Rethinking the Synthesis Period in Evolutionary Studies

I propose we abandon the unit concept of “the evolutionary synthesis”. There was much more to evolutionary studies in the 1920s and 1930s than is suggested in our commonplace narratives of this object in history. Instead, four organising threads capture much of evolutionary studies at this time. First, the nature of species and the process of speciation were dominating, unifying subjects. Second, research into these subjects developed along four main lines, or problem complexes: variation, divergence, isolation, and selection. Some calls for ‹synthesis’ focused on these problem complexes (sometimes on one of these; other times, all). In these calls, comprehensive and pluralist compendia of plausibly relevant elements were preferred over reaching consensus about the value of particular formulae. Third, increasing confidence in the study of common problems coincided with methodological and epistemic changes associated with experimental taxonomy. Finally, the surge of interest in species problems and speciation in the 1930s is intimately tied to larger trends, especially a shifting balance in the life sciences towards process-based biologies and away from object-based naturalist disciplines. Advocates of synthesis in evolution supported, and were adapting to, these larger trends.     

The temporal dimension of marine speciation

Speciation is a process that occurs over time and, as such, can only be fully understood in an explicitly temporal context. Here we discuss three major consequences of speciation’s extended duration. First, the dynamism of environmental change indicates that nascent species may experience repeated changes in population size, genetic diversity, and geographic distribution during their evolution. The present characteristics of species therefore represents a static snapshot of a single time point in a species’ highly dynamic history, and impedes inferences about the strength of selection or the geography of speciation. Second, the process of speciation is open ended—ecological divergence may evolve in the space of a few generations while the fixation of genetic differences and traits that limit outcrossing may require thousands to millions of years to occur. As a result, speciation is only fully recognized long after it occurs, and short-lived species are difficult to discern. Third, the extinction of species or of clades provides a simple, under-appreciated, mechanism for the genetic, biogeographic, and behavioral ‘gaps’ between extant species. Extinction also leads to the systematic underestimation of the frequency of speciation and the overestimation of the duration of species formation. Hence, it is no surprise that a full understanding of speciation has been difficult to achieve. The modern synthesis—which united genetics, development, ecology, biogeography, and paleontology—greatly advanced the study of evolution. Here we argue that a similarly synthetic approach must be taken to further our understanding of the origin of species.     

Darwin’s contributions to genetics

Darwin’s contributions to evolutionary biology are well known, but his contributions to genetics are much less known. His main contribution was the collection of a tremendous amount of genetic data, and an attempt to provide a theoretical framework for its interpretation. Darwin clearly described almost all genetic phenomena of fundamental importance, such as prepotency (Mendelian inheritance), bud variation (mutation), heterosis, reversion (atavism), graft hybridization (Michurinian inheritance), sex-limited inheritance, the direct action of the male element on the female (xenia and telegony), the effect of use and disuse, the inheritance of acquired characters (Lamarckian inheritance), and many other observations pertaining to variation, heredity and development. To explain all these observations, Darwin formulated a developmental theory of heredity — Pangenesis — which not only greatly influenced many subsequent theories, but also is supported by recent evidence.     

Early 20th-century research at the interfaces of genetics, development, and evolution: reflections on progress and dead ends

