Playing Darwin. Part A. Experimental Evolution in Drosophila

In 2009 we celebrate Charles Darwin’s second centenary, and 150 years since the publication of ‘The Origin of Species’. After so many years, what has changed in the way we understand Evolution? Obviously we have now a full understanding of the mechanisms underlying heritability. Many molecular tools are available, allowing among other things to reconstruct more accurately the evolutionary history of species and use a comparative approach to infer evolutionary processes. But we can also study evolution in action. Such studies—Experimental Evolution—help us to characterize in detail the evolutionary processes and patterns as a function of environmental challenges, the previous history and present state of populations, and the interactions between such factors. We have now a wide variety of organisms that have been studied with this approach, exploring a diversity of potentialities, in biological characteristics and genetic tools, and covering a variety of evolutionary questions. In this short article I will illustrate the potentialities of Experimental Evolution, focusing in three studies in Drosophila. These and other studies of Experimental Evolution illustrate that Evolution is often local, involving complex patterns and processes, which lead both to specific adaptations and to biological diversity, as Darwin already stated clearly in ‘The Origin of Species’.     

The individuality of the species: A Darwinian theory? — from Buffon to Ghiselin, and back to Darwin

Since the 1970s, there has been a tremendous amount of literature on Ghiselin's proposal that “species are individuals”. After recalling the origins and stakes of this thesis in contemporary evolutionary theory, I show that it can also be found in the writings of the French naturalist Buffon in the 18th Century. Although Buffon did not have the conception that one species could be derived from another, there is an interesting similarity between the modern argument and that of Buffon regarding the “individuality of species’. The analogy is strong enough to force us to recognize that genuine evolutionary (or Darwinian) questions might be of secondary importance in the discussion. In consequence, the third section of the paper proposes an alternative schema for the “logical structure” of the Darwinian concept of species. Darwin distinguished the problem of the designation of a concrete species, and the problem of its signification of species within his theory of descent? The resulting notion of species involves a logical structure based on the fusion of the logical operations of classification and ordering. The difficulty — and interest — is that this interpretation of species does not entail any precise operational definition of species; it can only tell us what the ultimate signification of classification is within the theory of descent with modification through natural selection.     

Four Darwinian themes on the origin,evolution and preservation of island life

Charles Darwin’s observations and insights continue to inspire nearly all scientists who are captivated by both the marvels and the perils of island life. Here I feature four themes inspired by Darwin’s singular insights: themes that may continue to provide valuable lessons for understanding the ecological and evolutionary development of insular biotas, and for conserving the natural character and evolutionary potential of all species restricted to isolated ecosystems (natural or anthropogenic).     

Mystery of mysteries: Darwin and the species problem

Darwin offered an intriguing answer to the species problem. He doubted the existence of the species category as a real category in nature, but he did not doubt the existence of those taxa called “species”. And despite his scepticism of the species category, Darwin continued using the word “species”. Many have said that Darwin did not understand the nature of species. Yet his answer to the species problem is both theoretically sound and practical. On the theoretical side, Darwin’s answer is confirmed by contemporary biology, and it offers a more satisfactory answer to the species problem than recent attempts to save the species category. On the practical side, Darwin’s answer frees us from the search for the correct theoretical definition of “species”. But at the same time it does not require that we banish the word “species” from biology as some recent sceptics of the species category advocate. © The Willi Hennig Society 2010.     

Social life: the paradox of multiple-queen colonies

The evolution of animal societies in which some individuals forego their own reproductive opportunities to help others to reproduce poses an evolutionary paradox that can be traced to Darwin. Altruism may evolve through kin selection when the donor and recipient of altruistic acts are related to each other, as generally is the case in social birds and mammals. Similarly, social insect workers are highly related to the brood they rear when colonies are headed by a single queen. However, recent studies have shown that insect colonies frequently contain several queens, with the effect of decreasing relatedness among colony members. How can one account for the origin and maintenance of such colonies? This evolutionary enigma presents many of the same theoretical challenges as does the evolution of cooperative breeding and eusociality.     

