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The Genetic Causes of Convergent Evolution

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The Genetic Causes of Convergent Evolution Nature Reviews Genetics | AOP, published online 9 October 2013; doi:10.1038/nrg3483 REVIEWS The genetic causes of convergent evolution David L. Stern Abstract | The evolution of phenotypic similarities between species, known as convergence, illustrates that populations can respond predictably to ecological challenges. Convergence often results from similar genetic changes, which can emerge in two ways: the evolution of similar or identical mutations in independent lineages, which is termed parallel evolution; and the evolution in independent lineages of alleles that are shared among populations, which I call collateral genetic evolution. Evidence for parallel and collateral evolution has been found in many taxa, and an emerging hypothesis is that they result from the fact that mutations in some genetic targets minimize pleiotropic effects while simultaneously maximizing adaptation. If this proves correct, then the molecular changes underlying adaptation might be more predictable than has been appreciated previously. (FIG. 1) Fitness Different species often evolve similar solutions to envi­ introgression . It is worth distinguishing between The potential evolutionary ronmental challenges. Insects, birds and bats evo­ these scenarios because each provides evidence for a dif­ success of a genotype, defined lved wings, and octopi, vertebrates and spiders ferent evolutionary path3. The first case, the independent as the reproductive success or evolved focusing eyes. Phenotypic convergence provides origin and spread of mutations, has been called parallel the proportion of genes that an individual leaves in the gene compelling evidence that ecological circumstances can genetic evolution. I suggest that the evolution of alleles 1,2 pool of the next generation in a select for similar evolutionary solutions . Historically, which were present in an ancestral population (the sec­ population. The individuals convergent evolution was thought to occur primarily by ond case) and the evolution of introgressed alleles (the with the greatest fitness leave divergent evolution of genetic mechanisms. For exam­ third case) should be collectively called collateral genetic the highest number of ple, multiple instances of wing evolution almost cer­ evolution (the Oxford Dictionary of English109 defines surviving offspring. tainly reflect evolution mainly through different genetic collateral as being “descended from the same stock but Hybridization mechanisms in different taxa. Also, if convergence is by a different line”). This precedent comes from palae­ Interbreeding of individuals considered at a sufficiently general level, such as con­ ontology, in which, in 1969, Shaw4 defined collateral from genetically distinct vergence of organismal fitness to similar environmental evolution as the simultaneous appearance of the same populations, regardless of the taxonomic status of the challenges, then multiple divergent genetic mechanisms phenotypic forms in the stratigraphic record. populations. might often contribute to increasing fitness. However, at Although phenotypic convergence provides evidence a more fine­grained level, recent studies have revealed for similar patterns of natural selection1, parallel and col­ that morphology and physiology often converge lateral evolution can provide evidence for constraints on owing to the evolution of similar molecular mecha­ how variation can be generated by the genome or for nat­ nisms in independent lineages. In microorganisms, ural selection that favours the fixation of some genetic even fitness convergence often evolves through simi­ variants over others, or both3,5–8. More than 100 cases lar genetic changes. These new data reveal that genetic of parallel and collateral genetic evolution have been evolution may be more predictable than was appreci­ identified in recent years3 and have been studied using a ated before the application of molecular biology to variety of approaches (BOX 1). The abundance of parallel Janelia Farm Research Campus, Howard Hughes evolutionary questions. and collateral evolution therefore implies that genome Medical Institute, 19700 Convergent evolution at the genetic level can result evolution is not random, but rather that the origin or Helix Drive, Ashburn, from one of three processes: first, evolution by mutations the selective consequences of genetic variants, or both, Virginia 20147, USA. that occurred independently in different populations or might be somewhat predictable. e-mail: species; second, evolution of an allele that was polymor­ In this Review, I discuss three major topics. First, I [email protected] doi:10.1038/nrg3483 phic in a shared ancestral population; and third, evolu­ clarify