Three early 20th-century attempts at unifying separate areas of biology, in particular development, genetics, physiology, and evolution, are compared in regard to their success and fruitfulness for further research: Jacques Loeb's reductionist project of unifying approaches by physico-chemical explanations; Richard Goldschmidt's anti-reductionist attempts to unify by integration; and Sewall Wright's combination of reductionist research and vision of hierarchical genetic systems. Loeb's program, demanding that all aspects of biology, including evolution, be studied by the methods of the experimental sciences, proved highly successful and indispensible for higher level investigations, even though evolutionary change and properties of biological systems up to now cannot be fully explained on the molecular level alone. Goldschmidt has been appraised as pioneer of physiological and developmental genetics and of a new evolutionary synthesis which transcended neo-Darwinism. However, this study concludes that his anti-reductionist attempts to integrate genetics, development and evolution have to be regarded as failures or dead ends. His grand speculations were based on the one hand on concepts and experimental systems that were too vague in order to stimulate further research, and on the other on experiments which in their core parts turned out not to be reproducible. In contrast, Sewall Wright, apart from being one of the architects of the neo-Darwinian synthesis of the 1930s, opened up new paths of testable quantitative developmental genetic investigations. He placed his research within a framework of logical reasoning, which resulted in the farsighted speculation that examinations of biological systems should be related to the regulation of hierarchical genetic subsystems, possibly providing a mechanism for development and evolution. I argue that his suggestion of basing the study of systems on clearly defined properties of the components has proved superior to Goldschmidt's approach of studying systems as a whole, and that attempts to integrate different fields at a too early stage may prove futile or worse.     

Three reciprocally monophyletic mtDNA lineages elucidate the taxonomic status of Grant’s gazelles

The intraspecific phylogeography of Grant’s gazelles Nanger granti was assessed with mitochondrial DNA control region sequences. Samples of 177 individuals from 17 Kenyan and Tanzanian populations were analysed. Three highly divergent, reciprocally monophyletic lineages were found, with among group net nucleotide distances of 8–12%. The three lineages—notata, granti and petersii—grouped populations according to their geographic origin, encompassing populations in the north, southwest, and east, respectively. The mtDNA lineages reflected distinct evolutionary trajectories, and the data are discussed in reference to the four currently recognised subspecies. We suggest Grant’s gazelles be raised to the superspecies Nanger (granti) comprising three taxonomic units corresponding to the three mtDNA lineages. There was no evidence of gene flow between the notata and granti lineages, despite their geographic proximity, suggesting reproductive isolation. These constitute evolutionary significant units within the adaptive evolutionary framework. Due to its restricted geographic distribution and genetic and morphological distinctiveness, we suggest the petersii lineage be raised to the species Nanger (granti) petersii within the Grant’s gazelles superspecies.     

Post-Haeckelian comparative biology — Adolf Naef’s idealistic morphology

Summary The present study describes the conceptual framework of Adolf Naef’s idealistic morphology as presented at the onset of the 20^th century. According to Naef, Haeckel’s and Gegenbaur’s approaches towards a phylogenetic biology were insufficient. He made it clear that Haeckel’s ideas were based on typological morphology. Thus, Haeckel’s views on comparative biology pointed back to pre-Darwinian concepts. Naef’s consequence was not to work out his own evolutionary morphology but to systematize the earlier typological concept. Consequently, he separated comparative morphology from phylogenetic studies. This idea was adopted by Hennig and was even imported into modern cladism.     

The molecular basis of speciation: from patterns to processes,rules to mechanisms

The empirical study of speciation has brought us closer to unlocking the origins of life’s vast diversity. By examining recently formed species, a number of general patterns, or rules, become apparent. Among fixed differences between species, sexual genes and traits are one of the most rapidly evolving and novel functional classes, and premating isolation often develops earlier than postmating isolation. Among interspecific hybrids, sterility evolves faster than inviability, the X-chromosome has a greater effect on incompatibilities than autosomes, and hybrid dysfunction affects the heterogametic sex more frequently than the homogametic sex (Haldane’s rule). Haldane’s rule, in particular, has played a major role in reviving interest in the genetics of speciation. However, the large genetic and reproductive differences between taxa and the multi-factorial nature of each rule have made it difficult to ascribe general mechanisms. Here, we review the extensive progress made since Darwin on understanding the origin of species. We revisit the rules of speciation, regarding them as landmarks as species evolve through time. We contrast these ‘rules’ of speciation to ‘mechanisms’ of speciation representing primary causal factors ranging across various levels of organization—from genic to chromosomal to organismal. To explain the rules, we propose a new ‘hierarchical faster-sex’ theory: the rapid evolution of sex and reproduction-related (SRR) genes (faster-SRR evolution), in combination with the preferential involvement of the X-chromosome (hemizygous X-effects) and sexually selected male traits (faster-male evolution). This unified theory explains a comprehensive set of speciation rules at both the prezyotic and postzygotic levels and also serves as a cohesive alternative to dominance, composite, and recent genomic conflict interpretations of Haldane’s rule.     