Reconsidering Darwin’s “Several Powers”

Contemporary textbooks often define evolution in terms of the replication, mutation, and selective retention of DNA sequences, ignoring the contribution of the physical processes involved. In the closing line of The Origin of Species, however, Darwin recognized that natural selection depends on prior more basic living functions, which he merely described as life’s “several powers.” For Darwin these involved the organism’s capacity to maintain itself and to reproduce offspring that preserve its critical functional organization. In modern terms we have come to recognize that this involves the continual generation of complex organic molecules in complex configurations accomplished with the aid of persistent far-from-equilibrium chemical self-organizing and self-assembling processes. But reliable persistence and replication of these processes also requires constantly available constraints and boundary conditions. Organism autonomy further requires that these constraints and co-dependent dynamics are reciprocally produced, each by the other. In this paper I argue that the different constraint-amplifying dynamics of two or more self-organizing processes can be coupled so that they reciprocally generate each other’s critical supportive boundary conditions. This coupling is a higher-order constraint (which can be distributed among components or offloaded onto molecular structures) that effectively constitutes a sign vehicle “interpreted” by the synergistic dynamics of these co-dependent self-organizing process so that they reconstitute this same semiotic-dynamic relationship and its self-reconstituting potential in new substrates. This dynamical co-dependence constitutes Darwin’s “several powers” and is the basis of the biosemiosis that enables evolution.     

The evolution of cooperative breeding through group augmentation

Some individuals (helpers) in cooperatively breeding species provide alloparental care and often suppress their own reproduction. Kin selection is clearly an important explanation for such behaviour, but a possible alternative is group augmentation where individuals survive or reproduce better in large groups and where it therefore pays to recruit new members to the group. The evolutionary stability of group augmentation is currently disputed. We model evolutionarily stable helping strategies by following the dynamics of social groups with varying degrees of subordinate help. We also distinguish between passive augmentation, where a group member benefits from the mere presence of others, and active augmentation, where their presence as such is neutral or harmful, but where helping to recruit new group members may still be beneficial if they in turn actively provide help for the current reproductives ('delayed reciprocity'). The results show that group augmentation (either passive or active) can be evolutionarily stable and explain costly helping by non-reproductive subordinates, either alone or leading to elevated help levels when acting in concert with kin selection. Group augmentation can thus potentially explain the weak relationships between relatedness and helping behaviour that are observed in some cooperatively breeding species. In some cases, the superior mutualistic performance of cooperatively behaving groups can generate an incentive to stay and help which is strong enough to make ecological constraints unnecessary for explaining the stability of cooperatively breeding groups.     

Zum konzept der »inneren« selektion: Stellungnahme zu einer evolutionstheoretischen kontroverse

Recently the concept of natural selection in Darwin’s sense has been criticized by some authors. It has been argued that this concept does not explain certain phenomena of evolutionary change, especially in the reach of macroevolution. Some biologists, therefore, demanded for evolution a new model of selection which focuses internal factors in phytogeny. — This paper is a brief discussion of some aspects of “internal” selection and its meaning in contemporary evolutionary biology. The argument of the paper is that evolution can only be explained by a theory taking cognizance of interactions between external and internal selective agencies. Such a theory would be a systems theory of evolution.     

Darwin Day in deep time: promoting evolutionary science through paleontology

Charles Darwin’s birthday, February 12th, is an international celebration coined Darwin Day. During the week of his birthday, universities, museums, and science-oriented organizations worldwide host events that celebrate Darwin’s scientific achievements in evolutionary biology. The University of Tennessee, Knoxville (UT) has one of the longest running celebrations in the nation, with 2016 marking the 19th year. For 2016, the theme for our weeklong series of events was paleontology, chosen to celebrate new research in the field and to highlight the specific misconceptions of evolution within the context of geologic time. We provide insight into the workings of one of our largest and most successful Darwin Day celebration to date, so that other institutions might also be able to host their own rewarding Darwin Day events in the future.     

