ellisii (Reichenb. fil.) Schltr. (Orchidaceae). Botanical Journal of the Linnean Society, 97: 49–61. doi:10.1111/j.1095-8339.1988.tb01686.x
- Exact tracking of pollen transfer and mating in plants (nature.com) Nilsson, L. A., Rabakonandrianina, E. and Pettersson, B. (1992). Exact tracking of pollen transfer and mating in plants. Nature 360, 666-668 (17 December 1992); doi:10.1038/360666a0
- The Scents and Smells of Orchids (queenslandorchid.wordpress.com)
- Evolving Digital Ecological Networks (journals.plos.org)
- The Genetic Basis of Pollinator Adaptation in a Sexually Deceptive Orchid (journals.plos.org)
- Trends in the pollination ecology of the Orchidaceae: evolution and systematics (researchgate.net) Raymond Louis Tremblay (1992). Trends in the pollination ecology of the Orchidaceae: evolution and systematics. Canadian Journal of Botany, 70(3): 642-650. https://doi.org/10.1139/b92-083
- Generalization in Pollination Systems, and Why it Matters (jstor.org) Nikolas M. Waser, Lars Chittka, Mary V. Price, Neal M. Williams and Jeff Ollerton (1996). Generalization in Pollination Systems, and Why it Matters. Ecology, 77(4), 1043-1060. doi:1. Retrieved from http://www.jstor.org/stable/2265575 doi:1. Also available from eebweb.arizona.edu
- Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification (academic.oup.com) Tremblay RL, Ackerman JD, Zimmerman JK, Calvo RN. (2005). Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biological Journal of the Linnean Society, 84, 1–54. Also available from researchgate.net
- Dispelling the myth that orchid species usually only have a single pollinator (jeffollerton.wordpress.com)
- The Pollination Ecology of an Assemblage of Grassland Asclepiads in South Africa (aob.oxfordjournals.org) Jeff Ollerton, Steven D. Johnson, Louise Cranmer and Sam Kellie (2003). The Pollination Ecology of an Assemblage of Grassland Asclepiads in South Africa. Ann Bot 92 (6): 807-834. doi: 10.1093/aob/mcg206
- Hot Spots, Cold Spots, and the Geographic Mosaic Theory of Coevolution. (ncbi.nlm.nih.gov) Gomulkiewicz R, Thompson JN, Holt RD, Nuismer SL, Hochberg ME (2003). Hot Spots, Cold Spots, and the Geographic Mosaic Theory of Coevolution. Ann Bot 92 (6): 807-834. doi: 10.1093/aob/mcg206
- Coevolution: Plant–Insect (els.net)
- Coevolution of angiosperms and insects (palaeo.gly.bris.ac.uk)
- Coevolution of Insects and (Flowering) Plants (biol.wwu.edu)
- Coevolution (sonoma.edu)
- Coevolution (evolution.berkeley.edu)
- Biodiversity and Plant-Animal Coevolution (press.princeton.edu)
- BIOL 2007 – COEVOLUTION (ucl.ac.uk)
- Natural Selection, Coevolution, and the Web of Life (jstor.org) Thompson, J. (2014). Natural Selection, Coevolution, and the Web of Life. The American Naturalist, 183(1), Iv-V. doi:1. Retrieved from http://www.jstor.org/stable/10.1086/674238 doi:1
- Evolution for the Community Ecologist (jstor.org) Callaway, R. (2006). Evolution for the Community Ecologist. BioScience, 56(3), 266-267. doi:1. Retrieved from http://www.jstor.org/stable/10.1641/0006-3568(2006)056[0266:eftce]2.0.co;2 doi:1
- Imperfect Batesian Mimicry and the Conspicuousness Costs of Mimetic Resemblance (jstor.org) Speed, M., Ruxton, G., Associate Editor: Franz J. Weissing, & Editor: Donald L. DeAngelis (2010). Imperfect Batesian Mimicry and the Conspicuousness Costs of Mimetic Resemblance. The American Naturalist, 176(1), E1-E14. doi:1. Retrieved from http://www.jstor.org/stable/10.1086/652990 doi:1
- Optimal Control and Cold War Dynamics between Plant and Herbivore (jstor.org) Low, C., Ellner, S., Holden, M., Associate Editor: William F. Morris, & Editor: Judith L. Bronstein (2013). Optimal Control and Cold War Dynamics between Plant and Herbivore. The American Naturalist, 182(2), E25-E39. doi:1. Retrieved from http://www.jstor.org/stable/10.1086/670810 doi:1