Genes versus phenotypes in the study of speciation

Despite persistent debate on the nature of species, the widespread adoption of Mayr’s biological species concept has led to a heavy emphasis on the importance of reproductive isolation to the speciation process. Equating the origin of species with the evolution of reproductive isolation has become common practice in the study of speciation, coincident with an increasing focus on elucidating the specific genetic changes (i.e.—speciation genes) underlying intrinsic reproductive barriers between species. In contrast, some have recognized that reproductive isolation is usually a signature effect rather than a primary cause of speciation. Here we describe a research paradigm that shifts emphasis from effects to causes in order to resolve this apparent contradiction and galvanize the study of speciation. We identify major elements necessary for a balanced and comprehensive investigation of the origin of species and place the study of so-called “speciation genes” into its appropriate context. We emphasize the importance of characterizing diverging phenotypes, identifying relevant evolutionary forces acting on those phenotypes and their role in the causal origins of reduced gene flow between incipient species, and the nature of the genetic and phenotypic boundaries that results from such processes. This approach has the potential to unify the field of speciation research, by allowing us to make better “historical” predictions about the fate of diverging populations regardless of taxon.     

On the dependence of speciation rates on species abundance and characteristic population size

The question of the potential importance for speciation of large/small population sizes remains open. We compare speciation rates in twelve major taxonomic groups that differ by twenty orders of magnitude in characteristic species abundance (global population number). It is observed that the twenty orders of magnitude’s difference in species abundances scales to less than two orders of magnitude’s difference in speciation rates. As far as species abundance largely determines the rate of generation of intraspecific endogenous genetic variation, the result obtained suggests that the latter rate is not a limiting factor for speciation. Furthermore, the observed approximate constancy of speciation rates in different taxa cannot be accounted for by assuming a neutral or nearly neutral molecular clock in subdivided populations. Neutral fixation is only relevant in sufficiently small populations with 4N _ev < 1, which appears an unrealistic condition for many taxa of the smaller organisms. Further research is clearly needed to reveal the mechanisms that could equate the evolutionary pace in taxa with dramatically different population sizes     

Practice and Politics in Japanese Science: Hitoshi Kihara and the Formation of a Genetics Discipline

This paper examines the history of Japanese genetics in the 1920s to 1950s as seen through the work of Hitoshi Kihara, a prominent wheat geneticist as well as a leader in the development of the discipline in Japan. As Kihara’s career illustrates, Japanese genetics developed quickly in the early twentieth century through interactions with biologists outside Japan. The interactions, however, ceased due to the war in the late 1930s, and Japanese geneticists were mostly isolated from outside information until the late 1940s. During the isolation in wartime and under the postwar U.S. Occupation, Kihara adapted to political changes. During wartime, he developed a research institute focusing on applied biology of various crops, which conformed to the national need to address food scarcity. After the war, he led the campaign for the establishment of a national institute of genetics and negotiated with American Occupation officers. The Americans viewed this Japanese effort with suspicion because of the rising popularity of the controversial theory of the Russian agronomist, Trofim Lysenko, in Japan. The institute was approved in 1949 partly because Kihara was able to bridge the gap between the American and Japanese sides. With Kihara’s flexible and generous leadership, Japanese genetics steadily developed, survived the wartime, and recovered quickly in the postwar period. The article discusses Kihara’s interest in cytoplasmic inheritance and his synthetic approach to genetics in this political context, and draws attention to the relation between Kihara’s genetics and agricultural practice in Japan.     

