The Hamiltonian view of social evolution

Hamilton’s Rule, named after the evolutionary biologist Bill Hamilton, and the related concepts of inclusive fitness and kin selection, have been the bedrock of the study of social evolution for the past half century. In ’The Philosophy of Social Evolution’ (Oxford University Press, 2017), Jonathan Birch provides a comprehensive introduction to the conceptual foundations of the Hamiltonian view of social evolution, and a passionate defence of its enduring value in face of the recent high profile criticism. In this review essay, I first outline the version of Hamilton’s Rule defended by Birch, dubbed Hamilton’s Rule General, and its derivation. With this in place, I then navigate through the fierce disagreements that Hamilton’s Rule generates among social evolution researchers and evaluate Birch’s central argument of the book that HRG serves as an organizing framework for social evolution research under which we can compare and interpret more detailed causal models. I then spend the remainder of the review discussing what I take to be three of the most exciting implications of Hamilton’s thinking raised by Birch: (1) the extension of Hamilton’s Rule to mobile genetic elements, (2) maximization of inclusive fitness models and the idea of adaptation as organism design, and (3) the relationship between Hamilton’s approaches to social behaviour and the gene’s-eye view of evolution

The Hamiltonian view of social evolution

Hamilton’s Rule, named after the evolutionary biologist Bill Hamilton, and the related concepts of inclusive fitness and kin selection, have been the bedrock of the study of social evolution for the past half century. In ’The Philosophy of Social Evolution’ (Oxford University Press, 2017), Jonathan Birch provides a comprehensive introduction to the conceptual foundations of the Hamiltonian view of social evolution, and a passionate defence of its enduring value in face of the recent high profile criticism. In this review essay, I first outline the version of Hamilton’s Rule defended by Birch, dubbed Hamilton’s Rule General, and its derivation. With this in place, I then navigate through the fierce disagreements that Hamilton’s Rule generates among social evolution researchers and evaluate Birch’s central argument of the book that HRG serves as an organizing framework for social evolution research under which we can compare and interpret more detailed causal models. I then spend the remainder of the review discussing what I take to be three of the most exciting implications of Hamilton’s thinking raised by Birch: (1) the extension of Hamilton’s Rule to mobile genetic elements, (2) maximization of inclusive fitness models and the idea of adaptation as organism design, and (3) the relationship between Hamilton’s approaches to social behaviour and the gene’s-eye view of evolution

Genes and organisms in the legacy of the modern synthesis

The gene's-eye view of evolution is an influential but contentious perspective on biology. It emerged in the aftermath of the Modern Synthesis and both proponents and detractors have stressed the link between the two. In particular, both the Modern Synthesis and the gene's-eye view have been criticized for overemphasizing the role genes at the expense of organisms in evolutionary explanations. In this chapter, I discuss the connection between the Modern Synthesis and the gene’s-eye view and evaluate the status of genes and organisms in contemporary biology. I show that while the gene’s-eye view traces its origin back to the Modern Synthesis, it can most accurately be said to represent a specific – adaptationist and gene-centric – version of it. To assess the role of genes and organisms, I examine the intimate relationship between the gene’s-eye view and another post-Synthesis development, the concept of inclusive fitness. I argue that the popularity and influence of inclusive fitness theory demonstrate that the individual organism remains safe at the heart of modern evolutionary biology

Enforcement is central to the evolution of cooperation.

Cooperation occurs at all levels of life, from genomes, complex cells and multicellular organisms to societies and mutualisms between species. A major question for evolutionary biology is what these diverse systems have in common. Here, we review the full breadth of cooperative systems and find that they frequently rely on enforcement mechanisms that suppress selfish behaviour. We discuss many examples, including the suppression of transposable elements, uniparental inheritance of mitochondria and plastids, anti-cancer mechanisms, reciprocation and punishment in humans and other vertebrates, policing in eusocial insects and partner choice in mutualisms between species. To address a lack of accompanying theory, we develop a series of evolutionary models that show that the enforcement of cooperation is widely predicted. We argue that enforcement is an underappreciated, and often critical, ingredient for cooperation across all scales of biological organization

Exogenous selection shapes germination behaviour and seedling traits of populations at different altitudes in a Senecio hybrid zone

