Defining and Refining Selfish Genes

This chapter navigates through the rather confusing vocabulary surrounding the gene’s-eye view. It explains how the gene’s-eye view defines the word gene in an unusual way, differently from molecular biologists, and how this leads to the central claim that evolution requires two entities, replicators and vehicles. The chapter evaluates the success of the replicator–vehicle distinction compared to other general accounts, such as Lewontin’s principles, and how the debate has changed in light of the growing interests in major transitions. Finally, the chapter outlines the application of the gene’s-eye view to cultural evolution—the concept of memetics—and why it has failed to have the same influence there as it has on the study of organic evolution.

Life and Death of Selfish Genes: Comparative Genomics Reveals the Dynamic Evolution of Cytoplasmic Incompatibility

Cytoplasmic incompatibility is a selfish reproductive manipulation induced by the endosymbiont Wolbachia in arthropods. In males Wolbachia modifies sperm, leading to embryonic mortality in crosses with Wolbachia-free females. In females, Wolbachia rescues the cross and allows development to proceed normally. This provides a reproductive advantage to infected females, allowing the maternally transmitted symbiont to spread rapidly through host populations. We identified homologs of the genes underlying this phenotype, cifA and cifB, in 52 of 71 new and published Wolbachia genome sequences. They are strongly associated with cytoplasmic incompatibility. There are up to seven copies of the genes in each genome, and phylogenetic analysis shows that Wolbachia frequently acquires new copies due to pervasive horizontal transfer between strains. In many cases, the genes have subsequently acquired loss-of-function mutations to become pseudogenes. As predicted by theory, this tends to occur first in cifB, whose sole function is to modify sperm, and then in cifA, which is required to rescue the cross in females. Although cif genes recombine, recombination is largely restricted to closely related homologs. This is predicted under a model of coevolution between sperm modification and embryonic rescue, where recombination between distantly related pairs of genes would create a self-incompatible strain. Together, these patterns of gene gain, loss, and recombination support evolutionary models of cytoplasmic incompatibility.

‘Bacterial Programmed Cell Death’: cellular altruism or genetic selfism?

ABSTRACT Cell-dependent propagation of the ‘self’ is the driver of all species, organisms and even genes. Conceivably, elimination of these entities is caused by cellular death. Then, how can genes that cause the death of the same cell evolve? Programmed cell death (PCD) is the gene-dependent self-inflicted death. In multicellular organisms, PCD of a cell confers fitness to the surviving rest of the organism, which thereby allows the selection of genes responsible for PCD. However, PCD in free-living bacteria is intriguing; the death of the cell is the death of the organism. How can such PCD genes be selected in unicellular organisms? The bacterial PCD in a population is proposed to confer fitness to the surviving kin in the form of sporulation, nutrition, infection-containment and matrix materials. While the cell-centred view leading to propositions of ‘altruism’ is enticing, the gene-centred view of ‘selfism’ is neglected. In this opinion piece, we reconceptualize the PCD propositions as genetic selfism (death due to loss/mutation of selfish genes) rather than cellular altruism (death for the conferment of fitness to kin). Within the scope and the available evidence, we opine that some of the PCD-like observations in bacteria seem to be the manifestation of genetic selfism by Restriction–Modification systems and Toxin–Antitoxin systems.

An introgressed gene causes meiotic drive in Neurospora sitophila

Meiotic drive elements cause their own preferential transmission following meiosis. In fungi this phenomenon takes the shape of spore killing, and in the filamentous ascomycete Neurospora sitophila, the Sk-1 spore killer element is found in many natural populations. In this study, we identify the gene responsible for spore killing in Sk-1 by generating both long and short-read genomic data and by using these data to perform a genome wide association test. Through molecular dissection, we show that a single 405 nucleotide long open reading frame generates a product that both acts as a poison capable of killing sibling spores and as an antidote that rescues spores that produce it. By phylogenetic analysis, we demonstrate that the gene is likely to have been introgressed from the closely related species N. hispaniola, and we identify three subclades of N. sitophila, one where Sk-1 is fixed, another where Sk-1 is absent, and a third where both killer and sensitive strain are found. Finally, we show that spore killing can be suppressed through an RNA interference based genome defense pathway known as meiotic silencing by unpaired DNA. Spk-1 is not related to other known meiotic drive genes, and similar sequences are only found within Neurospora. These results shed new light on the diversity of genes capable of causing meiotic drive, their origin and evolution and their interaction with the host genome.Significance StatementIn order to survive, most organisms have to deal with parasites. Such parasites can be other organisms, or sometimes, selfish genes found within the host genome itself. While much is known about parasitic organisms, the interaction with their hosts and their ability to spread within and between species, much less is known about selfish genes. We here identify a novel selfish “spore killer” gene in the fungus Neurospora sitophila. The gene appears to have evolved within the genus, but has entered the species through hybridization and introgression. We also show that the host can counteract the gene through RNA interference. These results shed new light on the diversity of selfish genes in terms of origin, evolution and host interactions.