This article examines the critique of the biological species concept advanced by protozoan geneticist Tracy Sonneborn at the 1955 AAAS symposium on "the species problem," published subsequently in 1957. Although Sonneborn was a strong proponent of a population genetical conception of species, he became critical of the biological species concept for its failure to incorporate asexual and obligatory inbreeding organisms. It is argued that Sonneborn's intimate knowledge of the ciliate protozoan Paramecium aurelia species complex brought him into conflict with a (...) growing pressure in the biological sciences to emphasize universal principles of life. Faced with the need to defend the value of P. aurelia as an investigative tool, Sonneborn argued that the sharp break in nature between sexual and asexual organisms posited by proponents of the biological species concept was not an existential feature of the living world, but rather the misleading consequence of an operational definition of species based only upon sexual organisms. Drawing upon his knowledge of the immense variability of P. aurelia, he proposed instead a continuum of breeding systems from obligatory outbreeding to asexual organisms, and a more broadly unifying definition of species that incorporated asexual as well as sexual organisms. Paradoxically, the push for unification that then characterized the evolutionary synthesis served to debar critical consideration of Sonneborn's more unificatory alternative, and his underlying contention that biological anomaly could serve as an important source of conceptual unification. (shrink)

Marine interstitial environments are teeming with an extraordinary diversity of coexisting microeukaryotic lineages collectively called “meiofauna.” Interstitial habitats are broadly distributed across the planet, and the complex physical features of these environments have persisted, much like they exist today, throughout the history of eukaryotes, if not longer. Although our general understanding of the biological diversity in these environments is relatively poor, compelling examples of developmental heterochrony (e.g., pedomorphosis) and convergent evolution appear to be widespread among meiofauna. Therefore, an improved understanding (...) of meiofaunal biodiversity is expected to provide some of the deepest insights into the following themes in evolutionary biology: (i) the origins of novel body plans, (ii) macroevolutionary patterns of miniaturization, and (iii) the intersection of evolution and community assembly – e.g., “community convergence” involving distantly related lineages that span the tree of eukaryotes. (shrink)

With historical hindsight, it can be little questioned that the view of protozoa as unicellular organisms was important for the development of the discipline of protozoology. In the early years of this century, the assumption of unicellularity provided a sound justification for the study of protists: it linked them to the metazoa and supported the claim that the study of these “simple” unicellular organisms could shed light on the organization of the metazoan cell. This prospect was significant, given the state (...) of cytology circa 1910. In the wake of the major gains made in understanding nuclear division in the last two decades of the nineteenth century, cytology was suddenly confronted with many, seemingly less penetrable, problems. Several aspects of nuclear organization still remained unexplained, and recent research had revealed the presence in the cytoplasm of structures whose functions in cell life were unknown. Classical methods of cytology, relying on descriptive, morphological analysis, seemed ill equipped to resolve these questions.Hertwig's program for protozoology, grounded in the assumption of the fundamental unity of organization in protozoa and metazoa, offered a potential means for investigating these and other problems of cell theory. Linked to mainstream cytology, protozoology was advocated as a means of experimentally investigating key biolobical processes — reproduction, metabolism, and organelle morphology and physiology — less accessible in higher organisms. Protozoa were hailed as prime experimental organisms, in which cell structure and function could be more easily studied. Unlike the metazoan cell, they could be subjected to controlled experiments in which the external environment was modified and the effects monitored. Protozoa offered, in other words, a promising experimental means by which to investigate the cell — its structures and its processes.The success of this program within Germany was soon apparent. In contrast to the rather neglected state of the discipline in 1900, protozoology began to be recognized as more than a somewhat obscure area of study for specialists. In practical terms, this translated into greater numbers of students attracted to the field, increased institutional support for the discipline, and its elevation in status within the biological sciences as new developments, particularly in connection with medical applications, began to draw attention to the field.64The unicellular hypothesis also promoted the internal development of the science. It provided a rationale for introducing the various techniques used in cytology, embryology, physiology, and the new field of biochemistry as suitable research tools for protozoology as well. This vastly extended the research possibilities and facilitated the understanding of, among other things, protozoan organization, modes of reproduction, and evolutionary relationships. The new experimental grounding of the discipline in turn fitted in well with developments in biology at large: in contrast to the descriptive methodology that had predominated in the nineteenth century, this new experimental program placed protozoology at the forefront of the early twentieth-century movement to make biology an experimental science comparable to physics and chemistry.Yet the criticism of the unicellular hypothesis can also be seen as having served a valuable function within the development of the discipline. It focused attention on the study of protists as organisms in their own right, not simply as models for metazoan cells. More generally, it helped to remind biologists of the particular evolutionary assumptions that supported this conception. Dobell and other British critics pointed out, among other things, the association between the theory of recapitulation and the interpretation of protozoa as unicellular organisms. At the time when the recapitulation theory and the germ-layer doctrine were in decline, it was important to stress how these evolutionary ideas also entered into the contemporary concepts of subsidiary specialties. This was as true for protozoology as it was for cell theory itself. The chromidial theory, in its various guises, and the binuclearity hypothesis did in fact contain elements of recapitulationist reasoning, and they were open to criticism for the same kind of overly speculative theorizing that characterized this evolution theory. Dobell's critique forced protozoologists and cell theorists alike to review the theoretical postulates guiding their investigations.In the absence of further historical studies, it is hard to evaluate the consequences of this debate in later years. The issue was not whether protozoa were the precursors of metazoa — both sides accepted this. They disagreed over which particular protozoon had served as the ancestral form, and this, in turn, influenced their stance on the question of unicellularity. The situation is little changed today. Because the former question is still an open one, the latter remains so too. Both of the models for the origin of multicellular organisms — colonies of ciliates versus multinucleate protists — are still presented as possible mechanisms in modern textbooks of evolution. Unable to judge the dispute in terms of the ultimate validity of the competing conceptions, the historian requires other criteria. It perhaps becomes more important to evaluate the issues in the context of the internal and external stimulus they provided the discipline.65 In these terms, and from the present historical vantage point, Hertwig's research program for protozoology, based upon the unicellular hypothesis, appears to have been a successful one. (shrink)