Method as a Function of “Disciplinary Landscape”: C.D. Darlington and Cytology, Genetics and Evolution, 1932–1950

This article considers the reception of British cytogeneticist C.D. Darlington’s controversial 1932 book, Recent Advances in Cytology. Darlington’s cytogenetic work, and the manner in which he made it relevant to evolutionary biology, marked an abrupt shift in the status and role of cytology in the life sciences. By focusing on Darlington’s scientific method – a stark departure from anti-theoretical, empirical reasoning to a theoretical and speculative approach based on deduction from genetic first principles – the article characterises the relationships defining the “disciplinary landscape” of the life sciences of the time, namely those between cytology, genetics, and evolutionary theory.     

为什么在物种概念上难以达成共识?

生物学家通常认为物种是生命多样性的基本单位。然而, 尽管近一个世纪以来生物学家们不断地讨论物种概念问题, 但到目前为止仍然难以形成共识。大多数生物学家关注如何定义物种主要是因为它有非常重要的实践意义, 所以, 不同学者提出的物种概念在很大程度上是基于实践应用上的可操作性, 并且其视角难免受其专业见地以及对形成新物种的进化过程的认识所影响。物种代表了进化过程的一个阶段, 而且不同的“物种”可能处于物种形成这个进化过程的不同阶段。鉴于“定义”实际上是一种类似协议的约定或界定, 任何定义都是一种带有局限性的概括, 因此我们可能很难建立一个与分类实践中千变万化的情况都能完全匹配协调的物种定义。已经提出来的那些物种概念或定义都有其合理性, 但是也没有一个是完美无缺的。认识到这一点很重要, 否则就可能会因为固执地坚持某一特定的物种概念而在物种界定和进化研究中自觉或不自觉地引入错误甚至制造混乱。     

Toward Conceptual Cohesiveness: a Historical Analysis of the Theory and Utility of Ecological Boundaries and Transition Zones

Ecological transition zones are increasingly recognized as systems that play a critical role in controlling or modifying flows of organisms, materials, and energy across landscapes. Many concepts describing transitional areas have been proposed over the years, such as the prevalent and durable ecotone concept. Confusion among ecologists and land managers about transition zone concepts and the isolation of studies that use only one transition concept can hinder unified progress in understanding these key systems. Currently, a movement toward conceptual synthesis under the umbrella concept of ‘ecological boundary’ is underway. Here we examine the history and theoretical baggage of the ecotone, riparian zone, and several other concepts. Subsequently, we present a conceptual cluster analysis, which facilitates a better understanding of the similarities and differences between boundary and transition concepts. We emphasize the hierarchical nature of these concepts: higher-level synthetic concepts can be used in the development of theory, whereas lower-level concepts allow more specificity and the formulation of operational definitions. Finally, we look briefly at the utility and future use of boundary and transition zone concepts.     

Instinct in the '50s: the British reception of Konrad Lorenz's theory of instinctive behavior<Superscript>*</Superscript>

At the beginning of the 1950s most students of animal behavior in Britain saw the instinct concept developed by Konrad Lorenz in the 1930s as the central theoretical construct of the new ethology. In the mid 1950s J.B.S. Haldane made substantial efforts to undermine Lorenz's status as the founder of the new discipline, challenging his priority on key ethological concepts. Haldane was also critical of Lorenz's sharp distinction between instinctive and learnt behavior. This was inconsistent with Haldane's account of the evolution of language, and, according to Haldane, inconsistent with elementary genetics. British attitudes to the instinct concept changed dramatically in the wake of Daniel S. Lehraman's 1953 critique of Lorenz, and by the 1960s Lorenz drew a clear distinction between his own views and those of the English-speaking ethologists. The inconsistencies between Lorenz's ideas and the trends in contemporary evolutionary genetics that are reflected in Haldane's critiques may help to explain why the Lorenzian instinct concept was unable to maintain itself in Britian.     

