Experiments on yeast cells that are hosts to a killer virus confirm that natural selection can sometimes reduce fitness

Greig, D

Ono, J

English

UCL Discovery

EXPERIMENTAL EVOLUTIONFailure to progressExperiments on yeast cells that are hosts to a killer virus confirm thatnatural selection can sometimes reduce fitness.DUNCAN GREIG AND JASMINE ONOIt is hard to ignore the sense that life has pur-pose. This idea – known as teleology – iscentral to religious thinking. However, it isalso found in many areas of human culture andscholarship that one might expect to be freefrom divine influence. These other areas include,somewhat surprisingly, the study of evolution.Look at the March of Progress, for example: inthis infamous illustration a knuckle-draggingbeast gradually evolves to become an erectintelligent human. Experts agree that this widelyparodied image gives the wrong impression, butthe feeling that evolution is progressive persists.Perhaps the problem is the word itself. Toevolve originally meant to unroll, implying theroll-out of a predetermined form (Bowler, 1975).Scientists used it to describe the embryonicdevelopment of an individual, back when it wasthought that every human grew from a homun-culus, a complete miniature person containedwithin sperm, just waiting to ’evolve’ (Hor-der, 2010). By the mid-19th century ’evolution’had evolved to mean not just the developmentalchanges that occurred in individuals during theirlifetimes, but directional changes observed inspecies across the geological timescales pre-served within the fossil record. Early evolution-ists, such as Lamarck, proposed teleologies inwhich living things are innately driven to pro-gressively evolve more advanced adaptations.But Darwinian natural selection works withoutthese vital forces or supernatural design, and itis notable that Darwin himself rarely used theword evolution in reference to his revolutionarytheory.Evolution, in the modern Darwinian sense, isessentially a random process. Mutations are ran-dom, but they are also heritable, so those thathappen to improve their own transmission (thatis, to increase fitness) will spread, resulting inadaptation. This is natural selection. But there isno direction to the process. Consider eyes,organs so complex that they fool some intothinking they must have been designed by a cre-ator. Yet, having finally evolved this magnificentcomplexity, eyes will quite readily un-evolveagain when their owners move into lightlesscaves, where vision is a useless and expensiveliability.But does natural selection not imply a particu-lar form of progress, in that fitness itself mustalways increase? Not necessarily. Now, in eLife,Sean Buskirk, Alecia Rokes and Greg Langreport the results of experiments confirming thatnatural selection can sometimes result in areduction of fitness (Buskirk et al., 2020).The researchers, who are based at LehighUniversity, allowed populations of yeast cells toevolve for 1000 generations, freezing live sam-ples at regular intervals to create a ‘fossil record’from which ancestors and descendants could bedefrosted and compared. They found that themost evolved generations (those from the endof the experiment) would leave more offspringthan intermediate generations (from the middleof the experiments) when both were mixed andallowed to compete directly: that is, their Dar-winian fitness had increased. But when mixedwith their original ancestors (from the start ofCopyright Greig and Ono. Thisarticle is distributed under the termsof the Creative Commons AttributionLicense, which permits unrestricteduse and redistribution provided thatthe original author and source arecredited.Related research article Buskirk SW, RokesAB, Lang GI. 2020. Adaptive evolution ofnontransitive fitness in yeast. eLife 9:e62238. doi: 10.7554/eLife.62238Greig and Ono. eLife 2021;10:e66254. DOI: https://doi.org/10.7554/eLife.66254 1 of 3INSIGHTthe experiments), they were less fit; the originalancestors left more offspring. Yet, the intermedi-ate generations were fitter than the originalancestors. So, while fitness did in fact increase ateach step, it did not add up – together, some-how, two increases made a decrease.To understand why, we need to know thatthe ancestor yeast cells were host to a common‘killer’ virus (Figure 1). The virus encodes both adeadly toxin and resistance to that toxin, soyeast cells containing the virus are immune, butthe yeast cells without are not. The virus cannotinfect new host cells and is only transmittedthrough the offspring