* Department of Genetics, University of Wisconsin, Madison
Fukui Prefectural University, Matsuoka-Cho, Yoshida-gun, Fukui, Japan
Correspondence: E-mail: jdoebley{at}wisc.edu.
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Abstract |
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Key Words: simple sequence repeat SSR genome size Zea mutation rate
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Introduction |
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One well-documented type of bias in microsatellite mutation is the tendency for new mutations to cause an increase in the size of an allele. This phenomenon has been documented in both plants (Udupa and Baum 2001; Vigouroux et al. 2002) and animals (Amos et al. 1996; Primmer et al. 1996; Cooper et al. 1999). This mutational bias and a differential mutation rate could explain the observed increase in the average size of microsatellites (directional evolution) between humans and nonhuman primates (Rubinsztein et al. 1995). However, this report of directional evolution has been questioned (Amos et al. 1996; Ellegren, Primmer, and Sheldon 1995) because the apparent directional evolution could be an artifact of ascertainment bias during microsatellite discovery (Hutter, Schug, and Aquadro 1998). A more recent study has shown evidence for directional evolution even when ascertainment bias is taken into account (Amos et al. 2003).
In this study, we take advantage of the known phylogeographic history of maize to ask whether maize microsatellites have experienced directional evolution in size. We analyze the evolution of microsatellite size between groups separated by fewer than 10,000 generations. We report both a directional increase in microsatellite size in geographically derived groups and a negative correlation of allele size and altitude that arose independently in North and South America. We discuss possible mechanisms that could generate these patterns and the implication of these biases for the application of microsatellite data to questions surrounding maize evolution and population genetics.
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Microsatellite Data |
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Maize was domesticated about 7,500 years ago in Mexico, and then spread to North and South America (Matsuoka et al. 2002b). A phylogenetic study has shown that North and South American maize are independently derived from the ancestral population in Mexico (Matsuoka et al. 2002b). Knowing this phylogeographic structure of maize enables us to ask whether directional evolution in maize microsatellites has occurred. For some of the analysis, we used the phylogeographic data as the basis for dividing our sample between 69 South American plants (SA), 71 Mexican and Guatemalan plants (ME), and 46 United States and Canadian plants (NA). Seven Caribbean plants were not classified in any of these three groups.
Statistical tests were performed using the software SYSTAT (Systat, Inc.).
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Results |
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Discussion |
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Directional evolution of this type could be explained in several ways. First, there could be a change in the degree of mutational bias to larger alleles in the derived groups. In our case, this would have had to occur twice, independently in North and South America. Second, given that mutations are more likely to cause an increase in allele size in maize (Vigouroux et al. 2002), a change in the mutation rate with movement into a new environment could cause directional evolution (Rubinsztein et al. 1995). Third, one could also propose a demographic explanation. For example, if the ancestral population is stable in size and at Hardy-Weinberg equilibrium, then the coalescence tree for a sample of alleles could be shorter than the coalescence tree for a similar sample in an expanding, nonequilibrium, derived population. The longer tree implies more opportunity for mutation, and given that mutation tends to increase allele size in maize, the result would be a larger average allele size in the derived population. This explanation implies that the formation of the derived population was not associated with a severe bottleneck. Other demographic scenarios could give the opposite outcome, i.e., a shorter coalescence tree for a derived population.
We have also observed a negative correlation between allele size and altitude in Mexico and North and South America that must have been independently derived given the known phylogeography of maize (Matsuoka et al. 2002b). Moreover, the strength of the correlation is similar in all three regions. There is an average decrease of 1.8 bp per locus per thousand meters elevation. This relationship represents a form of directional evolution. Accordingly, one can propose a set of explanations similar to those stated above. For example, at higher elevation, maize has a shorter generation time (fewer cell divisions). This is expected to result in a reduced mutation rate per generation. Given that mutations tend to increase the size of microsatellites, a lower mutation rate at high elevation is expected to yield a smaller average allele size.
In addition, there is a known negative correlation between genome size and altitude in maize (Poggio et al. 1998). Rayburn et al. (1985) have proposed that this correlation is due to selection for a smaller genome in short-seasoned environments, because a large genome would take longer to replicate at each cell division. To be effective for microsatellites, such selection should affect thousands of loci. With an average estimate of 58.2 dinucleotide microsatellites per Mbp (Morgante, Hanafey, and Powell 2002), a variance of 1.8 bp per locus per thousand meters corresponds to only 0.01% of the maize genome. This value is quite small compared to the genome size variation in heterochromatin of 36% for maize varieties (Poggio et al. 1998). Because variation in microsatellite size contributes very little to genome size variation in maize, it is difficult to imagine that selection is the driving force, although one cannot exclude the possibility that small differences may come under selection (Hughes and Hughes 1995).
A final point is that the occurrence of directional evolution for maize microsatellites cautions against using microsatellites nonchalantly for the estimation of population parameters. For example, the divergence time between maize populations can be estimated using the difference in the average allele size between populations (Wehrhahn 1975; Goldstein et al. 1995). However, directionality between populations in the evolution of microsatellite size will cause an upwardly biased estimate of the mean divergence between populations. Similarly, because of the relationship between mutation rate and the number of repeats, a mutation rate estimated using a population with high average size (e.g., North American maize) would likely give an overestimation of the mutation rate in maize (Amos et al. 1996). Accordingly, we urge caution when using microsatellite data for the estimation of population parameters in maize with simple mutational models. Because we were aware of the problem of directional evolution of maize microsatellites in geographically derived populations, we restricted our prior estimate of the maize-teosinte divergence time (Matsuoka et al. 2002b) to a comparison within a single environment (Mexico). Nevertheless, that estimate needs to be viewed with caution because the dynamics of microsatellite evolution in maize are not yet fully understood.
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Acknowledgements |
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Footnotes |
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Literature Cited |
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