In the nineteenth century protozoology and early cell biology intersected through the nexus of Darwin's theory of evolution. As single-celled organisms, amoebae offered an attractive focus of study for researchers seeking evolutionary relationships between the cells of humans and other animals, and their primitive appearance made them a favourite model for the ancient ancestor of all living things. Their resemblance to human and other metazoan cells made them popular objects of study among morphologists, physiologists, and even those investigating animal behaviour. (...) The amoeba became the exemplar of the new protoplasmic cell concept of mid-century and because its apparent simplicity made it widely generalizable it became a popular subject in a breadth of experimental investigations and theoretical speculations. It was able to do this because "the amoeba" denotes not a particular organism, but a general type of behaviour common to the cells of a range of protozoa, simple plants and higher animals. Its status as an exemplary cell also rested upon auxiliary philosophical assumptions about what constitutes a primitive characteristic and the thesis that evolution is a progressive development of order from chaos. (shrink)

The eukaryote cell is one of the most radical innovations in the history of life, and the circumstances of its emergence are still deeply contested. This paper will outline the recent history of attempts to reveal these origins, with special attention to the argumentative strategies used to support claims about the first eukaryote cell. I will focus on two general models of eukaryogenesis: the phagotrophy model and the syntrophy model. As their labels indicate, they are based on claims about metabolic (...) relationships. The first foregrounds the ability to consume other organisms; the second the ability to enter into symbiotic metabolic arrangements. More importantly, however, the first model argues for the autogenous or self-generated origins of the eukaryote cell, and the second for its exogenous or externally generated origins. Framing cell evolution this way leads each model to assert different priorities in regard to cell-biological versus molecular evidence, cellular versus environmental influences, plausibility versus evolutionary probability, and irreducibility versus the continuity of cell types. My examination of these issues will conclude with broader reflections on the implications of eukaryogenesis studies for a philosophical understanding of scientific contestation. (shrink)

The fitness of any evolutionary unit can be understood in terms of its two basic components: fecundity (reproduction) and viability (survival). Trade-offs between these fitness components drive the evolution of life-history traits in extant multicellular organisms. We argue that these trade-offs gain special significance during the transition from unicellular to multicellular life. In particular, the evolution of germ–soma specialization and the emergence of individuality at the cell group (or organism) level are also consequences of trade-offs between the two basic fitness (...) components, or so we argue using a multilevel selection approach. During the origin of multicellularity, we study how the group trade-offs between viability and fecundity are initially determined by the cell level trade-offs, but as the transition proceeds, the fitness trade-offs at the group level depart from those at the cell level. We predict that these trade-offs begin with concave curvature in single-celled organisms but become increasingly convex as group size increases in multicellular organisms. We argue that the increasingly convex curvature of the trade-off function is driven by the cost of reproduction which increases as group size increases. We consider aspects of the biology of the volvocine green algae – which contain both unicellular and multicellular members – to illustrate the principles and conclusions discussed. (shrink)