Diversity Over Time

Temporal turnover is a fundamental feature of ecological communities. Darwin 1859 noted the ecological and evolutionary significance of turnover, Fisher and Preston acknowledged its role in their models of species abundance, while this ongoing and entirely natural rearrangement of species underpins key ecological concepts such as MacArthur and Wilson’s theory of island biogeography. However, the current focus on spatial patterns of diversity means that temporal changes are often overlooked. Here I argue that failure to take heed of the time frame over which data are collected can lead to both artefacts and artifictions. There are also deeper issues, such as the consequences for species richness estimation and rarefaction methods of a constantly changing community. Moreover, some of the confusion surrounding species abundance distributions may be resolved by taking account of time. A better appreciation of temporal turnover is essential for accurate diversity measurement and assessment, and, more importantly, will also lead to improved understanding of the processes that underpin community structure.     

Methods of ethics and the descent of man: Darwin and Sidgwick on ethics and evolution

Darwin’s treatment of morality in The Descent of Man has generated a wide variety of responses among moral philosophers. Among these is the dismissal of evolution as irrelevant to ethics by Darwin’s contemporary Henry Sidgwick; the last, and arguably the greatest, of the Nineteenth Century British Utilitarians. This paper offers a re-examination of Sidgwick’s response to evolutionary considerations as irrelevant to ethics and the absence of any engagement with Darwin’s work in Sidgwick’s main ethical treatise, The Methods of Ethics. This assessment of Sidgwick’s response to Darwin’s work is shown to have significance for a number of ongoing controversies in contemporary metaethics.     

Engaging with Lyell: Alfred Russel Wallace’s Sarawak Law and Ternate papers as reactions to Charles Lyell’s Principles of Geology

Alfred Russel Wallace (1823–1913) and Charles Darwin (1809–1882) are honored as the founders of modern evolutionary biology. Accordingly, much attention has focused on their relationship, from their independent development of the principle of natural selection to the receipt by Darwin of Wallace’s essay from Ternate in the spring of 1858, and the subsequent reading of the Wallace and Darwin papers at the Linnean Society on 1 July 1858. In the events of 1858 Wallace and Darwin are typically seen as central players, with Darwin’s friends Charles Lyell (1797–1875) and Joseph Dalton Hooker (1817–1911) playing supporting roles. This narrative has resulted in an under-appreciation of a more central role for Charles Lyell as both Wallace’s inspiration and foil. The extensive anti-transmutation arguments in Lyell’s landmark Principles of Geology were taken as the definitive statement on the subject. Wallace, in his quest to solve the mystery of species origins, engaged with Lyell’s arguments in his private field notebooks in a way that is concordant with his engagement with Lyell in the 1855 and 1858 papers. I show that Lyell was the object of Wallace’s Sarawak Law and Ternate papers through a consideration of the circumstances that led Wallace to send his Ternate paper to Darwin, together with an analysis of the material that Wallace drew upon from the Principles. In this view Darwin was, ironically, intended for a supporting role in mediating Wallace’s attempted dialog with Lyell.     

The evolution of extreme altruism and inequality in insect societies

In eusocial organisms, some individuals specialize in reproduction and others in altruistic helping. The evolution of eusociality is, therefore, also the evolution of remarkable inequality. For example, a colony of honeybees (Apis mellifera) may contain 50 000 females all of whom can lay eggs. But 100 per cent of the females and 99.9 per cent of the males are offspring of the queen. How did such extremes evolve? Phylogenetic analyses show that high relatedness was almost certainly necessary for the origin of eusociality. However, even the highest family levels of kinship are insufficient to cause the extreme inequality seen in e.g. honeybees via ‘voluntary altruism’. ‘Enforced altruism’ is needed, i.e. social pressures that deter individuals from attempting to reproduce. Coercion acts at two stages in an individual''s life cycle. Queens are typically larger so larvae can be coerced into developing into workers by being given less food. Workers are coerced into working by ‘policing’, in which workers or the queen eat worker-laid eggs or aggress fertile workers. In some cases, individuals rebel, such as when stingless bee larvae develop into dwarf queens. The incentive to rebel is strong as an individual is the most closely related to its own offspring. However, because individuals gain inclusive fitness by rearing relatives, there is also a strong incentive to ‘acquiesce’ to social coercion. In a queenright honeybee colony, the policing of worker-laid eggs is very effective, which results in most workers working instead of attempting to reproduce. Thus, extreme altruism is due to both kinship and coercion. Altruism is frequently seen as a Darwinian puzzle but was not a puzzle that troubled Darwin. Darwin saw his difficulty in explaining how individuals that did not reproduce could evolve, given that natural selection was based on the accumulation of small heritable changes. The recognition that altruism is an evolutionary puzzle, and the solution was to wait another 100 years for William Hamilton.     

