Hybrid Sterility, Genetic Conflict and Complex Speciation: Lessons From the Drosophila simulans Clade Species

The three fruitfly species of the Drosophila simulans clade— D. simulans, D. mauritiana, and D. sechellia— have served as important models in speciation genetics for over 40 years. These species are reproductively isolated by geography, ecology, sexual signals, postmating-prezygotic interactions, and postzygotic genetic incompatibilities. All pairwise crosses between these species conform to Haldane’s rule, producing fertile F1 hybrid females and sterile F1 hybrid males. The close phylogenetic proximity of the D. simulans clade species to the model organism, D. melanogaster, has empowered genetic analyses of their species differences, including reproductive incompatibilities. But perhaps no phenotype has been subject to more continuous and intensive genetic scrutiny than hybrid male sterility. Here we review the history, progress, and current state of our understanding of hybrid male sterility among the D. simulans clade species. Our aim is to integrate the available information from experimental and population genetics analyses bearing on the causes and consequences of hybrid male sterility. We highlight numerous conclusions that have emerged as well as issues that remain unresolved. We focus on the special role of sex chromosomes, the fine-scale genetic architecture of hybrid male sterility, and the history of gene flow between species. The biggest surprises to emerge from this work are that (i) genetic conflicts may be an important general force in the evolution of hybrid incompatibility, (ii) hybrid male sterility is polygenic with contributions of complex epistasis, and (iii) speciation, even among these geographically allopatric taxa, has involved the interplay of gene flow, negative selection, and positive selection. These three conclusions are marked departures from the classical views of speciation that emerged from the modern evolutionary synthesis.

Interpreting the History of Evolutionary Biology through a Kuhnian Prism: Sense or Nonsense?

Traditionally, Thomas S. Kuhn’s The Structure of Scientific Revolutions (1962) is largely identified with his analysis of the structure of scientific revolutions. Here, we contribute to a minority tradition in the Kuhn literature by interpreting the history of evolutionary biology through the prism of the entire historical developmental model of sciences that he elaborates in The Structure. This research not only reveals a certain match between this model and the history of evolutionary biology but, more importantly, also sheds new light on several episodes in that history, and particularly on the publication of Charles Darwin’s On the Origin of Species (1859), the construction of the modern evolutionary synthesis, the chronic discontent with it, and the latest expression of that discontent, called the extended evolutionary synthesis. Lastly, we also explain why this kind of analysis hasn’t been done before.

Extending the Explanatory Scope of Evolutionary Theory: The Origin of Historical Kinds in Biology and Culture

Since its inception, evolutionary theory has experienced a number of extensions. The most important of these took the forms of the Modern Evolutionary Synthesis (MES), embracing genetics and population biology in the early 20th century, and the Extended Evolutionary Synthesis (EES) of the last thirty years, embracing, among other factors, non-genetic forms of inheritance. While we appreciate the motivation for this recent extension, we argue that it does not go far enough, since it restricts itself to widening explanations of adaptation by adding mechanisms of inheritance and variation. Here we argue that a more thoroughgoing extension is needed, one that broadens the explanatory scope of evolutionary theory. In addition to adaptation and its various mechanisms, evolutionary theory must recognize as a distinct intellectual challenge the origin of what we call “historical kinds.” Under historical kinds we include any process that acquires a quasi-independent and traceable lineage-history in biological and cultural evolution. A limited number of historical kinds have been recognized in evolutionary biology, and corresponding research programs have been formed around them. The best characterized examples are biological species and genes. We propose that the conceptual category of historical kinds can and needs to be extended, and we develop the notion of a historical kind in a series of paradigmatic exemplars, from genes and cell types to rituals and music. The explanation of the origin of historical kinds should be a main objective of biological and cultural sciences.

Biology and panpsychism: German evolutionists and a philosopher Theodor Ziehen (1862–1950)

Theodor Ziehen was a prominent German psychiatrist and psychologist and a marginal philosopher of the first half of the 20th century who developed an exotic subjective-idealistic theory based on quasi-empirical psychological arguments. Although Ziehen was seen by contemporaries (most prominently by Vladimir Lenin) as a representative of the same philosophical current (empirio-criticism) as Mach and Avenarius, he never achieved their prominence in the history of philosophy. At the same time, Ziehen’s philosophy became influential in German biology, first of all, due to his direct and very strong impact on Bernhard Rensch. Rensch, in his turn, was the most significant figure on the international scene of what is known as the Modern Evolutionary Synthesis in biology. Rensch was not the only biologist influenced by Ziehen’s ideas. Ziehen had some communication with the “German Darwin” Ernst Haeckel and played a prominent role in the concept of the founder of biological systematics Willi Hennig. How to explain Ziehen’s prominent place in the history of evolutionary biology, despite his obscurity in the history of philosophy? Our hypothesis is that Ziehen became a visible figure in evolutionary theory because of the monistic bias in German biology. Ziehen’s epistemology appeared to be compatible with evolutionary monism and was developed by a practicing psychiatrist therefore obtaining a character of a quasi-experimental doctrine.

Extending the Explanatory Scope of Evolutionary Theory: The Origin of Historical Kinds in Biology and Culture

Since its inception, evolutionary theory has experienced a number of extensions. The most important of these took the forms of the Modern Evolutionary Synthesis (MES), embracing genetics and population biology in the early 20th century, and the Extended Evolutionary Synthesis (EES) of the last thirty years, embracing, among other factors, non-genetic forms of inheritance. While we appreciate the motivation for this recent extension, we argue that it does not go far enough, since it restricts itself to widening explanations of adaptation by adding mechanisms of inheritance and variation. A more thoroughgoing extension is needed, one that widens the explanatory scope of evolutionary theory. In addition to adaptation and its various mechanisms, evolutionary theory must recognize as a distinct intellectual challenge the origin of what we call “historical kinds.” Under historical kinds we include any process that acquires a quasi-independent and traceable lineage-history in biological and cultural evolution. We develop the notion of a historical kind in a series of paradigmatic exemplars, from genes and homologues to rituals and music, and we propose a preliminary characterization.

Applications of Supercomputers in Population Genetics

Population genetics is the study of the frequency and interaction of alleles and genes in population and how this allele frequency distribution changes over time as a result of evolutionary processes such as natural selection, genetic drift, and mutation. This field has become essential in the foundation of modern evolutionary synthesis. Traditionally regarded as a highly mathematical discipline, its modern approach comprises more than the theoretical, lab, and fieldwork. Supercomputers play a critical role in the success of this field and are discussed in this chapter.

Missing compared to what? Revisiting heritability, genes and culture

Standard models for the determination of phenotypes from genes are grounded in simple assumptions that are inherent in the modern evolutionary synthesis (MES), which was developed in the 1930s, 1940s and 1950s. The MES was framed in the context of Mendelian genetic transmission enhanced by the Fisherian view of the way discretely inherited genes determine continuously quantitative phenotypes. The statistical models that are used to estimate and interpret genetic contributions to human phenotypes—including behavioural traits—are constructed within the framework of the MES. Variance analysis constitutes the main tool and is used under this framework to characterize genetic inheritance, and hence determination of phenotypes. In this essay, we show that cultural inheritance, when incorporated into models for the determination of phenotypes, can sharply reduce estimates of the genetic contribution to these phenotypes. Recognition of the importance of non-genetic transmission of many human traits is becoming ever more necessary to prevent regression to the debates of the 1970s and 1980s concerning policies based on genetic determination of complex human phenotypes. This article is part of the theme issue ‘Bridging cultural gaps: interdisciplinary studies in human cultural evolution’.