The origin of the eukaryotic cell nucleus and the selective forces that drove its evolution remain unknown and are a matter of controversy. Autogenous models state that both the nucleus and endoplasmic reticulum (ER) derived from the invagination of the plasma membrane, but most of them do not advance clear selective forces for this process. Alternative models proposing an endosymbiotic origin of the nucleus fail to provide a pathway fully compatible with our knowledge of cell biology. We propose here an (...) evolutionary scenario that reconciles both an ancestral endosymbiotic origin of the eukaryotic nucleus (endosymbiosis of a methanogenic archaeon within a fermentative myxobacterium) with an autogenous generation of the contemporary nuclear membrane and ER from the bacterial membrane. We specifically state two selective forces that operated sequentially during its evolution: (1) metabolic compartmentation to avoid deleterious co‐existence of anabolic (autotrophic synthesis by the methanogen) and catabolic (fermentation by the myxobacterium) pathways in the cell, and (2) avoidance of aberrant protein synthesis due to intron spreading in the ancient archaeal genome following mitochondrial acquisition and loss of methanogenesis. BioEssays 28: 525–533, 2006. © 2006 Wiley Periodicals, Inc. (shrink)

This chapter develops a subtle model that integrates environmental and internal factors. It describes the phylogenetic distribution of multicellular organisms in general and complex multicellular life in particular, clarifying the important distinction between the two. This chapter shows that the long apparent lag between the appearance of simple multicellularity in eukaryotes and the radiation of groups with complex multicellular organization has an environmental component that can be associated back to the consequences of life with interior and exterior cells. It suggests (...) that the evolutionary transition from unicells to complex multicellular organisms has several steps. (shrink)

We hypothesize that aspects of animal multicellularity originated before the divergence of metazoans from fungi and social amoebae. Polarized epithelial tissues are a defining feature of metazoans and contribute to the diversity of animal body plans. The recent finding of a polarized epithelium in the non‐metazoan social amoeba Dictyostelium discoideum demonstrates that epithelial tissue is not a unique feature of metazoans, and challenges the traditional paradigm that multicellularity evolved independently in social amoebae and metazoans. An alternative view, presented here, is (...) that the common ancestor of social amoebae, fungi, and animals spent a portion of its life cycle in a multicellular state and possessed molecular machinery necessary for forming an epithelial tissue. Some descendants of this ancestor retained multicellularity, while others reverted to unicellularity. This hypothesis makes testable predictions regarding tissue organization in close relatives of metazoans and provides a novel conceptual framework for studies of early animal evolution.Editor's suggested further reading in BioEssays Searching for Eve: Basal metazoans and the evolution of multicellular complexity Abstract. (shrink)

Experimental research is commonly held up as the paradigm of "good" science. Although experiment plays many roles in science, its classical role is testing hypotheses in controlled laboratory settings. Historical science is sometimes held to be inferior on the grounds that its hypothesis cannot be tested by controlled laboratory experiments. Using contemporary examples from diverse scientific disciplines, this paper explores differences in practice between historical and experimental research vis-à-vis the testing of hypotheses. It rejects the claim that historical research is (...) epistemically inferior. For as I argue, scientists engage in two very different patterns of evidential reasoning and, although there is overlap, one pattern predominates in historical research and the other pattern predominates in classical experimental research. I show that these different patterns of reasoning are grounded in an objective and remarkably pervasive time asymmetry of nature. (shrink)

We began our survey at a time when Ehrenberg's functional principles concerning the design of all organisms prevailed in interpreting the taxonomic place and internal structure of Infusoria. Other options existed, such as Dujardin's sarcode theory and Siebold's cellular analogy, but these were not persuasive for reasons both relevant to and in addition to the microscopic observations. By mid-century other considerations, including the continuing search for complex life cycles and manifestations of sex, dictated the microscopist's rendering of infusorians. Müller and (...) his students saw spermatozoa and gonads; Stein envisioned alternating generations and generative nuclei; Balbiani found sexual behavior in the events of conjugation; and all interpreted the nuclei and nucleoli as gonads or gonadal products. Evolutionary theory provided a fourth dimension. Obsessed with phylogenies, particularly when joined with the germ-layer theory of development, Haeckel emphasized a structural interpretation and found a considerably altered cell theory ready to fill the breach.By the mid-1870s advances in cytology secured Siebold's original analogy. Infusorians now became single-celled organisms, the first in a long phylogenetic sequence that led to the “highest” metazoans. The analogy allowed Bütschli to invoke another biological principle, the physiological division of labor, to reinterpret the origin of the bisexual state. The ghost of Ehrenberg's polygastric theory had completely vanished. (shrink)

