Selfish genes, the phenotype, paradigm and genome evolution

Ford Doolittle and Carmen Sapienza, Nature, 1980
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Ford Doolittle is a biochemist and member of the National Academy of Sciences. In 1980 he and Sapienza argued for large amounts of junk DNA must exist in higher organisms because selfish genes would duplicate much faster than selection could remove them. He and Sapienza write:

Natural selection operating within genomes will inevitably result in the appearance of DNAs with no phenotypic expression whose only 'function' is survival within genomes. Prokaryotic transposable elements and eukaryotic middle-repetitive sequences [repeats in the middle of a chromosome] can be seen as such DNAs, and thus no phenotypic or evolutionary function need be assigned to them. The assertion that organisms are simply DNA's way of producing more DNA has been made so often that it is hard to remember who made it first... The DNA is there because it facilitates genetic rearrangements which increase evolutionary versatility (and hence long-term phenotypic benefit), or because it is a repository from which new functional sequences can be recruited or, at worst, because it is the yet-to-be-eliminated by-product of past chromosomal rearrangements of evolutionary significance.

[page 601, Non-phenotypic selection]

if it can be shown that a given gene (region of DNA) or class of genes (regions) has evolved a strategy which increases its probability of survival within cells, then no additional (phenotypic) explanation for its origin or continued existence is required. This proposal is not altogether new; Dawkins, Crick, and Bodmer have briefly alluded to it...

[page 602, left column]

A single copy of a DNA sequence of no phenotypic benefit to the host risks deletion, but a sequence which spawns copies of itself elsewhere in the genome can only be eradicated by simultaneous multiple deletions.

[page 603, The rest of the eukaryotic genome]

Such [transposlabe] elements, once inserted, are relatively immune to deletion (Since only very precise deletion can be non-lethal)

[page 603, Necessary and unnecessary explanations]

It is inevitable that natural selection of the special sort we call non-phenotypic will favor the development within genomes of DNAs whose only 'function' is survival within genomes [selfish genes]. When a given DNA, or class of DNAs, of unproven phenotpyic function can be shown to have evolved a strategy (such as transposition) which ensures its genomic survival, then no other explanation for its existence is necessary. The search for other explanations may prove, if not intellectually sterile, ultimately futile.

Like Ohno, Doolittle and Sapienza suggest that a large genome couldn't be maintianed by selection, claiming duplicating selfish genes as a plausible alternative:

if the calculations of Kimura and Salser and Isaacson are correct, middle-repetitive DNAs together comprise too large a fraction of most eukaryotic genomes to be kept accurate by Darwinian selection operating on organismal phenotype. The most plausible form of "remultiplication of the 'correct' surviving sequences" is transposition.