Role of selection versus neutral processes determining genetic variation in a small mammal along a climatic gradient in southern Africa

Evolutionary Ecology

Volumn 28, Issue 6, 2014, Pages 1169-1190

  Froeschke, Götz ^a   Sommer, Simone ^a,b  

^a LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

^b UNIVERSITY OF ULM   (Germany)

Author keywords

Contemporary selection; Gastrointestinal helminths; MHC; Microsatellites; Rhabdomys pumilio; Small mammal; Southern Africa

Indexed keywords

CLIMATE EFFECT; ENVIRONMENTAL GRADIENT; GENE EXPRESSION; GENETIC VARIATION; POPULATION DISTRIBUTION; SMALL MAMMAL; TIMESCALE;

AFRICA;

MAMMALIA; RHABDOMYS PUMILIO; VERMES;

EID: 84912050546     PISSN: 02697653     EISSN: 15738477     Source Type: Journal    
DOI: 10.1007/s10682-014-9731-x     Document Type: Article

References (113)

1. 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
2. Alcaide M (2010) On the relative roles of selection and genetic drift in shaping MHC variation. Mol Ecol 19:3842–3844
3. Alcaide M, Edwards SV, Negro JJ, Serrano D, Tella JL (2008) Extensive polymorphism and geographical variation at a positively selected MHC class II B gene of the lesser kestrel (Falco naumanni). Mol Ecol 17:2652–2665
4. Alcaide M, Lemus JA, Tella JL, Serrano D, Negro JJ, Rodriguez A, Garcia-Montijano M (2010) MHC diversity and differential exposure to pathogen is kestrels (Aves: Falconidae). Mol Ecol 19:691–705
5. Anisimova M, Nielsen R, Yang Z (2003) Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164:1229–1236
6. ST-outlier method. BMC Bioinformatics 9:323
7. Babik WP, Taberlet MJ, Ejsmond MJ, Radwan J (2009) New generation sequencers as a tool for genotyping of highly polymorphic multilocus MHC system. Mol Ecol Resour 9:713–719
8. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B Biol Sci 263:1619–1626
9. 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
10. Biedrzycka A, Radwan J (2008) Population fragmentation and major histocompatibility complex variation in the spottet suslik, Spermophilus suslicus. Mol Ecol 17:4801–4811
11. Bierne N (2010) The distinctive footprints of local hitchhiking in a varied environment and global hitchhiking in a subdivided population. Evolution 64:3254–3272
12. Bierne N, Welch J, Loire E, Bonhomme F, David P (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol Ecol 20:2044–2072
13. Biswas S, Akey JM (2006) Genomic insights into positive selection. Trends Genet 22:437–446
14. Bondinas GP, Moustakas AK, Papadopoulos GK (2007) The spectrum of HLA-DQ and HLA-DR alleles, 2006: a listing correlating sequence and structure with function. Immunogenetics 59:539–553
15. Bonneaud C, Pérez-Tris J, Federici P, Chastel O, Sorci G (2006) Major histocompatibilty alleles associated with local resistance to malaria in a passerine. Evolution 60:383–389
16. Boyce WM, Hedrick PW, MuggliCockett NE et al (1997) Genetic variation of major histocompatibility complex and microsatellite loci: a comparison in bighorn sheep. Genetics 145(421):433
17. Brown JS, Kotler BP, Smith RJ, Wirtz II (1988) The effects of owl predation on the foraging behaviour of heteromyid rodents. Oecologia 76:408–415
18. Brown JH, Jardetzky TS, Gorga JC et al (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364:33–39
19. Bryja J, Charbonnel N, Berthier K, Galan M, Cosson J-F (2007) Density-related changes in selection pattern for major histocompatibility complex genes in fluctuating populations of voles. Mol Ecol 16:5084–5097
20. 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
21. Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631
22. Charbonnel N, Pemberton J (2005) A long-term genetic survey of an ungulate population reveals balancing selection acting on MHC through spatial and temporal fluctuations in selection. Heredity 95:377–388
23. Charlesworth B (1998) Measures of divergence between populations and the effect of forces that reduce variability. Mol Biol Evol 15:538–543
24. Charlesworth B, Nordborg M, Charlesworth D (1997) The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet Res 70:155–174
