Selfish genetic element
Selfish genetic elements are genetic segments that can enhance their own transmission at the expense of other genes in the genome, even if this has no positive or a net negative effect on organismal fitness. Genomes have traditionally been viewed as cohesive units, with genes acting together to improve the fitness of the organism.
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 and Richard Dawkins, two papers were published back-to-back in Nature in 1980 – by Leslie Orgel and Francis Crick and by Ford Doolittle and Carmen Sapienza – introducing the concept of selfish genetic elements 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. 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.
History
Early observations
Observations of what is now referred to as selfish genetic elements go back to the early days in the history of genetics. Already in 1928, Russian geneticist Sergey Gershenson reported the discovery of a driving X chromosome in Drosophila obscura. Crucially, he noted that the resulting female-biased sex ratio may drive a population extinct. The earliest clear statement of how chromosomes may spread in a population not because of their positive fitness effects on the individual organism, but because of their own "parasitic" nature came from the Swedish botanist and cytogeneticist Gunnar Östergren in 1945. Discussing B chromosomes in plants he wrote:In many cases these chromosomes have no useful function at all to the species carrying them, but that they often lead an exclusively parasitic existence... need not be useful for the plants. They need only be useful to themselves.
Around the same time, several other examples of selfish genetic elements were reported. For example, the American maize geneticist Marcus Rhoades described how chromosomal knobs led to female meiotic drive in maize. Similarly, this was also when it was first suggested that an intragenomic conflict between uniparentally inherited mitochondrial genes and biparentally inherited nuclear genes could lead to cytoplasmic male sterility in plants. Then, in the early 1950s, Barbara McClintock published a series of papers describing the existence of transposable elements, which are now recognized to be among the most successful selfish genetic elements. The discovery of transposable elements led to her being awarded the Nobel Prize in Medicine or Physiology in 1983.
Conceptual developments
The empirical study of selfish genetic elements benefited greatly from the emergence of the so-called gene-centred view of evolution in the nineteen sixties and seventies. In contrast with Darwin's original formulation of the theory of evolution by natural selection that focused on individual organisms, the gene's-eye view takes the gene to be the central unit of selection in evolution. It conceives evolution by natural selection as a process involving two separate entities: replicators and vehicles.Since organisms are temporary occurrences, present in one generation and gone in the next, genes are the only entity faithfully transmitted from parent to offspring. Viewing evolution as a struggle between competing replicators made it easier to recognize that not all genes in an organism would share the same evolutionary fate.
The gene's-eye view was a synthesis of the population genetic models of the modern synthesis, in particular the work of RA Fisher, and the social evolution models of W. D. Hamilton. The view was popularized by George Williams's Adaptation and Natural Selection and Richard Dawkins's best seller The Selfish Gene. Dawkins summarized a key benefit from the gene's-eye view as follows:
"If we allow ourselves the license of talking about genes as if they had conscious aims, always reassuring ourselves that we could translate our sloppy language back into respectable terms if we wanted to, we can ask the question, what is a single selfish gene trying to do?" — Richard Dawkins, The Selfish Gene
In 1980, two high-profile papers published back-to-back in Nature by Leslie Orgel and Francis Crick, and by Ford Doolittle and Carmen Sapienza, brought the study of selfish genetic elements to the centre of biological debate. The papers took their starting point in the contemporary debate of the so-called C-value paradox, the lack of correlation between genome size and perceived complexity of a species. Both papers attempted to counter the prevailing view of the time that the presence of differential amounts of non-coding DNA and transposable elements is best explained from the perspective of individual fitness, described as the "phenotypic paradigm" by Doolittle and Sapienza. Instead, the authors argued that much of the genetic material in eukaryotic genomes persists, not because of its phenotypic effects, but can be understood from a gene's-eye view, without invoking individual-level explanations. The two papers led to a series of exchanges in Nature.
Current views
If the selfish DNA papers marked the beginning of the serious study of selfish genetic elements, the subsequent decades have seen an explosion in theoretical advances and empirical discoveries. Leda Cosmides and John Tooby wrote a landmark review about the conflict between maternally inherited cytoplasmic genes and biparentally inherited nuclear genes. The paper also provided a comprehensive introduction to the logic of genomic conflicts, foreshadowing many themes that would later be subject of much research. Then in 1988 John H. Werren and colleagues wrote the first major empirical review of the topic. This paper achieved three things. First, it coined the term selfish genetic element, putting an end to a sometimes confusingly diverse terminology. Second, it formally defined the concept of selfish genetic elements. Finally, it was the first paper to bring together all different kinds of selfish genetic elements known at the time.In the late 1980s, most molecular biologists considered selfish genetic elements to be the exception, and that genomes were best thought of as highly integrated networks with a coherent effect on organismal fitness. In 2006, when Austin Burt and Robert Trivers published the first book-length treatment of the topic, the tide was changing. While their role in evolution long remained controversial, in a review published a century after their first discovery, William R. Rice concluded that "nothing in genetics makes sense except in the light of genomic conflicts".
Logic
Though selfish genetic elements show a remarkable diversity in the way they promote their own transmission, some generalizations about their biology can be made. In a classic 2001 review, Gregory D.D. Hurst and John H. Werren proposed two 'rules' of selfish genetic elements.Rule 1: Spread requires sex and outbreeding
Sexual reproduction involves the mixing of genes from two individuals. According to Mendel's Law of Segregation, alleles in a sexually reproducing organism have a 50% chance of being passed from parent to offspring. Meiosis is therefore sometimes referred to as "fair".Highly self-fertilizing or asexual genomes are expected to experience less conflict between selfish genetic elements and the rest of the host genome than outcrossing sexual genomes. There are several reasons for this. First, sex and outcrossing put selfish genetic elements into new genetic lineages. In contrast, in a highly selfing or asexual lineage, any selfish genetic element is essentially stuck in that lineage, which should increase variation in fitness among individuals. The increased variation should result in stronger purifying selection in selfers/asexuals, as a lineage without the selfish genetic elements should out-compete a lineage with the selfish genetic element. Second, the increased homozygosity in selfers removes the opportunity for competition among homologous alleles. Third, theoretical work has shown that the greater linkage disequilibrium in selfing compared to outcrossing genomes may in some, albeit rather limited, cases cause selection for reduced transposition rates. Overall, this reasoning leads to the prediction that asexuals/selfers should experience a lower load of selfish genetic elements. One caveat to this is that the evolution of selfing is associated with a reduction in the effective population size. A reduction in the effective population size should reduce the efficacy of selection and therefore leads to the opposite prediction: higher accumulation of selfish genetic elements in selfers relative to outcrossers.
Empirical evidence for the importance of sex and outcrossing comes from a variety of selfish genetic elements, including transposable elements, self-promoting plasmids, and B chromosomes.