The Nature of Evolutionary Radiations: A Case Study Involving Devonian Trilobites

Evolutionary radiations, times of profound diversification of species against a broader background of more muted evolutionary change, have long been considered one of the fundamental patterns in the fossil record. Further, given the important role geological, environmental, and climatic processes play in causing speciation, analyzing the biogeographic context of radiations can yield important insight into their evolutionary mechanisms. In this study we examine biogeographic patterns and quantify rates of speciation in a diverse group of Devonian trilobites, the calmoniids, that has been hailed as a classic paleontological example of an evolutionary radiation. In particular, a phylogenetic biogeographic analysis—modified Brooks Parsimony Analysis—was used to examine the processes and geographic setting of speciation within the group. Results indicate that the Malvinokaffric Realm was a geographically complex area, and this geographic complexity created various opportunities for speciation via geodispersal and vicariance that created the fuel that fed the speciation in these taxa. Part of the geographic complexity was created not only by the inherent geologic backdrop of the region, but the overlying changes of sea level rise and fall. Rates of speciation were highest when sea level was lowest. Low sea level encouraged isolation of faunas in different tectonic basins. By contrast, sea level rise facilitated range expansion and geodispersal to other distinct tectonic basins, and speciation rates concomitantly fell; however, the taxa with the expanded ranges were later fodder for diversification when sea level fell again. Here we present a view of evolutionary radiations driven fundamentally by external abiotic factors—geology and climate—that cause range expansion and opportunities for geographic isolation with resultant rapid speciation.     

Multivariate morphometrics,quantitative genetics,and neutral theory: Developing a “modern synthesis” for primate evolutionary morphology

Anthropologists are increasingly turning to explicit model‐bound evolutionary approaches for understanding the morphological diversification of humans and other primate lineages. Such evolutionary morphological analyses rely on three interconnected conceptual frameworks; multivariate morphometrics for quantifying similarity and differences among taxa, quantitative genetics for modeling the inheritance and evolution of morphology, and neutral theory for assessing the likelihood that taxon diversification is due to stochastic processes such as genetic drift. Importantly, neutral theory provides a framework for testing more parsimonious explanations for observed morphological differences before considering more complex adaptive scenarios. However, the consistency with which these concepts are applied varies considerably, which mirrors some of the theoretical obstacles faced during the “modern synthesis” of classical population genetics in the early 20th century. Here, each framework is reviewed and some potential stumbling blocks to the full conceptual integration of multivariate morphometrics, quantitative genetics, and neutral theory are considered.     

Psychoontogeny and psychophylogeny: Bernhard Rensch’s (1900–1990) selectionist turn through the prism of panpsychistic identism

Toward the end of the 1930s, Bernhard Rensch (1900–1990) turned from Lamarckism and orthogenesis to selectionism and became one of the key figures in the making of the Synthetic Theory of Evolution (STE). He contributed to the Darwinization of biological systematics, the criticism of various anti-Darwinian movements in the German lands, but more importantly founded a macroevolutionary theory based on Darwinian gradualism. In the course of time, Rensch’s version of the STE developed into an all-embracing metaphysical conception based on a kind of Spinozism. Here we approach Rensch’s “selectionist turn” by outlining its context, and by analyzing his theoretical transformation. We try to reconstruct the immanent logic of Rensch’s evolution from a “Lamarckian Synthesis” to a “Darwinian Synthesis”. We will pay close attention to his pre-Darwinian works, because this period has not been treated in detail in English before. We demonstrate an astonishing continuity in topics, methodology, and empirical generalizations despite the shift in Rensch’s views on evolutionary mechanisms. We argue that the continuity in Rensch’s theoretical system can be explained, at last in part, by the guiding role of general methodological principles which underlie the entire system, explicitly or implicitly. Specifically, we argue that Rensch’s philosophy became an asylum for the concept of orthogenesis which Rensch banned from evolutionary theory. Unable to explain the directionality of evolution in terms of empirically based science, he “pre-programmed” the occurrence of human-level intelligence by a sophisticated philosophy combined with a supposedly naturalistic evolutionary biology.