- Biotic Interactions, Rapid Evolution, and the Establishment of Introduced Species (jstor.org) Jones, E., Gomulkiewicz, R., Associate Editor: Diane S. Srivastava, & Editor: Mark A. McPeek (2012). Biotic Interactions, Rapid Evolution, and the Establishment of Introduced Species. The American Naturalist, 179(2), E28-E36. doi:1. Retrieved from http://www.jstor.org/stable/10.1086/663678 doi:1
- Source Populations Act as Coevolutionary Pacemakers in Experimental Selection Mosaics Containing Hotspots and Coldspots (jstor.org) Vogwill, T., Fenton, A., Buckling, A., Hochberg, M., Brockhurst, M., Associate Editor: Craig W. Benkman, & Editor: Michael C. Whitlock (2009). Source Populations Act as Coevolutionary Pacemakers in Experimental Selection Mosaics Containing Hotspots and Coldspots. The American Naturalist, 173(5), E171-E176. doi:1. Retrieved from http://www.jstor.org/stable/10.1086/597374 doi:1
- Multidimensional (Co)Evolutionary Stability (jstor.org) Débarre, F., Nuismer, S., Doebeli, M., Associate Editor: Maria R. Servedio, & Editor: Troy Day (2014). Multidimensional (Co)Evolutionary Stability. The American Naturalist, 184(2), 158-171. doi:1. Retrieved from http://www.jstor.org/stable/10.1086/677137 doi:1
- Comparative Dating of Attine Ant and Lepiotaceous Cultivar Phylogenies Reveals Coevolutionary Synchrony and Discord (jstor.org) Mikheyev, A., Mueller, U., Abbot, P., Associate Editor: Jukka Jokela, & Editor: Ruth G. Shaw (2010). Comparative Dating of Attine Ant and Lepiotaceous Cultivar Phylogenies Reveals Coevolutionary Synchrony and Discord. The American Naturalist, 175(6), E126-E133. doi:1. Retrieved from http://www.jstor.org/stable/10.1086/652472 doi:1
- Inverse-Gene-for-Gene Infection Genetics and Coevolutionary Dynamics (jstor.org) Fenton, A., Antonovics, J., Brockhurst, M., Associate Editor: Greg Dwyer, & Editor: Mark A. McPeek (2009). Inverse-Gene-for-Gene Infection Genetics and Coevolutionary Dynamics. The American Naturalist, 174(6), E230-E242. doi:1. Retrieved from http://www.jstor.org/stable/10.1086/645087 doi:1
- Herbivory and Defensive Characteristics of Tree Species in a Lowland Tropical Forest (jstor.org) Coley, P. (1983). Herbivory and Defensive Characteristics of Tree Species in a Lowland Tropical Forest. Ecological Monographs, 53(2), 209-229. doi:1. Retrieved from http://www.jstor.org/stable/1942495 doi:1
- Orchid Sexual Deceit Provokes Ejaculation (jstor.org) Gaskett, A., Winnick, C., Herberstein, M., & Natural History Editor: Henry M. Wilbur (2008). Orchid Sexual Deceit Provokes Ejaculation. The American Naturalist, 171(6), E206-E212. doi:1. Retrieved from http://www.jstor.org/stable/10.1086/587532 doi:1
- Pollination and evolution of the genus Mystacidium (Orchidaceae) (researchspace.ukzn.ac.za)
- Mystacidium capense: A Dainty Orchid from South Africa (queenslandorchid.wordpress.com)
- Prosthechea cochleata: An Upside-Down, Dangly and Charming Orchid (queenslandorchid.wordpress.com)
- The Living, Breathing World of Borneo’s Carnivorous Pitcher Plants (proof.nationalgeographic.com)
- Cool Bugs #9 – Acacia ants (bioblog.biotunes.org)
- Beetle-Pollination ─ Cantharophlly ─ in Amorpbopballus bobenackeri (Araceae) (aroid.org)
- Jonathan Drori: The beautiful tricks of flowers (ted.com)
- Co-evolution with dinosaurs? (palaeo.gly.bris.ac.uk)
- Tough Questions (dailypost.wordpress.com)
- The Poetry of List-Making (dailypost.wordpress.com)
- Mixing Media (dailypost.wordpress.com)
- Symbiosis (dailypost.wordpress.com)