25. Clarke B, Kirby DR (1966) Maintenance of histocompatibility polymorphisms. Nature 211:999–1000
26. 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
27. Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509
28. De Graaff G (1981) The rodents of southern Africa. Butterworths, Durban
29. Deter J, Bryja J, Chaval Y et al (2008) Association between the DQA MHC class II gene and Puumala virus infection in Myodes glareolus, the bank vole. Infect Genet Evol 8:450–458
30. Dionne M, Miller KM, Dodson JJ, Caron F, Bernatchez L (2007) Clinal variation in MHC diversity with temperature: evidence for the role of host-pathogen interaction on local adaptation in Atlantic salmon. Evolution 61:2154–2164
31. Dionne M, Miller KM, Dodson JJ, Caron F, Bernatchez L (2009) MHC standing genetic variation and pathogen resistance in wild Atlantic salmon. Philos Trans R Soc B 364:1555–1565
32. Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256:50–52
33. du Toit N, van Vuuren BJ, Matthee S, Matthee C (2012) Biome specificity of distinct genetic lineages within the four-striped mouse Rhabdomys pumilio (Rodentia: Muridae) from southern Africa with implications for taxonomy. Mol Phylogenet Evol 65:75–86
34. Ejsmond MJ, Babik W, Radwan J (2010) MHC allele frequency distributions under parasite-driven selection: a simulation model. BMC Evol Biol 10:332
35. Ekblom R, Sæther SA, Jacobsson P et al (2007) Spatial pattern of MHC class II variation in the great snipe (Gallinago media). Mol Ecol 16:1439–1451
36. Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Popul Biol 3:87–112
37. Filip SD (1997) ABE unit conversion calculator. Agricultural and Biological Engineering, Mississippi State University, Mississippi
38. Fraser BA, Neff BD (2010) Parasite mediated homogenizing selection at the MHC in guppies. Genetica 138:273–278
39. Fraser BA, Ramnarine IW, Neff BD (2009) Selection at the MHC class IIB locus across guppy (Poecilia reticulata) populations. Heredity 104:155–167
40. Froeschke G, Sommer S (2005) MHC class II DRB variability and parasite load in the striped mouse (Rhabdomys pumilio) in the Southern Kalahari. Mol Biol Evol 22:1254–1259
41. Froeschke G, Sommer S (2012) Insights into the complex associations between MHC class II DRB polymorphism and multiple gastrointestinal parasite infestations in the striped mouse. PLoS ONE 7:e31820. doi:10.1371/journal.pone.0031820
42. Froeschke G, von der Heyden S (2014) A review of molecular approaches for investigating patterns of coevolution in marine host-parasite relationships. Adv Parasitol 84:209–252
43. Froeschke G, Harf R, Sommer S, Matthee S (2010) Effects of precipitation on parasite burden along a natural climatic gradient in southern Africa—implications for possible shifts in infestation patterns due to global changes. Oikos 119:1029–1039
44. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709
45. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318
46. Gockel J, Harr B, Schloetterer C, Arnold W, Gerlach G, Tautz D (1997) Isolation and characterization of microsatellite loci from Apodemus flavicollis (rodentia, muridae) and Clethrionomys glareolus (rodentia, cricetidae). Mol Ecol 6:597–599
47. Goslee SC, Urban D (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19
48. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices. Ver. 2.9.3. http://www.unil.ch/izea/softwares/fstat.html
49. Gutierrez-Espeleta GA, Hedrick PW, Kalinowski ST, Garrigan D, Boyce WM (2001) Is the decline of desert bighorn sheep from infectious disease the result of low MHC variation? Heredity 86:439–450
50. Hansen MM, Olivieri I, Waller DM, Nielsen EE, The GeM Working Group (2012) Monitoring adaptive genetic responses to environmental change. Mol Ecol 21:1311–1329
51. Harr B, Musolf K, Gerlach G (2000) Characterization and isolation of DNA microsatellite primers in wood mice (Apodemus sylvaticus, Rodentia). Mol Ecol 9:1664–1665
52. Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318
