One of the most bizarre phenomena uncovered since we’ve been able to sequence genomes is that of “programmed genome rearrangement” (PGR), whereby an animal starts its life as a zygote with a full genome, and then some of its genes are lost from the somatic (body) cells as development proceeds. This has been seen in organisms as diverse as flies, hagfish, zebra finches, and, especially, ciliate protozoans, which extensively remodel their genomes during development, getting rid of repetitive DNA elements (“satellite DNA”).
It’s not entirely clear why this happens, but what is clear is that in organisms like us that whose somatic cells are segregated from the germ cells (cells that produce our sperm and eggs) gene loss doesn’t occur in germ cells. It couldn’t, for if those genes did have functions in the germ tissue, they’d be irrevocably lost in the next generation. In fact, if you find a gene present in germ cells but not somatic cells, because it’s lost in the latter, that gene almost certainly does something in germ cells.
Gene loss has also been described previously in the hagfish, a jawless vertebrate that, together with lampreys, make up the monophyletic group cyclostomes. Here’s a hagfish:
But the most comprehensive study yet of programmed genome reduction was just published by Jeremiah Smith and three colleagues in Current Biology (reference below). Building on previous but less comprehensive work suggesting that from development of egg to adult, the sea lamprey (Petromyzon marinus) lost about 20% of its genes in body tissues (while retaining them all in the germ line), Smith et al. sequenced DNA from both germ tissues and body tissues of single individuals. Here’s are two sea lampreys on a brown trout: they’re parasitic on fish and usually kill them by sucking blood:
The authors sequenced DNA from body tissues (and blood) as well as germline tissue (sperm), and also looked at the RNA transcripts. What they found was this:
- 13% of DNA sequences found in the germline were missing in body tissues, roughly consonant with the 20% reported in previous work on this species.
- The genes eliminated from the DNA during development—and we’re not quite sure how this happens— included not just repeated satellite DNA, but real, single-copy genes that have functions. Eight genes were identified that were active in germ cells but not somatic cells, and there are undoubtedly more.
- The functions of these genes in germ cells give one clue why they might be eliminated in body cells. (The genes include APOBEC-1 Complementation Factor, RNA Binding Motif 46 [cancer/testis antigen 68], and two “zinc finger” proteins.) The authors note that these genes do act very early in development to segregate the germ cells from the body cells, and have other unknown functions in the germline—they could, for example, be involved in crossing-over between chromosomes or the production of sperm and eggs themselves.
- Why, then are those genes eliminated from body cells? The authors suggest that genes like those identified above have crucial functions either in germ cells or in segregating germ cells from body cells early in development, but might be deleterious within body cells, perhaps because their bad effects—in particular, in causing cancers—outweigh any good effects. In other words, there’s a conflict within the bodies of lampreys and hagfish between germ and body cells. The way evolution appears to have resolved this conflict is to simply get rid of the “bad” body genes during development. An alternative strategy would be to “silence” those genes in the body tissues—prevent their expression in non-germ cells—and I’m not sure why they’re removed rather than silenced. (It might be evolutionarily “easier” to snip out genes than silence them, but yet many species, including ourselves, have ways of silencing different genes in different tissues without removing those genes from the DNA. The reason different tissues are different is because they express different sets of genes.)
Many questions remain. Are those genes eliminated from body cells in fact deleterious if they remain in body cells? If so, why do they remain active in the bodies of non-jawless vertebrates, like ourselves? Second, if they’re harmful in the body, how are they harmful? Do they cause disease, or do they simply impose a useless metabolic and somatic burden? Third, is this phenomenon of PGR an ancestral condition, since jawless vertebrates are the descendants of the earliest vertebrates, or has it evolved secondarily in those lineages? As the authors note:
Notably, both extant lineages of jawless vertebrates (agnathans: lampreys and hagfish) are known to undergo PGR, which would seem to indicate that the phenomenon is common to all extant agnathans [jawless fish] and potentially represents an ancestral condition. Thus, PGR may represent an ancient mechanism for moderating genetic conflict between germline and soma that evolved within an ancestral vertebrate lineage (alternately, repeated evolution of PGR in lamprey, hagfish, and numerous invertebrate and protist lineages may reflect recurrent selective advantages for PGR).
Finally, are different genes eliminated in different body tissues, or do all body cells get rid of the same set of genes? The authors’ analysis was too coarse to answer this question.
Regardless, the phenomenon of eliminating some genes from body tissues but not from germ tissues appears to have an evolutionary advantage, for it has happened (or been retained) in many lineages. What that advantage is remains to be seen. This is an example of one of the evolutionary questions that could only be studied properly once we became able to sequence DNA.
Smith, J.J., Baker, C., Eichler, E.E., and Amemiya, C.T. (2012). Genetic consequences of programmed genome rearrangement. Curr. Biol. 22, 1524–1529.