Freud’s Lamarckism’ and the Politics of Racial Science

This article re-contextualizes Sigmund Freud’s interest in the idea of the inheritance of acquired characteristics in terms of the socio-political connotations of Lamarckism and Darwinism in the 1930s and 1950s. Many scholars have speculated as to why Freud continued to insist on a supposedly outmoded theory of evolution in the 1930s even as he was aware that it was no longer tenable. While Freud’s initial interest in the inheritance of phylogenetic memory was not necessarily politically motivated, his refusal to abandon this theory in the 1930s must be understood in terms of wider debates, especially regarding the position of the Jewish people in Germany and Austria. Freud became uneasy about the inheritance of memory not because it was scientifically disproven, but because it had become politically charged and suspiciously regarded by the Nazis as Bolshevik and Jewish. Where Freud seemed to use the idea of inherited memory as a way of universalizing his theory beyond the individual cultural milieu of his mostly Jewish patients, such a notion of universal science itself became politically charged and identified as particularly Jewish. The vexed and speculative interpretations of Freud’s Lamarckism are situated as part of a larger post-War cultural reaction against Communism on the one hand (particularly in the 1950s when Lamarckism was associated with the failures of Lysenko), and on the other hand, against any scientific concepts of race in the wake of World War II.     

The expanded evolutionary synthesis—a response to Godfrey-Smith,Haig, and West-Eberhard

In responding to three reviews of Evolution in Four Dimensions (Jablonka and Lamb, 2005, MIT Press), we briefly consider the historical background to the present genecentred view of evolution, especially the way in which Weismann’s theories have influenced it, and discuss the origins of the notion of epigenetic inheritance. We reaffirm our belief that all types of hereditary information—genetic, epigenetic, behavioural and cultural—have contributed to evolutionary change, and outline recent evidence, mainly from epigenetic studies, that suggests that non-DNA heritable variations are not rare and can be quite stable. We describe ways in which such variations may have influenced evolution. The approach we take leads to broader definitions of terms such as ‘units of heredity’, ‘units of evolution’, and ‘units of selection’, and we maintain that ‘information’ can be a useful concept if it is defined in terms of its effects on the receiver. Although we agree that evolutionary theory is not undergoing a Kuhnian revolution, the incorporation of new data and ideas about hereditary variation, and about the role of development in generating it, is leading to a version of Darwinism that is very different from the gene-centred one that dominated evolutionary thinking in the second half of the twentieth century.     

Scientific Discrimination and the Activist Scientist: L.C. Dunn and the Professionalization of Genetics and Human Genetics in the United States

During the 1920s and 1930s geneticist L.C. Dunn of Columbia University cautioned Americans against endorsing eugenic policies and called attention to eugenicists’ less than rigorous practices. Then, from the mid-1940s to early 1950s he attacked scientific racism and Nazi Rassenhygiene by co-authoring Heredity, Race and Society with Theodosius Dobzhansky and collaborating with members of UNESCO (United Nations Educational, Scientific, and Cultural Organization) on their international campaign against racism. Even though shaking the foundations of scientific discrimination was Dunn’s primary concern during the interwar and post-World War II years, his campaigns had ancillary consequences for the discipline. He contributed to the professionalization of genetics during the 1920s and 1930s and sought respectability for human genetics in the 1940s and 1950s. My article aims to elucidate the activist scientist’s role in undermining scientific discrimination by exploring aspects of Dunn’s scientific work and political activism from the 1920s to 1950s. Definitions are provided for scientific discrimination and activist scientist.