Genes in Conflict: The Biology of Selfish Genetic Elements
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Werren et al. (1988) published the first general review of selfish or parasitic genes and defined an SGE as an element that has characteristics enhancing its own transmission relative to the rest of an individual’s genome but neutral or detrimental to the organism as a whole. Examples include transposable elements (TEs), meiotic drivers, supernumerary B chromosomes, postsegregation killers, and heritable microbes and organelles that distort sex determination. In 1988, the idea that elements in the genome could be parasitic was still contrary to prevailing opinions of many molecular biologists, who viewed the cell and organism as a highly integrated machine, and therefore considered the idea that components of the cell could be maintained because of their selfish replication as a bizarre and foreign concept. In contrast, the SGE model
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The critical feature of earliest life had to be a way to reproduce itself, and is common to all cellular life today. The DNA that exists today was almost certainly not a feature of the first life. The most accepted hypothesis is that . The mechanism today is that DNA makes RNA, and RNA makes proteins. DNA, RNA, proteins, sugars, and fats are the most important molecules in life forms, and very early on, protein “learned” the most important trick of all, which was an energy innovation: facilitate biological reactions. If we think about at the molecular level, it is the energy that crashes molecules into each other, and if they are crashed into each other fast enough and hard enough, the reaction becomes more likely. But that is an incredibly inefficient way to do it. It is like putting a key in a room with a lock in a door and shaking up the room in the hope that the key will insert itself into the lock during one of its collisions with the room’s walls. Proteins make the process far easier, and those proteins are called enzymes.
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is a more “ecological” view that considers the genome as a set of genetic elements with potentially different kinds of interactions, ranging from cooperative (mutualistic), to neutral (commensal), to selfish (parasitic) (Avise, 2001). According to this paradigm, genetic conflict can arise among components of the genome that have different transmission patterns (e.g., transposons, nuclear genes, cytoplasmic genes), and therefore conflicting genetic interests. The basic idea is as follows: When components of the genome have different transmission patterns, selection can act on an element to increase its transmission even if that is detrimental to the organism and/or other heritable components of the genome. Genetic conflict within the genome will then result, because enhanced transmission of an SGE decreases transmission of other genetic elements. An evolutionary “arms race” can then occur among different components of the genome over basic biological processes.
Here, we have a rogue’s gallery of the genome. SGEs can be placed into the following broad categories (Werren et al., 1988; Hurst and Werren, 2001; Burt and Trivers, 2006): TEs, biased gene converters, meiotic drivers, postsegregation drivers, and cytoplasmic drivers. These elements act to increase their own transmission to the detriment of other components of an individual’s genome. This does not mean that such elements cannot have positive long-term evolutionary consequences, and some of the elements in this list can have both selfish and beneficial components.
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Genomes are vulnerable to selfish genetic elements (SGEs), which enhance their own transmission relative to the rest of an individual’s genome but are neutral or harmful to the individual as a whole. As a result, genetic conflict occurs between SGEs and other genetic elements in the genome. There is growing evidence that SGEs, and the resulting genetic conflict, are an important motor for evolutionary change and innovation. In this review, the kinds of SGEs and their evolutionary consequences are described, including how these elements shape basic biological features, such as genome structure and gene regulation, evolution of new genes, origin of new species, and mechanisms of sex determination and development. The dynamics of SGEs are also considered, including possible “evolutionary functions” of SGEs.
Mobile elements include plasmids, endogenous viruses, and TEs. TEs have the ability to copy and move to new locations within the genome; as a consequence, they can accumulate. Doolittle and Sapienza (1980) and Orgel and Crick (1980) first proposed that they can be considered SGEs, and this view is now widely accepted (although see below). TEs fall into two main categories: DNA transposons move via DNA copies, and ret-rotransposons use an RNA intermediate (Kidwell and Lisch, 2001). TEs can also be autonomous (encoding proteins that promote their transposition) or nonautonomous (not encoding proteins needed for transposition but using the cellular machinery or proteins provided by other TEs). An interesting category of mobile elements is group I and II self-splicing introns (Lambowitz and Zimmerly, 2004), which can be tolerated in the typically streamlined genomes of prokaryotes and organelles because self-splicing restores functional open reading frames in genes with the inserts, thus reducing negative fitness costs. Although group II introns are not found in eukaryotes, shared features with the spliceosome of
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Other forms of biased gene conversion have been found in recombination hotspots in humans through detailed analysis of the products of recombination (Jeffreys and Neumann, 2002). The extent to which such biased gene conversion can be considered selfish depends on whether conversion bias is dependent on the sequence of the putative SGE. There is growing evidence in eukaryotes of a general GC gene conversion bias in DNA repair of double-strand breaks, resulting in AT/GC hetero-zygotes producing more GC than AT gametes (Duret and Galtier, 2009). Can we therefore consider G and C to be our smallest selfish elements? Probably not, because conversion is likely attributable to a general bias in using G and C during double-stranded break repair rather than to a biased conversion attributable to a specific sequence motif. In any case, GC-biased conversion clearly has major consequences for genome composition and evolution (Duret and Galtier, 2009).
