Abstract
The diversity of functional genes and the related processes are important issues for conservation biology. This is especially relevant for populations that have suffered from demographic reduction as a consequence of the processes of postglacial colonization. In this perspective, the aims of the present study are (1) to quantify the genetic diversity of functional genes and (2) to disentangle the long- and short-term effects of natural selection that shapes genetic diversity from those of drift, mutation, and allopatric fragmentation. This research was conducted using an extensive genetic polymorphism analysis of populations of longnose dace (Rhinichthys cataractae) living over an area once covered by Pleistocene glaciations. The sequence and diversity of one exon of three genes (MHC IIβ, growth hormone, and trypsin) were jointly analyzed with non-coding nuclear loci from 27 populations; these populations were sampled over four major basins of northeastern North America. The survey revealed a surprisingly low allelic richness, especially for the MHC gene, considering the number of individuals and populations sampled. The results suggest that there is a complex mixture of different evolutionary processes shaping the level of polymorphism among longnose dace. While our study underlines the importance of the short-term effects of neutral processes and the major impact of post-glacial colonization on gene diversity, locally dependent balancing selection was detected on MHC. From this perspective, our results support an understanding of the importance of drift on functional gene diversity but also highlight the transient effects of natural selection on allelic composition, even in populations that show drastic reduction of genetic diversity.
References
Aguilar A, Garza JC (2006) A comparison of variability and population structure for major histocompatibility complex and microsatellite loci in California coastal steelhead (Oncorhynchus mykiss Walbaum). Mol Ecol 15:923–937
Aguilar A, Garza JC (2007) Patterns of historical balancing selection on the salmonid major histocompatibility complex class II β gene. J Mol Evol 65:34–43
Babik W, Pabijan M, Arntzen W, Cogalniceanu D, Durka W, Radwan J (2009) Long-term survival of a urodele amphibian despite depleted major histocompatibility complex variation. Mol Ecol 18:769–781
Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc Roy Soc B 263:1619–1626
Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377
Bernatchez L, Wilson C (1998) Comparative phylogeography of nearctic and palearctic fishes. Mol Ecol 7:431–452
Bryja J, Galan M, Charbonnel N, Cosson JF (2006) Duplication, balancing selection and trans-species evolution explain the high levels of polymorphism of the DQA MHC class II gene in voles (Arvicolinae). Immunogenetics 58:191–202
Campos JL, Posada D, Moran P (2006) Genetic variation at MHC, mitochondrial and microsatellite loci in isolated populations of Brown trout (Salmo trutta). Conserv Genet 7:515–530
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839
Excoffier L (2001) Analysis of population subdivision. In: Balding DJ, Bishop MJ, Cannings C (eds) Handbook of statistical genetics. Wiley, London, pp 271–308
Excoffier L (2006) Arlequin: an integrated software for population genetics data analysis Version 3.1. Distributed by the author, Computational and Molecular Population Genetics Lab, University of Berne, Bern. http://cmpg.unibe.ch/software/arlequin3/
Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180(2):977–993
Ford MJ (2002) Applications of selective neutrality tests to molecular ecology. Mol Ecol 11:1245–1262
Fraser BA, Neff BD (2009) MHC class IIB additive and non-additive effects on fitness measures in the guppy. J Fish Biol 75:2299–2312
Froeschke G, Sommer S (2005) MHC Class II DRB Variability and parasite load in the Stripped mouse (Rhabdomys pumilio) in the Southern Kalahari. Mol Biol Evol 22:1254–1259
Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709
Garrigan D, Edwards SV (1999) Polymorphism across an exon-intron boundary in an avian MHC class II B gene. Mol Biol Evol 16:1599–1606
Geweke J (1992) Evaluating the accuracy of sampling-based approaches to the calculation of posterior moments. In: Berger JO, Bernardo JM, Dawid AP, Smith AFM (eds) Bayesian statistics. Oxford University Press, New York, pp 169–194
Girard P, Angers B (2006a) Characterization of microsatellite loci in longnose dace (Rhinichthys cataractae) and interspecific amplification in five other Leuciscinae species. Mol Ecol Notes 6:69–71
Girard P, Angers B (2006b) The impact of post-glacial marine invasions on the genetic diversity of an obligate freshwater fish, the longnose dace (Rhinichthys cataractae), on the Quebec peninsula. Can J Fish Aquat Sci 63:1429–1438
Girard P, Angers B (2008) Assessment of power and accuracy of methods for detection and frequency-estimation of null alleles. Genetica 134:187–197
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices Version 2.9.3. Distributed by the author, Population genetics Lab, University of Lausanne, Lausanne. http://www2.unil.ch/popgen/softwares/fstat.htm
Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372
Hayashi K, Yoshida H, Nishida S, Goto M, Pastene LA, Kanda N, Baba Y, Koike H (2005) Genetic variation of the MHC DQB locus in the finless porpoise (Neophocaena phocaenoides). Zool Sci 23:147–153