This paper examines the contents and institutional context of August Weismann's long essay on Amphimixis (1891). Therein he presented detailed discussions of his on-going studies of reduction division and parthenogenesis, but more to the point, he included an elaborate examination of Émile Maupas's two major publications in protozoology. To understand the relevance of this part to the other two, the author briefly reviews highpoints in earlier nineteenth century protozoology and concludes that only in the mid-1870s and 1880s did protozoa add (...) an important dimension to heredity theory. Otto Bütschli and then Maupas provided Weismann with a deeper understanding of how conjugation and fertilization were related but not identical processes. This allowed him to integrate the two into a fuller understanding of evolution by natural selection. (shrink)

This paper describes a pattern of explanation prevalent in the biological sciences that I call a ‘lineage explanation’. The aim of these explanations is to make plausible certain trajectories of change through phenotypic space. They do this by laying out a series of stages, where each stage shows how some mechanism worked, and the differences between each adjacent stage demonstrates how one mechanism, through minor modifications, could be changed into another. These explanations are important, for though it is widely accepted (...) that there is an ‘incremental constraint’ on evolutionary change, in an important class of cases it is difficult to see how to satisfy this constraint. I show that lineage explanations answer important questions about evolutionary change, but do so by demonstrating differences between individuals rather than invoking population processes, such as natural selection.1. Introduction2. Turning a ‘Scale’ into a ‘Plume’3. Lineage Explanations in Biology3.1. The evolution of eyes3.2. The evolution of feathers4. The Two Dimensions of a Lineage Explanation4.1. The production dimension4.2. The continuity dimension4.3. The dual role of the parts5. Constraining the Explanations6. Operational and Generative Lineages7. Explaining Change Without Populations8. Conclusion. (shrink)

This book reviews some of life’s history. It suggests that one crucial feature of John Maynard Smith and Eörs Szathmáry’s The Major Transitions in Evolution is that it has a dynamic approach. In The Major Transitions in Evolution, Maynard Smith and Szathmáry bought a much more dynamic model to debates about the history of life. This book also shows that in the decade and more that has followed, the legacy of Maynard Smith and Szathmáry has been developed in important ways.

Drawing on recent advances in evolutionary biology, prominent scholars return to the question posed in a pathbreaking book: how evolution itself evolved.

Constructive neutral evolution (CNE) suggests that neutral evolution may follow a stepwise path to extravagance. Whether or not CNE is common, the mere possibility raises provocative questions about causation: in classical neo-Darwinian thinking, selection is the sole source of creativity and direction, the only force that can cause trends or build complex features. However, much of contemporary evolutionary genetics departs from the conception of evolution underlying neo-Darwinism, resulting in a widening gap between what formal models allow, and what the prevailing (...) view of the causes of evolution suggests. In particular, a mutationist conception of evolution as a 2-step origin-fixation process has been a source of theoretical innovation for 40 years, appearing not only in the Neutral Theory, but also in recent breakthroughs in modeling adaptation (the "mutational landscape" model), and in practical software for sequence analysis. In this conception, mutation is not a source of raw materials, but an agent that introduces novelty, while selection is not an agent that shapes features, but a stochastic sieve. This view, which now lays claim to important theoretical, experimental, and practical results, demands our attention. CNE provides a way to explore its most significant implications about the role of variation in evolution. REVIEWERS: Alex Kondrashov, Eugene Koonin and Johann Peter Gogarten reviewed this article. (shrink)

Many scientists believe that there is a uniform, interdisciplinary method for the prac- tice of good science. The paradigmatic examples, however, are drawn from classical ex- perimental science. Insofar as historical hypotheses cannot be tested in controlled labo- ratory settings, historical research is sometimes said to be inferior to experimental research. Using examples from diverse historical disciplines, this paper demonstrates that such claims are misguided. First, the reputed superiority of experimental research is based upon accounts of scientific methodology (Baconian inductivism (...) or falsificationism) that are deeply flawed, both logically and as accounts of the actual practices of scientists. Second, although there are fundamental differences in methodology between experimental scien- tists and historical scientists, they are keyed to a pervasive feature of nature, a time asymmetry of causation. As a consequence, the claim that historical science is methodo- logically inferior to experimental science cannot be sustained. (shrink)