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is that SGEs lead to antagonistic co-evolution with other components of the genome. Important features of eukaryotic genomes (e.g., DNA methylation, RNAi, small RNA regulatory pathways, R-M systems) have evolved, at least in part, as defense mechanisms against SGEs. Many genetic elements have mixed phenotypes, with both selfish (parasitic) and “beneficial” (“mutualistic”) features. The classic example is the mitochondrion, which is clearly beneficial but also shows selfish features (e.g., cytoplasmic male sterility) that reduce nuclear gene fitness, thus leading to genetic conflict. Evolutionary dependency can also evolve in hosts with ubiquitous SGEs, which can lead to irreversible dependence. Growing evidence supports a significant role of SGEs in eukaryotic development and speciation, and possibly also in extinction of species. Genome domestication of SGEs leads to evolutionary innovations, including acquisition of new genes and gene regulation from TEs, heritable microbes (e.g., ), and selfish plasmids. Safe havens can promote longer associations of SGEs with host lineages and also may facilitate their domestication. Finally, distinctions are made between the evolutionary consequences of SGEs and the factors that maintain them over evolutionary time. Clear formulations of the idea of evolvability as a means for evolutionary maintenance of SGEs will facilitate rigorous testing of this idea. Nevertheless, current evidence strongly supports the view that SGEs are maintained by their transmission-enhancing phenotypes and that evolutionary innovations emerging from them are a consequence of their existence rather than the cause.
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The genetic testing that has been performed on humanity in the past generation has shown that the founder group’s pattern of migration was to continually spread out, and once the original settlement covered the continents, people did not move much at all, at least until Europe began conquering the world (and there were some ). There is little sign of warfare in those early days of migration, and the leading hypothesis is that people moved to the next valley rather than be close enough to fight each other. Any conflict would have been easily resolved by moving farther out, where more easily killed animals lived. Also, in those virgin continents, people need not have roamed far to obtain food. Today, an !Kung woman will carry her child more than 7,000 kilometers before the child can walk for himself/herself. If an !Kung woman bears twins, it is her duty to pick which child to murder, because she cannot afford to carry two. That demonstrates the limitations of today’s hunter-gatherer lifestyle, but in those halcyonic days of invading virgin continents (which had to be the Golden Age of the Hunter-Gatherer), those kinds of practices probably waned and bands grew fast. When they they split, and the new group moved to new lands where the animals, again, never saw people before. Unlike the case with humans, there would not have been a grapevine so that animals told their neighbors about the new super-predator. The first time that those megafauna saw humans was probably their last time. It is very likely, just as with all predators for all time, and as can be seen with historical hunting events such or , that those bands soon took to killing animals, harvesting the best parts, and moving on. To them it would not have been a “blitzkrieg,” but more like kids in candy stores. After a few thousand years of grabbing meat whenever the fancy took them, or perhaps less, those halcyonic days were over as the far coasts of Australia were reached and the easy meat was gone. When that land bridge formed to Tasmania about 43 kya, people crossed and were able to , until all the megafauna was gone on Tasmania. They also may have worked their way through the food chain, in which the first kills were the true mother lode. Nobody even deigned to raise a spear at anything less than a until they were gone. Then they started killing smaller prey, which eventually did wise up and were harder to kill, so humans had to work at it again and the brief golden age was over. The as they shaped the new continent to their liking, maybe recreating the savanna conditions that they left in Africa, may have also been used to flush out animals if they began to avoid humans.
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