Heath DD, Shrimpton JM, Hepburn RI, Jamieson SK, Brode S, Docker MF (2006) Population structure and divergence using microsatellite and gene locus markers in Chinook salmon (Oncorhynchus tshawytscha) populations. Can J Fish Aquat Sci 63:1370–1383
Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913
Hudson RR, Kreitman M, Aguadé M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159
Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167–170
Ingvarsson PK, Garcia MV, Hall D, Luquez V, Jansson S (2006) Clinal variation in phyB2, a candidate gene for day-length-induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula). Genetics 172:1845–1853
Landry C, Bernatchez L (2001) Comparative analysis of population structure across environments and geographical scales at major histocompatibility complex and microsatellite loci in Atlantic salmon (Salmo salar). Mol Ecol 10:2525–2539
Landry C, Garant D, Duchesne P, Bernatchez L (2001) ‘Good genes as heterozygosity’: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proc R Soc B 268:1279–1285
Langefors AH (2005) Adaptive and neutral genetic variation and colonization history of Atlantic salmon. Environ Biol Fishes 74:297–308
Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237
Mayer WE, O’hUigin C, Zaleska-Rutcynska Z, Klein J (1992) Trans-species origin of Mhc-DRB polymorphism in the chimpanzee. Immunogenetics 37:12–23
McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654
Miller KM, Kaukinen KH, Beacham TD, Withler RE (2001) Geographic heterogeneity in natural selection on an MHC locus in sockeye salmon. Genetica 111:237–257
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
O’Brien SJ, Yuhki N (1999) Comparative genome organization of the major histocompatibility complex: lessons from the Felidae. Immunol Rev 167:133–144
Ono H, O’Huigin C, Vincek V, Klein J (1993) Exon-intron organization of fish major histocompatibility complex class II beta genes. Immunogenetics 38:223–234
Orita M, Iwahana H, Kanazawa H, Hayashi K, Sekiya T (1989) Detection of polymorphisms of human DNA by gel electrophoresis as single-strand conformation polymorphism. Proc Natl Acad Sci USA 86:2766–2770
Otto SP (2000) Detecting the form of selection from DNA sequence data. Trends Genet 16:526–529
Ottovà E, Imkovà AT, Morand S (2007) The role of major histocompatibility complex diversity in vigour of fish males (Abramis brama L.) and parasite selection. Biol J Linnean Soc 90:525–538
Pamilo P, Nei M (1988) Relationships between gene trees and species trees. Mol Biol Evol 5:568–583
Peters MB, Turner TF (2008) Genetic variation of the major histocompatibility complex (MHC class II β gene) in the threatened Gila trout, Oncorhynchus gilae gilae. Conserv Genet 9:257–270
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
Sauermann U, Nurnberg P, Bercovitch FB, Berard JD, Trefilov A, Widdig A, Kessler M, Schmidtke J, Krawczak M (2001) Increased reproductive success of MHC class II heterozygous males among free-ranging rhesus macaques. Hum Genet 108:249–254
Schad J, Ganzhorn JU, Sommer S (2005) MHC constitution and parasite burden in the Malagasy mouse lemur, Microcebus murinus. Conserv Genet 5:299–309
Scott WB, Crossman EJ (1973) Freshwater fishes of Canada. Bulletin/Fisheries Research Board of Canada 184, Ottawa
Slade RW (1992) Limited MHC polymorphism in the southern elephant seal: implications for MHC evolution and marine mammal biology. Proc Roy Soc B 249:163–171
Smith BJ (2007) Boa: an R package for MCMC output convergence assessment and posterior inference. J Stat Softw 21(11):1–37
Suprunova T, Krugman T, Fahima T, Chen G, Shams I, Karol A, Nevo E (2004) Differential expression of dehydrin genes in wild barley, Hordeum spontaneum, associated with resistance to water deficit. Plant Cell Environ 27:1297–1308
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Takahata N (1989) Gene genealogy in three related populations: consistency probability between gene and population trees. Genetics 122:957–966
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
van Oosterhout C, Joyce DA, Cummings SM (2006) Evolution of MHC class IIB in the genome of wild and ornamental guppies, Poecilia reticulata. Heredity 97:111–118
Watterson GA (1978) The homozygosity test of neutrality. Genetics 88:405–417
Wegner KM (2008) Historical and contemporary selection of teleost MHC genes: did we leave the past behind? J Fish Biol 73:2110–2132
Acknowledgments
The authors wish to thank Kim-Pascale St-Pierre, Pascale Gibeau, Roland Vergilino, Isabelle Bouthillier, Isabelle Gaudet, Geneviève Roy, Simon Vervaet, and Bénédicte Poncet for the field and lab works. The authors are also grateful to Louis Bernatchez and two anonymous reviewers for their very helpful comments, and to Karyn Gray and Anna Lee-Popham for proofreading. This study was supported by an NSERC research grant to BA. PG was financially supported by the FQRNT, the Fonds Étienne-Magnin, the Faculté des Études Supérieure of Université de Montréal, and the Département des Sciences Biologiques.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Girard, P., Angers, B. The Functional Gene Diversity in Natural Populations over Postglacial Areas: The Shaping Mechanisms Behind Genetic Composition of Longnose Dace (Rhinichthys cataractae) in Northeastern North America. J Mol Evol 73, 45–57 (2011). https://doi.org/10.1007/s00239-011-9456-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-011-9456-1