53. Hedrick PW (2002) Pathogen resistance and genetic variation at MHC loci. Evolution 56:1902–1908
54. Hedrick H (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638
55. Hedrick PW (2006) Genetic polymorphism in heterogeneous environments: the age of genomics. Annu Rev Ecol Evol Syst 27:67–93
56. Hill AVS (1991) HLA associations with malaria in Africa: some implications for MHC evolution. In: Klein J, Klein D (eds) Molecular evolution of the major histocompatibility complex. Springer, Berlin, pp 403–419
57. Hill RE, Hastie ND (1987) Accelerated evolution in the reactive center regions of serine protease inhibitors. Nature 326:96–99
58. Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164
59. Huges SL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167–170
60. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132
61. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241
62. Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New York
63. Kloch A, Babik W, Bajer A, Sinski E, Radwan J (2010) Effects of an MHC–DRB genotype and allele number on the load of gut parasites in the bank vole Myodes glareolus. Mol Ecol 18:255–265
64. Lamaze FC, Pavey SA, Normandeau E, Roy G, Garant D, Bernatchez L (2014) Neutral and selective processes shape MHC gene diversity and expression in stocked brook charr populations (Salvelinus fontinalis). Mol Ecol 7:1730–1748
65. Lancaster AK, Nelson MP, Meyer D, Single RM, Solberg OD (2007) PyPop update—a software pipeline for large-scale multilocus population genomics. Tissue Antigens 69:192–197
66. 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
67. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
68. Loiseau C, Zoorob R, Garnier S et al (2008) Antagonistic effects of a MHC class I allele on malaria-infected house sparrows. Ecol Lett 11:258–265
69. Loiseau C, Richard M, Garnier S, Chastel O, Julliard R, Zoorob R, Sorci G (2009) Diversifying selection on MHC class I in the house sparrow (Passer domesticus). Mol Ecol 18:1331–1340
70. Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Heridity 89:238–247
71. Makova KD, Patton JP, Krysanov EYU, Chesser RK, Baker RJ (1998) Microsatellite markers in wood mouse and striped field mouse (genus Apodemus). Mol Ecol 7:247–255
72. McCairns RJS, Bourget S, Bernatchez L (2011) Putative causes and consequences of MHC variation within and between locally adapted stickleback demes. Mol Ecol 20:486–502
73. McClelland EK, Ming TJ, Tabata A, Kaukinen KH, Beacham TD, Withler RE, Miller KM (2013) Patterns of selection and allele diversity of class I and class II major histocompatibility loci across the species range of sockeye salmon (Oncorhynchus nerka). Mol Ecol 22:4783–4800
74. Meirmans PG (2006) Using the AMOVA framework to estimate a standardised genetic differentiation measure. Evolution 60:2399–2402
75. Meyer-Lucht Y, Otten C, Püttker T, Sommer S (2008) Selection, diversity and evolutionary patterns of the MHC class II DAB in free-ranging Neotropical marsupials. BMC Genet 9:39
76. Morin PA, Leduc RG, Archer FI et al (2009) Significant deviations from Hardy–Weinberg equilibrium caused by low levels of microsatellite genotyping errors. Mol Ecol Resour 9:498–504
77. Neff BD, Fraser BA (2010) A program to compare genetic differentiation statistics across loci using resampling of individuals and loci. Mol Ecol Resour 10:546–550
78. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426
79. Ohnishi N, Ishibashi Y, Saitoh T, Aben S, Yoshida MC (1998) Polymorphic microsatellite DNA markers in the Japanese wood mouse Apodemus argenteus. Mol Ecol 7:1431–1439
80. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21
81. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
82. Radwan J, Biedrzycka A, Babik W (2009) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 3:537–544
83. Rambau RV, Robinson TJ, Stanyon R (2003) Molecular genetics of Rhabdomys pumilio subspecies boundaries: mtDNA phylogeography and karyotypic analysis by fluorescence in situ hybridization. Mol Phylogenet Evol 28:564–575
84. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249
85. Richman AD, Herrera LG, Nash D, Schierup MH (2003) Relative roles of mutation and recombination in generating allelic polymorphism at an MHC class II locus in Peromyscus maniculatus. Genet Res 82:89–99
86. Schad J, Sommer S, Ganzhorn JU (2004) MHC variability of a small lemur in the littoral forest fragments of southeastern Madagascar. Conserv Genet 5:199–209
87. Scherman K, Råberg L, Westerdahl H (2014) Positive selection on MHC Class II DRB and DQB genes in the bank vole (Myodes glareolus). J Mol Evol 78:293–305
88. Schierup MH (1998) The number of self-incompatibility alleles in a finite, subdivided population. Genetics 149:1153–1162
89. Schradin C (2005) When to live alone and when to live in groups: ecological determinants of sociality in the African striped mouse (Rhabdomys pumilio, Sparrman, 1784). Belg J Zool 135:77–82
90. Skinner D, Chimimba CT (2005) The mammals of the southern African subregion, 3rd edn. Cambridge University Press, Cambridge
91. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462
92. Smith KF, Acevedo-Whitehouse K, Pederson AB (2009) The role of infectious dieseases in biological conservation. Anim Conserv 12:1–12
93. Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16. doi:10.1186/1742-9994-2-16
94. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc Lond B Biol Sci 277:979–988
95. Strand TM, Segelbacher G, Quintela M, Xiao L, Axelsson T, Höglund J (2012) Can balancing selection on MHC loci counteract genetic drift in small fragmented populations of black grouse? Ecol Evol 2:341–353
96. Sutton JT, Nakagawa S, Robertson BC, Jamieson IG (2011) Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Mol Ecol 20:4408–4420
97. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
98. Tamura K, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
99. Taylor AC, Cooper DW (1998) Microsatellite markers for the phalangerid marsupial, the common brushtail possum (Trichosurus vulpecula). Mol Ecol 7:1780–1782
100. Tishkoff SA, Kidd KK (2004) Implications of biogeography of human populations for ‘race’ and medicine. Nat Genet 36:21–27
101. Tollenaere C, Bryja J, Galan M et al (2008) Multiple parasites mediate balancing selection at two MHC class II genes in the fossorial water vole: insights from multivariate analyses and population genetics. J Evol Biol 21:1307–1320
102. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
103. van Oosterhout C, Joyce DA, Cummings SA et al (2006) Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution 60:2562–2574
104. Vassilakos D, Natoli A, Dahlheim M, Hoelzel AR (2009) Balancing and directional selection at exon-2 of the MHC DQB1 locus among populations of odontocete cetaceans. Mol Biol Evol 26:681–689
105. Wahlund S (1928) Zusammensetzung von Populationen und Korrelationserscheinungen vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas 11:65–106
106. Westerdahl H, Hansson B, Bensch S, Hasselquist D (2004) Between-year variation of MHC allele frequencies in great reed warblers: selection or drift? J Evol Biol 17:485–492
107. Wong WSW, Yang Z, Goldman N, Nielsen R (2004) Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identification of positively selected sites. Genetics 168:1041–1051
108. Yang Z (1997) PAML: a program pachage for phylogenetic analysis by maximum likelihood. Cabios 13:555–556
109. Yang Z, Bielawski JP (2000) Statistical methods for detecting molecular adaption. TREE 15:496–503
110. Yang Z, Nielsen R, Goldman N, Pedersen A-MK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sides. Genetics 155:431–449
111. Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118
112. Zeng K, Shi S, Wu C-I (2007) Compound tests for the detection of hitchhiking under positive selection. Mol Biol Ecol 24:1898–1908
113. Zhang M, Hongxuan H (2013) Parasite-mediated selection of major histocompatibility complex variability in wild brandt’s voles (Lasiopodomys brandtii) from Inner Mongolia, China. BMC Evol Biol 13:149