Selfish genetic element

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 by Ford Doolittle and Carmen Sapienza[10] – introducing the concept of selfish genetic elements (at the time called "selfish DNA") to the wider scientific community.

[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.

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.

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.

[9][10] 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.

Finally, it was the first paper to bring together all different kinds of selfish genetic elements known at the time (genomic imprinting, for example, was not covered).

[1] 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.

[11] 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".

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.

[34] 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.

Many forms of segregation distortion occur in male gamete formation, where there is differential mortality of spermatids during the process of sperm maturation or spermiogenesis.

The SR system in Drosophila pseudoobscura, for example, is on the X chromosome, and XSR/Y males produce only daughters, whereas females undergo normal meiosis with Mendelian proportions of gametes.

This gives homing endonucleases an allele frequency dynamics rather similar to a segregation distortion system, and generally unless opposed by strong countervailing selection, they are expected to go to fixation in a population.

[69] Why inheritance ended up being maternal, rather than paternal, is also much debated, but one key hypothesis is that the mutation rate is lower in female compared to male gametes.

Mitochondrial genes are typically only transmitted through female gametes, and therefore from their point of view the production of pollen leads to an evolutionary dead end.

[80][81] Furthermore, a 2017 paper showed how a mitochondrial mutation causing Leber's hereditary optic neuropathy, a male-biased eye disease, was brought over by one of the Filles du roi that arrived in Quebec, Canada, in the 17th century and subsequently spread among many descendants.

[82] Another sort of conflict that genomes face is that between the mother and father competing for control of gene expression in the offspring, including the complete silencing of one parental allele.

Due to differences in methylation status of gametes, there is an inherent asymmetry to the maternal and paternal genomes that can be used to drive a differential parent-of-origin expression.

[84] Several molecular mechanisms for genomic imprinting have been described, and all have the aspect that maternally and paternally derived alleles are made to have distinct epigenetic marks, in particular the degree of methylation of cytosines.

In ecologically challenged species, such biased sex ratios imply that the conversion of resources to offspring becomes very inefficient, to the point of risking extinction.

[104] Attempts to understand the extraordinary variation in genome size (C-value)—animals vary 7,000 fold and land plants some 2,400-fold—has a long history in biology.

[105] However, this variation is poorly correlated with gene number or any measure of organismal complexity, which led CA Thomas to coin the term C-value paradox in 1971.

[110] The presence of an abundance of transposable elements in many eukaryotic genomes was a central theme of the original selfish DNA papers mentioned above (See Conceptual developments).

[53] Unfortunately, the double-strand break that is introduced by Cas9 can be corrected by homology directed repair, which would make a perfect copy of the drive, or by non-homologous end joining, which would produce "resistant" alleles unable to further propagate themselves.

The mathematics can define very crisply the different classes of elements by their precise behavior within a population, sidestepping any distracting verbiage about the inner hopes and desires of greedy selfish genes.

This is another excellent example showing that just because an element appears to have a strong selfish transmission advantage, whether it can successfully spread may depend on subtle configurations of other parameters in the population.

What is impressive about all these modeling efforts is how well they fitted empirical data, given that this was decades before discovery of the fact that the host fly has a powerful defense mechanism in the form of piRNAs.

[130] This article was adapted from the following source under a CC BY 4.0 license (2018) (reviewer reports): J Arvid Ågren; Andrew G. Clark (15 November 2018).