of its hosts. However,there is no benefit to making a toxin if all yourcompetitors are resistant. So, as the virus popu-lations evolved, the ability to make a worthlesstoxin was lost. And without the toxin, there wasno advantage to having resistance to it so, even-tually, resistance was also lost in the mostevolved generations of yeast cells.Figure 1. An example of evolution going round in circles. Buskirk et al. used yeast cells (thin orange circles) thatare infected with a virus producing both a killer toxin (green arrows) and resistance to the toxin (thick blue circles)at the start of the experiment (represented by the 12 o’clock position). As evolution proceeds (black arrow), cellsthat no longer produce the toxin but are still resistant to it, take over. Eventually, these cells are replaced by cellsthat have lost their resistance (since resistance now provides no benefit). But when cells from the latest generationare pitted against cells from the original generation (grey arrows), the latter emerge victorious as the toxins theyproduce kill the former (open orange squiggles). However, cells from the latest generation can outcompete cellsfrom intermediate generations, and cells from intermediate generations can outcompete cells from the originalgenerations.Greig and Ono. eLife 2021;10:e66254. DOI: https://doi.org/10.7554/eLife.66254 2 of 3Insight Experimental Evolution Failure to progressThus, when cells from these generations wereintroduced to cells from the original generations,they succumbed to the viral toxin. Buskirk et al.were able to show that natural selection actingon the host genomes, the viral genomes, orboth, drove the entire process, eventually reduc-ing the long-term competitive fitness of theyeast. So, evolutionary changes, including fit-ness, are not necessarily progressive.Is this due to having two genomes – viral andnuclear – with intertwined fates? Probably not.Take the game rock-paper-scissors as an illustra-tion. An imaginary population of reproductiverocks might evolve into mutant pieces of paper,which would have higher fitness. But once paperhas taken over, it would be replaced bydescendants that evolved into scissors. Are scis-sors fitter than their distant ancestors, the rocks?No.Such circular interactions – where everyonecan beat someone, but everyone can also bebeaten by someone else – are common innature, both between and within species(Soliveres et al., 2018; Sinervo and Lively,1996). But Buskirk et al. show for the first timethat the different players can also replace eachother within a single evolutionary lineage. Wesometimes feel we are making great progress –in art, architecture, fashion, or even in theunfolding of historical events – only to recognizesomething from the past coming round again.Evolution seems much the same.Duncan Greig is in the Centre for Life’s Origins andEvolution, Department of Genetics, Evolution andEnvironment, University College London, London,United Kingdomd.greig@ucl.ac.ukhttps://orcid.org/0000-0002-8907-0253Jasmine Ono is in the Centre for Life’s Origins andEvolution, Department of Genetics, Evolution andEnvironment, University College London, London,United Kingdomhttps://orcid.org/0000-0003-3301-0507Competing interests: The authors declare that nocompeting interests exist.Published 16 February 2021ReferencesBowler PJ. 1975. The changing meaning of"evolution". Journal of the History of Ideas 36:95–114.DOI: https://doi.org/10.2307/2709013,PMID: 11610247Buskirk SW, Rokes AB, Lang GI. 2020. Adaptiveevolution of nontransitive fitness in yeast. eLife 9:e62238. DOI: https://doi.org/10.7554/eLife.62238,PMID: 33372653Horder T. 2010. History of developmental biology. In:Encyclopedia of Life Sciences. Chichester: John Wiley& Sons, Ltd. DOI: https://doi.org/10.1002/9780470015902.a0003080.pub2Sinervo B, Lively CM. 1996. The rock–paper–scissorsgame and the evolution of alternative male strategies.Nature 380:240–243. DOI: https://doi.org/10.1038/380240a0Soliveres S, Lehmann A, Boch S, Altermatt F, CarraraF, Crowther TW, Delgado-Baquerizo M, Kempel A,Maynard DS, Rillig MC, Singh BK, Trivedi P, Allan E.2018. Intransitive competition is common across fivemajor taxonomic groups and is driven by productivity,competitive rank and functional traits. Journal ofEcology 106:852–864. DOI: https://doi.org/10.1111/1365-2745.12959Greig and Ono. eLife 2021;10:e66254. DOI: https://doi.org/10.7554/eLife.66254 3 of 3Insight Experimental Evolution Failure to progress

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