Abstract
In order to evaluate effects of the population structure and natural selection on organisms having long generation times, we surveyed DNA polymorphisms at five loci encoding 9-cis-epoxycarotenoid dioxygenase (NCED), ammonium transporter, calmodulin, aquaporin, and the second major allergen with polymethylgalacturonase enzyme activity in the pollen (Cryj2) in a conifer, Cryptomeria japonica. The average nucleotide diversity at silent sites across 12 loci including the previously analyzed seven loci was 0.0044. The population recombination rate (4Nr, where N and r are the effective population size and recombination rate per base per generation, respectively) was estimated as 0.00046 and a slow reduction in the population size was indicated, according to the maximum likelihood method implemented in LAMARC. At NCED, the McDonald-Kreitman (MK) test revealed an excess of replacement polymorphisms, suggesting contributions of slightly deleterious mutations. In contrast, the MK test revealed an excess of replacement divergence at Cryj2 and a maximum likelihood approach using the PAML package revealed that certain amino acid sites had a nonsynonymous/synonymous substitution rate ratio (ω) > 4.0, indicating adaptive evolution at this locus. The overall analysis of the 12 loci suggested that adaptive, neutral, and slightly deleterious evolution played important roles in the evolution of C. japonica.
Similar content being viewed by others
References
Aguade M (2001) Nucleotide sequence variation at two genes of the phenylpropanoid pathway, the FAH1 and F3H genes, in Arabidopsis thaliana. Mol Biol Evol 18:1–9
Baum J, Thomas AW, Conway DJ (2003) Evidence for diversifying selection on erythrocyte-binding antigens of Plasmodium falciparum and P. vivax. Genetics 163:1327–1336
Bergelson J, Kreitman M, Stahl EA, Tian D (2001) Evolutionary dynamics of plant R-genes. Science 292:2281–2285
Brown GR, Gill GP, Kuntz RJ, Langley CH, Neale DB (2004) Nucleotide diversity and linkage disequilibrium in loblolly pine. Proc Natl Acad Sci USA 101:15255–15260
Bustamante CD, Nielsen R, Sawyer SA, Olsen KM, Purugganan MD, Hartl DL (2002) The cost of inbreeding in Arabidopsis. Nature 416:531–534
Clark NL, Aagaard JE, Swanson WJ (2006) Evolution of reproductive protein from animals and plants. Reproduction 131:11–22
Fay JC, Wu CI (2000) Hitchhiking under positive Darwinian selection. Genetics 155:1405–1413
Fay JC, Wyckoff GJ, Wu CI (2002) Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature 415:1024–1026
Felsenstein J (2004) Inferring phylogenies. Sinauer Associates, Sunderland, MA
Fu YX, Li WH (1993) Statistical tests of neutrality of mutation. Genetics 133:693–709
Gadek PA, Alpers DL, Heslewood MM, Quinn CJ (2000) Relationships within Cupressaceae sensu lato: a combined morphological and molecular approach. Am J Bot 87:1044–1057
Gillespie JH (1989) Lineage effects and the index of dispersion of molecular evolution. Mol Biol Evol 6:636–647
González-Martínez SC, Krutovsky KV, Neale DB (2006) Forest-tree population genomics and adaptive evolution. New Phytol 170:227–238
Hamrick JL, Godt MJW (1990) Allozyme diversity in plant species. In: Brown AHD, Clegg MT, Kahler AL, Weir BS (eds) Plant population genetics, breeding and genetic resources. Sinauer Associates, Sunderland, MA, pp 43–63
Heuertz M, De Paoli E, Kallman T, Larsson H, Jurman I, Morgante M, Lascoux M, Gyllenstrand N (2006) Multilocus patterns of nucleotide diversity, linkage disequilibrium and demographic history of Norway spruce [Picea abies (L.) Karst]. Genetics 174:2095–2105
Hizume M, Kondo T, Shibata F, Ishizuka R (2001) Flow cytometric determination of genome size in the Taxodiaceae, Cupressaceae sensu stricto and Sciadopityaceae. Cytologia 66:307–311
Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014
Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159
Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583–589
Ingvarsson PK (2005) Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European aspen (Populus tremula L., Salicaceae). Genetics 169:945–953
Kado T, Yoshimaru H, Tsumura Y, Tachida H (2003) DNA Variation in a conifer, Cryptomeria japonica (Cupressaceae sensu lato). Genetics 164:1547–1559
Kado T, Ushio Y, Yoshimaru H, Tsumura Y, Tachida H (2006) Contrasting patterns of DNA variation in natural populations of closely related conifers, Cryptomeria japonica and Taxodium distichum (Cupressaceae sensu lato). Genes Genet Syst 81(2):103–113
Kuhner MK, Yamato J, Felsenstein J (1998) Macimum likelihood estimation of population growth rates base on the coalescent. Genetics 149:429–434
Kuhner MK, Yamato J, Felsenstein J (2000) Maximum likelihood estimation of recombination rates from population data. Genetics 156:1393–1401