Species are individuals—the German tradition

The German tradition of considering species, and higher taxonomic entities, as individuals begins with the temporalization of natural history, thus pre‐dating Darwin’s ‘Origin’ of 1859. In the tradition of German Naturphilosophie as developed by Friedrich Schelling, species came to be seen as parts of a complex whole that encompasses all (living) nature. Species were comprehended as dynamic entities that earn individuality by virtue of their irreversible passage through time. Species individuality was conceived in terms of species taxa forming a spatiotemporally located relational system (complex whole), a conception of species that was easily assimilated to an evolutionary world view. However, the dynamics of an evolutionary process driven by variation and natural selection created a tension between continuity in nature as opposed to the discreteness and relative stasis of species. As a consequence, some authors such as Ernst Haeckel and Karl August Möbius denied the reality of species, while others explicitly linked the reality and individuality of species to their temporal duration. The mature conception of species as individuals, as formulated by Ludwig von Bertalanffy and adopted by Willi Hennig, is one of an historically conditioned, spatiotemporally located, causally integrated, dynamic yet transiently homeostatically stabilized relational system.     

The Impact of Lamarck’s Theory of Evolution Before Darwin’s Theory

This paper analyzes the impact that Lamarckian evolutionary theory had in the scientific community during the period between the advent of Zoological Philosophy and the publication Origin of Species. During these 50 years Lamarck’s model was a well known theory and it was discussed by the scientific community as a hypothesis to explain the changing nature of the fossil record throughout the history of Earth. Lamarck’s transmutation theory established the foundation of an evolutionary model introducing a new way to research in nature. Darwin’s selectionist theory was proposed in 1859 to explain the origin of species within this epistemological process. In this context, Charles Lyell’s Principles of Geology and Auguste Comte’s Cours de Philosophie Positive appear as two major works for the dissemination of Lamarck’s evolutionary ideology after the death of the French naturalist in 1829.     

Charles Darwin,embryology, evolution and skeletal plasticity

Darwin provided us with the theory of evolutionary change through natural selection. Just as important to the science of biology was Darwin’s recognition that all organisms could be classified and were related to one another because they arose from a single common universal ancestor – what we know as the universal tree of life (UtoL). All the features of the skeletal biology of fish therefore can be explained, both in an evolutionary framework (ultimate causation) and in the framework of development, growth and physiology (proximate causation). Neither approach is complete without the other. I will outline the elements of Darwin’s theories on evolution and classification and, as importantly, discuss what was missing from Darwin’s theories. An important class of evidence for evolution used by Darwin came from embryology, both comparative embryology and the existence of vestiges and atavisms. After discussing this evidence I examine some fundamental features of skeletal development and evolution These include: the presence of four skeletal systems in all vertebrates; the existence of two skeletons, one based on cartilage, the other on bone and dentine; the modular nature of skeletal development and evolution; and the plasticity of the skeleton in response to either genetic or environmental changes.     

Second‐order cooperation: Cooperative offspring as a living public good arising from second‐order selection on non‐cooperative individuals

Switching rate between cooperating and non‐cooperating genotypes is a crucial social evolution factor, often neglected by game theory‐inspired theoretical and experimental frameworks. We show that the evolution of alleles increasing the mutation or phenotypic switching rates toward cooperation is in itself a social dilemma. Although cooperative offspring are often unlikely to reproduce, due to high cost of cooperation, they can be seen both as a living public good and a part of the extended parental phenotype. The competition between individuals that generate cooperators and ones that do not is often more relevant than the competition between cooperators and non‐cooperators. The dilemma of second‐order cooperation we describe relates directly to eusociality, but can be also interpreted as a division of labor or a soma‐germline distinction. The results of our simulations shine a new light on what Darwin had already termed a “special difficulty” of evolutionary theory and describe a novel type of cooperation dynamics.     