some definitions and the implications of paral­ Published online tion of an allele that was introduced from one population lel versus collateral evolution. Second, I review recent 9 October 2013 into another by hybridization, a process that is known as examples that illustrate major patterns in parallel and NATURE REVIEWS | GENETICS ADVANCE ONLINE PUBLICATION | 1 © 2013 Macmillan Publishers Limited. All rights reserved REVIEWS a Parallel evolution b T A → T T A A A A A T A A → T T d Marine stickleback A c Collateral evolution through shared ancestry A/T Freshwater stickleback A → T T A/T Freshwater stickleback polymorphism 10 mm A A → T A/T f H. numata T H. ethilla H. hecale A H. pardalinus sergestus H. elevatus (rayed) e Collateral evolution H. pardalinus butleri through hybridization A H. timareta florencia (rayed) H. timareta sp. nov. A (postman) H. heurippa H. cydno A T H. melpomene rosina (postman) T H. melpomene melpomene (postman) A → T H. melpomene T amaryllis (postman) H. melpomene aglaope and malleti (rayed) H. erato T Nature Reviews | Genetics 2 | ADVANCE ONLINE PUBLICATION www.nature.com/reviews/genetics © 2013 Macmillan Publishers Limited. All rights reserved REVIEWS ◀ Figure 1 | Parallel and collateral genetic evolution. Convergent phenotypic evolution variants, or both. As discussed in further detail below, that results from similar molecular mechanisms acting in divergent taxa can occur the results of mutagenesis screens in multiple species through three historical paths, illustrated here in a phylogenetic framework. a | Parallel imply that mutations in many different genes can alter evolution refers to mutations that arise and spread in independent lineages. In this case, the phenotype in similar ways10,11. This suggests that, the ancestral state (A) independently evolved to a derived state (T) in two lineages. The yellow rectangles indicate the mutational origins of the T allele; the orange rectangles in many species, multiple mutations are accessible that represent substitutions of the A allele by the T allele throughout the population. could provide more than one solution to many ecologi­ b | An example of parallel evolution is shown: the monarch butterfly caterpillar (top left), cal challenges. Also, convergence often occurs through the red milkweed beetle (top right), oleander aphids (bottom left) and the large milkweed divergent genetic mechanisms in nature (BOX 2). Thus, beetle (bottom right), among others, have all evolved to feed on poisonous milkweed parallel evolution of mutations in the same genes in plants through parallel mutations in the (Na++K+) ATPase gene37,38. Extant species can different lineages suggests that evolution favours a undergo similar evolutionary changes by collateral evolution through shared ancestry or biased subset of mutations in these cases. through hybridization. c | In collateral evolution through shared ancestry, a mutation In contrast to parallel evolution, collateral evolu­ arises in an ancestral lineage (yellow rectangle) and later substitutes in multiple tion can provide evidence for the selection of individual descendent lineages (orange rectangles). d | An example of collateral evolution through variants, but it provides less compelling evidence than shared ancestry is shown. The loss of lateral plates in sticklebacks is illustrated by comparing a marine morph with complete body armour (top), a rare freshwater morph does parallel evolution that these variants are objectively with an intermediate number of lateral plates (middle) and a typical freshwater superior to other variants with respect to fitness. During morph with few lateral plates (bottom). The allele of major effect that reduces body parallel evolution, all mutations have the opportunity armour in most freshwater populations is also found at low frequency in the ancestral to be selected, and their likelihood of being exposed marine populations45. e | In collateral evolution through hybridization, a mutation arises to selection is proportional to their mutation rate. By in one lineage, descendants of which then hybridize with other species and spread the contrast, during collateral evolution, populations do not new mutation to related species. The mutation does not need to become fixed in need to wait for new mutations to arise, and pre­existing the population for it to spread by hybridization. f | An example of collateral evolution alleles can be selected even if alternative alleles would through hybridization is shown. The patterns of wing colours in three species of have provided superior fitness improvements12. In some butterflies from the genus Heliconius reflect, at least in part, the transfer of genomic cases, alleles that have been selected during previous regions through hybridization54. The curved arrows connect species that share similar alleles
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