Kuhner MK, Yamato J, Beerli P, Smith LP, Rynes E, Walkup E, Li C, Sloan J, Colacurcio P, Felsenstein J (2004) LAMARC v 1.2.1. University of Washington. Available at: http://evolution.gs.washington.edu/lamarc.html
Kusumi J, Tsumura Y, Yoshimaru H, Tachida H (2000) Phylogenetic relationships in Taxodiaceae and Cupressaceae sensu stricto based on matK gene, chlL gene, trnL-trnF IGS region, and trnL intron sequences. Am J Bot 87:1480–1488
Kusumi J, Tsumura Y, Yoshimaru H, Tachida H (2002) Molecular evolution of nuclear genes in Cupressaceae, a group of conifer trees. Mol Biol Evol 19:736–747
Krutovsky KV, Neale DB (2005) Nucleotide diversity and linkage disequilibrium in cold-hardiness- and wood quality-related candidate genes in Douglas fir. Genetics 171:2029–2041
Kvist L, Martens J, Nazarenko AA, Orell M (2003) Paternal leakage of mitochondrial DNA in the great tit (Parus major). Mol Biol Evol 20:243–247
McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654
Namba M, Kurose M, Torigoe K, Hino K, Taniguchi Y, Fukuda S, Usui M, Kutimoto M (1994) Molecular cloning of the second major allergen, Cry jII, from Japanese cedar pollen. FEBS Lett 353:124–128
Neale DB, Savolinen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:325–330
Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonuclease. Proc Natl Acad Sci USA 76:5269–5273
Nikaido AM, Ujino T, Iwata H, Yoshimura K, Yoshimaru H, Suyama Y, Murai M, Nagasaka K, Tsumura Y (2000) AFLP and CAPS linkage maps of Cryptomeria japonica. Theor Appl Genet 100:825–831
Nordborg M, Tina TH, Ishino Y et al (24 coauthors) (2005) The pattern of polymorphism in Arabidoposis thaliana. PLoS Biol 3(7):e196
Ohta T (1992) The nearly neutral theory of molecular evolution. Annu Rev Ecol Evol S 23:263–286
Ohta T (1995) Synonymous and nonsynonymous substitutions in mammalian genes and the nearly neutral theory. J Mol Evol 40:56–63
Ohtsuki T, Taniguchi Y, Kohno K, Fukuda S, Usui M, Kurimoto M (1995) Cry j 2, a major allergen of Japanese cedar pollen, shows polymethylgalacturonase activity. Allergy 50:483–488
Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100
Rozas J, JSánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
Smith NG, Eyre-Walker A (2002) Adaptive protein evolution in Drosophila. Nature 415:1022–1024
Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J (1999) Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400:667–671
Tachida H (2000) Molecular evolution in a multisite nearly neutral mutation model. J Mol Evol 50:69–81
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Takahara H (1998) Sugi-rin no hensen. In: Yasuda Y, Miyoshi N (eds) Nippon rettou syokusei-si. Asakura Shoten, Tokyo, pp 207–223 (in Japanese)
Takahashi T, Tani N, Taira H, Tsumura Y (2005) Microsatellite markers reveal high allelic variation in natural populations of Cryptomeria japonica near refugial areas of the last glacial period. J Plant Res 118:83–90
Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS (2001) Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci USA 98:9161–9166
Tomaru N, Tsumura Y, Ohba K (1994) Genetic variation and population differentiation in natural populations of Cryptomeria japonica. Plant Species Biol 9:191–199
Tsukada M (1982) Cryptomeria japonica: glacial refugia and late-glacial and postglacial migration. Ecology 63:1091–1105
Tsumura Y, Tomaru N (1999) Genetic diversity of Cryptomeria japonica using co-dominant markers based on sequenced-tagged sites. Theor Appl Genet 98:396–404
Tsumura Y, Kado T, Takahashi T, Tani N, Ujino-Ihara T, Iwata H (2007) Genome scan to detect genetic structure and adaptive genes of natural populations of Cryptomeria japonica. Genetics 176:2393–2403
Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556. Available at: http://abacus.gene.ucl.ac.uk/software/paml.html
Yu N, Jensen-Seaman MI, Chemnick L, Kidd JR, Deinard AS, Ryder O, Kidd KK, Li WH (2003) Low nucleotide diversity in chimpanzees and bonobos. Genetics 164:1511–1518
Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276
Wright SI, Gaut BS (2005) Molecular population genetics and the search for adaptive evolution. Mol Biol Evol 22(3):506–519
Zeng LW, Comeron JM, Chen B, Kreitman M (1998) The molecular clock revisited: the rate of synonymous vs. replacement change in Drosophila. Genetica 102(103):369–382
Acknowledgments
We thank Hitoshi Araki and two anonymous referees for helpful comments on the manuscript. This work was partially supported by Grants-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (nos. 16370101, 19370099).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Fujimoto, A., Kado, T., Yoshimaru, H. et al. Adaptive and Slightly Deleterious Evolution in a Conifer, Cryptomeria japonica . J Mol Evol 67, 201–210 (2008). https://doi.org/10.1007/s00239-008-9140-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-008-9140-2