Use it or lose it?

This post is a guest contribution by Dr. Levi Morran, NIH postdoctoral fellow at Indiana University. Levi studies the role that both coevolutionary relationships and mating systems play in shaping evolutionary trajectories. His research using experimental coevolution to test the Red Queen hypothesis recently appeared in Science and was featured on NPR and the BBC.

The 40 Year-Old Virgin movie poster

The 40 Year-Old Virgin

In the movie, The 40 Year Old Virgin, Steve Carell’s character (the title character) asks a sex education instructor, “Is it true that if you don’t use it, you lose it?” Given the context, I’ll allow you to put the pieces together and figure out just what he was referencing with the question. But, the phrase “use it or lose it” is quite catchy isn’t it?

Surprisingly, the phrase is thought to have some relevance in the field of evolutionary genetics, particularly regarding bacterial genomes. You see, widespread gene loss and genome reduction has been observed in some strains of bacteria, particularly those that specialize in certain environments (Cramer et al. 2011; Ernst et al. 2003; Smith et al. 2006). But, how and why do bacteria “lose it”, and do they lose it because they don’t use it?

In a recent paper, Lee and Marx (2012) test both how and why they observe large-scale patterns of gene loss in their experimentally evolved populations of Methylobacterium extorquens. They evolved these bacterial populations under different treatments of resource availability (realms of specialization) and found that all replicate populations adapted to their specific treatment over 1,500 generations. During experimental evolution, 80% of the bacterial populations exhibited nearly a 10% reduction in genome size, and many of the gene losses occurred in similar regions of the genome, some even across treatments.

Methylobacterium extorquens
(photo credit R. Hermann)

First they address whether the large-scale reductions in genome size were adaptive, or more specifically, which evolutionary force was responsible for these changes? In terms of evolutionary forces, the two likely culprits are either natural selection or genetic drift. Losses due to drift should be random. Given that large portions of the genome were repeatedly lost in multiple lines it would appear that such loses were deterministic and thus indicative of natural selection. But Lee and Marx were able to test this hypothesis more explicitly.

The previously mentioned experimentally evolved populations were maintained under novel environmental conditions and at large population size, a great recipe for natural selection to act as the dominant evolutionary force. A different set of Methylobacterium extorquens were maintained under conditions maximizing the strength of genetic drift, a standard environment at the smallest possible population size. None of the populations in the group dominated by drift exhibited gene losses characteristic of the populations that adapted to novel conditions, a strong indication that the widespread gene losses were not random. Then to implicate selection in the genome reduction, several commonly deleted portions of the genome were removed from the bacterial ancestor, and its fitness increased in each specific treatment. Therefore, it appears that the deletions were adaptive and that natural selection was the primary force driving the observed gene losses.

Lee and Marx Modified Figure 1

Portions of the bacterial megaplasmid (a major piece of the genome) deleted across replicate populations. Each green, purple, blue, and red line represents the size and location of a deletion that occurred in a replicate population. Each color represents a different environment. DT1-3 where portions of the ancestral genome that were deleted to test the role of genome reduction in adaptation.

Lee and Marx went one step further to test the “use it or lose it” concept in bacteria. They addressed the question of why specific portions of the genome were lost due to selection. The predominant “use it or lose it” view is that DNA replication is time consuming and energetically expensive, therefore purifying selection streamlines the genome by removing non-essential genes. Contrary to this view, Lee and Marx found that the size of the deletion was in no way correlated with the magnitude of its deleterious effect (large pieces of DNA should be more costly in terms of replication). Rather, they found that specific genes in the regions of the genome that were lost actually reduced the fitness of individuals within the environment that they evolved. Thus, it appears that directional selection was the predominant force driving genome reduction in these populations, removing deleterious portions of the genome.

Ultimately, Lee and Marx demonstrate that portions of the wildtype bacterial genome can be deleterious under certain conditions, and that the bacterial genome can be streamlined as selection removes those genes and populations become adapted to specific conditions. So, rather than “use it or lose it”, I would say that this is a case of “lose it when its deleterious in specific environments” or “lose it in the event that you use it and it has negative effects”. Definitely not as catchy as “use it or lose it”, and its probably best if I refrain from putting either phrase back into the context of The 40 Year Old Virgin.

Literature Cited

Cramer N, Klockgether J, Wrasman K, Schmidt M, Davenport CF, et al. (2011) Microevolution of the major common Pseudomonas aeruginosa clones C and PA14 in cystic fibrosis lungs. Environ Microbiol 13: 1690–1704. DOI: 10.1111/j.1462-2920.2011.02483.x

Ernst RK, D’Argenio DA, Ichikawa JK, Bangera MG, Selgrade S, et al. (2003) Genome mosaicism is conserved but not unique in Pseudomonas aeruginosa isolates from the airways of young children with cystic fibrosis. Environ Microbiol 5:1341–1349. DOI: 10.1111/j.1462-2920.2003.00518

Lee, M.C. and C. J. Marx. (2012) Repeated, selection-driven genome reduction of accessory genes in experimental populations. PLoS Genetics. 8:e1002651. DOI: 10.1371/journal.pgen.1002651

Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, et al. (2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103: 8487–8492. DOI: 10.1073/pnas.0602138103

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5 comments on “Use it or lose it?

  1. Hi Levi.

    You say, First they address whether the large-scale reductions in genome size were adaptive, or more specifically, which evolutionary force was responsible for these changes? In terms of evolutionary forces, the two likely culprits are either natural selection or genetic drift.

    If we’re talking about fixation, then what else is there by NS and drift? Fixation due to gene flow or mutation are too unlikely that anyone ever considers them. I’m not even sure how fixation by gene flow would occur. A founder effect?

    Anyway, just a quibble. Great post.

  2. Levi Morran says:

    Hi Bjørn,

    Thanks for posting!

    I would say that calling selection and drift the “likely culprits” was more literary effect than acknowledgement that other evolutionary forces may be driving fixation. I agree that fixation by any other evolutionary force would be pretty improbable. However, it is kind of fun to think about fixation due to mutation, specifically in a large population. I guess that would be a situation of spontaneous fixation in which each gamete produced by every parent contained exactly the same mutation.

  3. Wil Fleming says:

    Well Levi I quit understanding after the 40 year old virgin reference (apparently my extensive bio knowledge was lost after completing L211 at IU). Regardless I really enjoyed your writing and think that this piece is the best piece of bio that I have read since L112!!!

  4. Levi Morran says:

    Thanks Wil! But, I don’t think you give your bio abilities enough credit. I remember those days of battling for the top score in Mrs. Horn’s class, not sure I ever beat you.

  5. [...] what a good guest post looks like? Check out previous ones by David Hembry, Kathryn Turner, Levi Morran, and Amy Dapper—who is now joining us as a regular [...]

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