De novo genes1 are quite rare but genome duplications are quite common. Sometimes the duplicated regions contain genes so the new genome contains two copies of a gene that was formerly present in only one copy. "Common" in this sense means on a scale of millions of years. Michael Lynch and his colleague have calculated that the rate of fixed gene duplication is about 0.01 per gene per million years (Lynch and Conery, 2003 a,b; Lynch 2007). Since a typical vertebrate has more than 20,000 genes, this means that 200 genes will be duplicated and fixed every million years.
The initial duplication event is likely to be deleterious since there will now be redundant DNA in the genome. The slightly deleterious allele (duplication) can be purged by negative selection in species with large population sizes (e.g. bacteria). But in species with smaller populations, natural selection is not powerful enough to eliminate slightly deleterious alleles so the duplication persists and may become fixed in the population.
Following the "birth" of a new gene by duplication, there are several possible fates for the duplicated gene in such species. They have been explored by Masatoshi Nei and his collaborators over the past 30 years. The process is usually referred to as "Birth-and-Death Evolution" (see Nei and Rooney, 2005). The basic idea goes back to Susumu Ohno (e.g. Ohno, 1972; see Meyer and Van der Peer, 2003). Here are the possible fates.
- One of the genes will "die" by acquiring fatal mutations. It becomes a pseudogene.
- One of the genes will die by deletion.
- Both genes will survive because having extra gene product (e.g. protein) will be beneficial (gene dosage).
- One of the genes acquires a new beneficial mutation that creates a new function and at the same time causes loss of the old function (neofunctionalization). Now both genes are retained by positive selection and the complexity of the genome has increased.
- Both genes acquire mutations that diminish function so the genome now needs two copies of the gene in order to survive (subfunctionalization).
Birth and death can be studied by looking at related lineages or by looking at large gene families. (The original idea came from studying genes at the MHC locus in mammals.) But there's a much easier way of getting information on this phenomemon and that's by looking at species that have undergone whole genome duplications (WGD) to create tetraploid cells. In those cases, every gene has been duplicated and you can follow the fate of every duplicate over time.
The birth and death of salmon genes]. In that species, about half the genes have been lost by deletion or by fatal mutations leading to a pseudogene. The other half appear to be functional. Most of them seem to have the same function as the original gene suggesting that there hasn't been enough time to inactivate them by mutation.
A similar study was done in carp where the genome duplication event took place only 8 My ago.
The latest study looks at the genome of the frog, Xenopus laevis (Session et al., 2016). The genome of this frog is essentially tetraploid, it derives from a hybridization between two species about 18 My ago. This was immediately followed by whole genome duplication (WGD) to restore chromosome pairing during meiosis. The two (unknown) progenitor species diverged about 34 My ago.
There's a nice News & Views article to accompany the paper: Genomics: A matched set of frog sequences (Burgess, 2017).
The analyses looked at which pairs of genes from the two different genomes survive. The authors found that genes were preferentially lost from the chromosomes of one of the parent species and not from the other. The reason for this preferential loss is not known.
Of the genes that are missing, the authors estimate that about 36% of the duplicate genes were deleted and about 64% became non-functional pseudogenes. The birth-and-death rates in Xenopus laevis are about the same as in other species that have been looked at, although there may be a slight tendency to retain more duplicate copies than in salmon or carp. It's possible that dosage effects are more important in this hybrid.
You can't easily determine whether some duplicated copies have acquired additional functions by neofunctionalization of subfunctioalization. The gene expression studies indicate that most duplicated genes have the same expression profile suggesting they probably still have the same function. Some are different and that's an indication of divergence.
All-in-all, the results are consistent with the basic concepts of birth-and-death and neutral evolution. Following duplication, the large genome gradually evolves back to the original number of genes but much of the duplicated sequences are retained as junk DNA. That's the same thing that happens with local DNA duplications.
1. Genes that arise from DNA sequences that are not genes in closely related species.
Lynch, M., and Conery, J.S. (2003a) The evolutionary demography of duplicate genes. Journal of structural and functional genomics, 3:35-44. [doi: 10.1023/A:1022696612931]
Lynch, M., and Conery, J.S. (2003b) The origins of genome complexity. Science, 302:1401-1404. [doi: 10.1126/science.1089370 ]
Lynch, M. (2007) The origins of genome architecture. Sunderland Massachusetts, USA: Sinauer Associates, Inc. Publishers. p. 45
Meyer, A., and Van de Peer, Y. (2003) 'Natural selection merely modified while redundancy created'–Susumu Ohno's idea of the evolutionary importance of gene and genome duplications. Journal of structural and functional genomics, 3:7-9. [PubMed]
Nei, M., and Rooney, A.P. (2005) Concerted and birth-and-death evolution of multigene families. Annual review of genetics, 39:121-152. [doi: 10.1146/annurev.genet.39.073003.112240]
Ohno, S. (1972) So much "junk" in our genome. In H. H. Smith (Ed.), Evolution of genetic systems (Vol. 23, pp. 366-370): Brookhaven symposia in biology.
Session, A.M., Uno, Y., Kwon, T., Chapman, J.A., Toyoda, A., Takahashi, S., Fukui, A., Hikosaka, A., Suzuki, A., and Kondo, M. (2016) Genome evolution in the allotetraploid frog Xenopus laevis. Nature, 538:336-343. [doi: 10.1038/nature19840]