This burden might seem prohibitive for strict adaptationists1 since everything that's detrimental should be lost by negative selection. Lynch, and others, ague that the cost is usually quite small and if it's small enough the detrimental effect might be below the threshold that selection can detect. When this happens, new stretches of DNA become effectively neutral (nearly neutral) and they can be fixed in the genome by random genetic drift.
The key parameter is the size of the population since the power of selection increases as the population size increases. Populations with large numbers of individuals (e.g. more than one million) can respond to the small costs/burdens and eliminate excess DNA whereas populations with smaller numbers of individuals cannot.
Michael Lynch and Georgi Marinov (Hi, Georgi!) have just published a paper where they attempt to calculate the cost of adding DNA as well as the cost associated with transcribing that DNA and translating it into protein (Lynch and Marinov, 2015). One of the goals of the paper is to figure out the overall selective advantage of a new gene given that its product might confer selective advantage when there's an energy cost—in ATP equivalents—associated with every new gene.
Here's how they put it ...
Based on its phenotypic manifestations, a gene may have a multiplicity of advantages, but the energetic cost of replication, maintenance, and expression represents a minimum burden that must be overcome to achieve a net selective advantage. If a genic variant or a novel gene is to be efficiently promoted by natural selection, the net selective advantage (beyond the energetic cost) must exceed the power of drift (defined as 1/Ne for a haploid organism, where Ne is the effective population size).This is all standard stuff. The innovative parts of the paper are: (1) more specific calculations of costs based on experimental results in the literature, and (2) whether the cost of a gene is related to cell size.
Why is this second goal significant? Because extreme complexity and multicellularity are only seen in eukaryotic cells and eukaryotic cells are much larger than prokaryotic cells. Larger cells require much more protein (and membranes) than small cells so each eukaryotic gene has to produce a lot more proteins than a the same gene in a small cell. The cost of adding a gene to the genome is small compared to the cost of making proteins. Cells could not grow larger and more complex as long as they were limited in their energy production.
Nick Lane and Bill Martin (Lane and Martin, 2010) have argued that eukaryotic cells overcame this limitation due to the inclusion of mitochondria. This allows the cell to produce much more energy making the cost of a gene (mostly protein synthesis) less detrimental than it would be if cell size and complexity increased in prokaryotic cells.
Lynch and Marinov looked at the cost of replicating DNA, the cost of making mRNA, and the cost of making proteins in different cells. The results show that increased cell size does not impose a significantly increased energy burden so there's no need to speculate that mitochondria were necessary for expanded genomes and more complexity. Population genetics can account for the observations.
Taken together, our observations suggest that an energetic boost associated with the emergence of the mitochondrion was not a precondition for eukaryotic genome expansion.This is probably a bit too much for most of you so I'll concentrate on the other conclusions. These are things you have to know if you want to understand genome evolution.
- Bacterial species (prokaryotes) typically have large population sizes. The cost/burden of adding even small amounts of DNA to the genome in these cells is sufficiently detrimental that it can be detected by natural selection. This is why bacterial genomes tend to be small and compact.
The preceding results indicate that the energetic cost of replicating a DNA segment of even just a few nucleotides (even if nontranscribed) can be sufficient to be perceived by selection in a typical bacterial population with large Ne.
- Eukaryotic species, especially multicellular eukaryotic species, tend to have small population sizes. In this case, the detrimental cost of adding extra DNA cannot be detected by natural selection so there's no impediment to expanding the genome.
In contrast, insertions of even many kilobases often impose a small enough energetic burden relative to the overall requirements of eukaryotic cells to be immune to selection.
- Transcription is also expensive so when a new segment of DNA is transcribed as well as replicated it imposes an even greater cost. However, the extra burden of transcription is still not sufficient to make the cost subject to natural selection in eukaryotic species. Junk RNA is not that harmful. Pervasive transcription is not that harmful.
Although RNA-level costs are frequently greater than those at the DNA level, these are often still not large enough to overcome the power of random genetic drift in eukaryotic cells. This means that many nonfunctional DNAs that are inadvertently, even if specifically, transcribed in eukaryotes (especially in multicellular species) cannot be opposed by selection, a consideration relevant to the debate as to whether transcriptional activity is an indicator of functional significance.
- Protein synthesis is expensive. If a new gene has to produce a lot of protein then the cost/burden can be prohibitive, even in eukaryotic species with small populations. This cost has to be overcome by a greater selective advantage to making the proteins. This is why a multicellular eukaryote can have lots of junk DNA making lots of junk RNA but NOT lots of junk protein. It's also why most accidental protein-coding gene duplications usually result in selection for turning off one of the copies.
However, with the cost at the protein level generally being much greater than that at the RNA level, segments of DNA that are translated can sometimes impose a large enough energetic cost to be susceptible to selection, even in multicellular species. This may explain why redundant duplicate genes commonly experience high rates of nonfunctionalization.
1. And for Intelligent Design Creationists who think that strict adapationism (Darwinism) is the only scientific game in town.
Lane, N., and Martin, W. (2010) The energetics of genome complexity. Nature, 467(7318), 929-934. [doi: 10.1038/nature09486]
Lynch, M., and Marinov, G.K. (2015) The bioenergetic costs of a gene. Proc. Natl. Acad. Sci. (USA) published online Nov. 2, 2105 [doi: 10.1073/pnas.1514974112]