Background and Aims The Senecio hybrid zone on Mt Etna, Sicily, is characterized by steep altitudinal clines in quantitative traits and genetic variation. Such clines are thought to be maintained by a combination of ‘endogenous' selection arising from genetic incompatibilities and environment-dependent ‘exogenous' selection leading to local adaptation. Here, the hypothesis was tested that local adaptation to the altitudinal temperature gradient contributes to maintaining divergence between the parental species, S. chrysanthemifolius and S. aethnensis. Methods Intra- and inter-population crosses were performed between five populations from across the hybrid zone and the germination and early seedling growth of the progeny were assessed. Key Results Seedlings from higher-altitude populations germinated better under low temperatures (9-13 °C) than those from lower altitude populations. Seedlings from higher-altitude populations had lower survival rates under warm conditions (25/15 °C) than those from lower altitude populations, but also attained greater biomass. There was no altitudinal variation in growth or survival under cold conditions (15/5 °C). Population-level plasticity increased with altitude. Germination, growth and survival of natural hybrids and experimentally generated F1s generally exceeded the worse-performing parent. Conclusions Limited evidence was found for endogenous selection against hybrids but relatively clear evidence was found for divergence in seed and seedling traits, which is probably adaptive. The combination of low-temperature germination and faster growth in warm conditions might enable high-altitude S. aethnensis to maximize its growth during a shorter growing season, while the slower growth of S. chrysanthemifolius may be an adaptation to drought stress at low altitudes. This study indicates that temperature gradients are likely to be an important environmental factor generating and maintaining adaptive divergence across the Senecio hybrid zone on Mt Etn

When and why are mitochondria paternally inherited?

In contrast with nuclear genes that are passed on through both parents, mitochondrial genes are maternally inherited in most species, most of the time. The genetic conflict stemming from this transmission asymmetry is well-documented, and there is an abundance of population-genetic theory associated with it. While occasional or aberrant paternal inheritance occurs, there are only a few cases where exclusive paternal inheritance of mitochondrial genomes is the evolved state. Why this is remains poorly understood. By examining commonalities between species with exclusive paternal inheritance, we discuss what they may tell us about the evolutionary forces influencing mitochondrial inheritance patterns. We end by discussing recent technological advances that make exploring the causes and consequences of paternal inheritance feasible

Selfish genetic elements.

Selfish genetic elements (historically also referred to as selfish genes, ultra-selfish genes, selfish DNA, parasitic DNA, genomic outlaws) are genetic segments that can enhance their own transmission at the expense of other genes in the genome, even if this has no or a negative effect on organismal fitness. [1-6] Genomes have traditionally been viewed as cohesive units, with genes acting together to improve the fitness of the organism. However, when genes have some control over their own transmission, the rules can change, and so just like all social groups, genomes are vulnerable to selfish behaviour by their parts. Early observations of selfish genetic elements were made almost a century ago, but the topic did not get widespread attention until several decades later. Inspired by the gene-centred views of evolution popularized by George Williams[7] and Richard Dawkins,[8] two papers were published back-to-back in Nature in 1980-by Leslie Orgel and Francis Crick[9] and Ford Doolittle and Carmen Sapienza[10] respectively-introducing the concept of selfish genetic elements (at the time called "selfish DNA") to the wider scientific community. Both papers emphasized that genes can spread in a population regardless of their effect on organismal fitness as long as they have a transmission advantage. Selfish genetic elements have now been described in most groups of organisms, and they demonstrate a remarkable diversity in the ways by which they promote their own transmission.[11] Though long dismissed as genetic curiosities, with little relevance for evolution, they are now recognized to affect a wide swath of biological processes, ranging from genome size and architecture to speciation.[12]

Genetic conflicts and the case for licensed anthropomorphizing

The use of intentional language in biology is controversial. It has been commonly applied by researchers in behavioral ecology, who have not shied away from employing agential thinking or even anthropomorphisms, but has been rarer among researchers from more mechanistic corners of the discipline, such as population genetics. One research area where these traditions come into contact-and occasionally clash-is the study of genetic conflicts, and its history offers a good window to the debate over the use of intentional language in biology. We review this debate, paying particular attention to how this interaction has played out in work on genomic imprinting and sex chromosomes. In light of this, we advocate for a synthesis of the two approaches, a form of licensed anthropomorphizing. Here, agential thinking's creative potential and its ability to identify the fulcrum of evolutionary pressure are combined with the rigidity of formal mathematical modeling

Supplementary Table 1

Information about samples used for Illumina sequecning and flow cytometry