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Adaptive Evolution Or Genetic Drift?

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Adaptive Evolution Or Genetic Drift? Heredity (2004) 93, 122–123 & 2004 Nature Publishing Group All rights reserved 0018-067X/04 $30.00 www.nature.com/hdy NEWS AND COMMENTARY ...............................................................Genome complexity The promoter regions in higher organ- isms are much larger, and there appears Adaptive evolution or genetic drift? to be a much greater variety of protein complexes that interact with these regu- Does genome complexity produce latory DNAs, which help to provide the tissue specificity of gene expression found in multicellular organisms. organismal complexity? These differences in the number of RB Phillips regulatory protein complexes between yeast and higher organisms may explain ........................................................... the findings in another recent paper by Heredity (2004) 93, 122–123, advance online publication, 12 May 2004; doi:10.1038/ Yang and Li (2003). The authors reason sj.hdy.6800494 that protein complexity, defined as the number of subunits in a protein (n), might explain whether duplicate genes are retained, since duplication of one n their recent Science paper, Lynch complexity provides the raw material subunit might cause a dosage imbalance and Conerly, 2003 argue that in the for organismic complexity, although the among the subunits of a protein. They I transition from prokaryotes to multi- authors acknowledge that the two are found that the proportion (P) of un- cellular eukaryotes, population sizes often not very well correlated. For duplicated genes increased with the decreased dramatically as the size of example, the fact that subfunctionaliza- number of subunits in a protein. How- organisms increased. This magnified the tion of genes is much more likely than ever, P was higher for both monomers power of random genetic drift and neofunctionalization means that posses- and multimers in yeast, but low in allowed the proliferation of genome sion of extra copies of genes does not humans, and the family size of genes features that would have been elimi- usually lead to evolutionary innovation. was also significantly higher in humans nated by purifying selection in larger Although the genomes of eukaryotes compared with yeast. These results populations. Once these features were are generally larger than those of pro- suggest that organismal complexity is in place, they provided the raw material karyotes, genome size is not correlated a stronger determinant of gene duplic- for evolution of phenotypic complexity with organismal complexity. Unicellular ability than is protein complexity, and by natural selection. eukaryotes have genome sizes that vary are consistent with the analysis of Lynch In support of the first part of their over 200 000-fold, with the genome of the and Conerly (2003) as well as that of hypothesis, the authors present convin- Amoeba being about 200 times greater Levine and Tjian (2003). The duplicate cing data showing that prokaryotes than that of humans (Gregory, 2001). genes would have a higher probability have larger effective population sizes The number of genes in the sequenced of being retained in higher organisms, than do most eukaryotes. In fact, one of organisms, in general, shows a gradual and this could lead to duplicate sets the few supposed exceptions to this increase in organismal complexity, from of regulatory multimers that acquire trend is probably not an exception after Escherichia coli with about 4300 genes, tissue-specific functions. all. The ciliate Tetrahymena thermophilia and yeast with 6000, to Drosophila with The idea that evolution of regulatory is listed as having a very large popula- 15 000 and humans with 30 000. How- genes might explain the disconnection tion size, more in keeping with prokar- ever, Caenorhabditis elegans has 21 000 between genome change and organis- yotes, but the reference cited ignores the genes and is morphologically less mic change was suggested about 30 fact that this ‘species’ is in reality a complex than Drosophila. The estimated years ago by Allan Wilson and colla- ‘species complex’ composed of repro- number of genes for the ciliate Para- borators (Cherty et al, 1978). This was ductively isolated syngens. mecium tetraurelia is similar to that for prompted by the discovery of the large The new genomic complexity found humans (McGrath and Katz, 2004). There genome differences among morphologi- in higher organisms includes introns, are many examples in higher plants of cally similar frog species and the small mobile genetic elements, and an in- polyploids with large num-bers of du- nucleotide difference between chimpan- crease in duplicate genes. Mobile ele- plicate genes, but no more organismic zees and humans. Thus, there are wide- ments are mainly found in genome sizes complexity than in related diploids. spread examples of structural stasis in above 100 MB, and larger introns are Genomic turnover is not related to the face of substantial genomic change found in areas of the genome with low organismic change either. Sequence from prokaryotes to unicellular eukar- recombination rates (Carvalho and divergence is substantial between some yotes to higher organisms including Clark, 1999). These observations sup- of the Tetrahymena ‘syngens’ that appear vertebrates. port their idea that these features might identical. Sequencing of a second worm Multicellular organisms have evolved be retained passively in larger genomes has revealed that there is a three-fold multiple times in prokaryotes and eu- in response to a reduction in purifying larger sequence divergence between the karyotes (Kaiser, 2001) and in some selection. The suggestion that the half- two worms (C. brigissae and C. elegans)than cases related unicellular and multicel- life of duplicate genes might increase between humans and mice (Blaxter, 2003). lular relatives live in the same environ- with genome size in response to de- So, what does determine organismic ment. It has been hypothesized that creasing effective population size is also complexity? Levine and Tjian, 2003 advantages in feeding and dispersion plausible. If so, genetic drift has had a argue that organismic complexity corre- may have driven the evolution of these much greater role in adaptive evolution lates with an increase in the ratio and new forms. The genomes of several of in complex genomes than has been number of transcription factors per these species pairs are currently being envisioned by advocates of neutral theory. gene. The yeast genome has 300 tran- sequenced, and some of these species The underlying assumption in Lynch scription factors, but there are 1000 in can be maintained in the laboratory, so and Conery’s report is that this genomic Drosophila and possibly 3000 in humans. they will be excellent models for in- News and Commentary 123 vestigation of the forces involved in require a deeper understanding of the Gregory TR (2001). Biol Rev 76: 65–101. evolution of organismic complexity. organization of this complexity. McGrath CL, Katz LA. (2004). Trends Ecol Evol 19: RB Philips is at the Department of Biological 32–38. In response to environmental change Blaxter M (2003). Nature 426: 395–396. Sciences, Washington State University, Vancouver, on our planet, most species have Levine M, Tjian R (2003). Nature 424:147– WA 98686-9600, USA. become extinct, some have retained 151. their structural integrity and a few e-mail: [email protected] Yang, Li (2003). Proc Natl Acad Sci USA 100: 15661–15665. have evolved greater organismic com- Lynch M, Conerly JS (2003). Science 302: Cherty LM, Case SM, Wilson AC (1978). Science plexity. Understanding how multicellu- 1401–1404. 200: 209–211. lar organisms evolved will in turn Carvalho AB, Clark AG (1999). Nature 401: 344. Kaiser D (2001). Ann Rev Genet 35: 103–123. Heredity.
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