Towards a postmodern synthesis of evolutionary biology

In 2009, we are celebrating the 200th anniversary of Charles Darwin and the 150th jubilee of his masterpiece, the Origin of Species. Darwin constructed the first coherent and compelling narrative of biological evolution and thus founded evolutionary biology—and modern biology in general, remembering the famous dictum of Dobzhansky. It is, however, counter-productive, and ultimately, a disservice to Darwin’s legacy, to define modern evolutionary biology as neo-Darwinism. The current picture of evolution, informed by results of comparative genomics and systems biology, is by far more complex than that presented in the Origin of Species, so that Darwinian principles, including natural selection, are incorporated into the evolving new synthesis as important but certainly not all-embracing tenets. This expansion of evolutionary biology does not denigrate Darwin in the least but rather emphasizes the fertility of his ideas.     

Darwin's biogeography

The year 2009 marks the 150th anniversary of the publication of Charles Darwin’s Origin of Species. This book was so influential that it is often considered to be the most important scientific work ever written. Many volumes have been published about the Origin and its lasting effects on religion and society, but few have examined its influence on biogeography. However, it was Darwin’s initial interest in comparing the natural history of different regions during the voyage of the Beagle that led him to propose natural selection as an evolutionary force. He had visited the Cape Verde Islands and saw the similarity of their biota to that of Africa, and then noted the South American relationships of the Galapagos fauna and flora. But the island plants and animals were different from their mainland relatives, and, in the Galapagos, each island appeared to have its own endemic forms. It was these biogeographical observations that were critical to Darwin’s formulation of a theory to account for them. His subsequent conclusions on the evolutionary importance of centres of origin and dispersal were generally well accepted for the next 100 years, until the advent of vicarianism, which began in the early 1970s. That vicarianist movement received an impetus from two sources: (1) the works of Leon Croizat, who did not believe that living organisms could disperse overseas by themselves; and (2) the development of plate tectonics and its causation of continental drift. Vicarianists believed that primitive species were originally widespread over the Earth’s surface but were rafted to different parts of the world by continental fractionation and movement. However, continental drift in the Mesozoic could not have involved contemporary species or genera as many vicarianists claimed. The development of phylogeography, beginning in the 1980s, and improved knowledge of the fossil record soon demonstrated that multitudes of living species, and even many genera and families, underwent long‐distance dispersal during the Cenozoic. This resulted in a decline of vicarianism and a vindication of Darwin’s conclusions on centres of origin and dispersal.     

Phylogenetic isolation increases plant success despite increasing susceptibility to generalist herbivores

Aim Theory suggests that introduced species that are phylogenetically distant from their recipient communities should be more successful than closely related introduced species because they can exploit open niches and escape enemies in their new range, i.e. Darwin’s Naturalization Hypothesis. Alternatively, it has also been hypothesized that closely related invaders might be more successful than novel invaders because they are pre‐adapted to conditions in their new range; a paradox coined Darwin’s Naturalization Conundrum. To date, these hypotheses have been tested primarily at the regional scale, not within local plant communities where introduced species colonize, compete and encounter herbivores. Location Global. Methods and Results We used community phylogenetics to analyse data from 49 published experiments to examine the importance of phylogenetic relatedness and generalist herbivory on native and exotic plant success at the community level. Plants that were categorized as ‘invasive’ were indeed less related to the recipient community than ‘non‐pest’ exotic plants. Distantly related exotic plants were also more abundant than closely related species. Phylogenetic relatedness predicted herbivore impact, but in a way that was opposite to predictions, as herbivores had stronger, not lesser, impacts on distantly related plants. Importantly, these same patterns generally held for native plants, as distantly related native plants were more abundant and more susceptible to herbivores than closely related species, ultimately resulting in herbivores suppressing community‐level phylogenetic diversity. Main conclusions Distantly related plants were more locally successful despite experiencing stronger control by generalist herbivores, a finding that was robust across native and exotic species. To our knowledge, this is the first evidence that phylogenetic matching influences the local success of both native and exotic species and that herbivores can influence community phylodiversity. Phylogenetic relatedness explained a relatively small portion of the variance in the data even after taking herbivory into account, however, suggesting that phylogenetic matching works in combination with other factors to influence community assembly.