Balancing selection at a frog antimicrobial peptide locus: fluctuating immune effector alleles?
Balancing selection is common on many defense genes, but it has rarely been reported for immune effector proteins such as antimicrobial peptides (AMPs). We describe genetic diversity at a brevinin-1 AMP locus in three species of leopard frogs (Rana pipiens, Rana blairi, and Rana palustris). Several highly divergent allelic lineages are segregating at this locus. That this unusual pattern results from balancing selection is demonstrated by multiple lines of evidence, including a ratio of nonsynonymous/synonymous polymorphism significantly higher than 1, the ZnS test, incongruence between the number of segregating sites and haplotype diversity, and significant Tajima's D values. Our data are more consistent with a model of fluctuating selection in which alleles change frequencies over time than with a model of stable balancing selection such as overdominance. Evidence for fluctuating selection includes skewed allele frequencies, low levels of synonymous variation, nonneutral values of Tajima's D within allelic lineages, an inverse relationship between the frequency of an allelic lineage and its degree of polymorphism, and divergent allele frequencies among populations. AMP loci could be important sites of adaptive genetic diversity, with consequences for host-pathogen coevolution and the ability of species to resist disease epidemics.
Tennessen
Jacob A
JA
Department of Zoology, Oregon State University, OR, USA. tennessj@science.oregonstate.edu
Blouin
Michael S
MS
D000595:Amino Acid Sequence; D029845:Amphibian Proteins / Q000737:chemistry / Q000235:genetics* / Q000276:immunology*; D000818:Animals; D023181:Antimicrobial Cationic Peptides / Q000737:chemistry / Q000235:genetics* / Q000276:immunology*; D005787:Gene Frequency; D008969:Molecular Sequence Data; D011898:Ranidae / Q000145:classification / Q000276:immunology*; D016415:Sequence Alignment
D029845:Amphibian Proteins; D023181:Antimicrobial Cationic Peptides; C078413:brevinin-1 protein, Rana
J Wildl Dis. 2006 Apr;42(2):207-18
16870844
Genetics. 2004 Sep;168(1):425-34
15454554
Genetics. 1997 Oct;147(2):713-24
9335607
Heredity (Edinb). 2008 Jan;100(1):79-91
17987057
Heredity (Edinb). 2006 Jan;96(1):7-21
16094301
Biochim Biophys Acta. 2004 Jan 14;1696(1):1-14
14726199
Mol Phylogenet Evol. 2001 Sep;20(3):351-60
11527463
Genetics. 2007 Sep;177(1):481-500
17660536
Mol Phylogenet Evol. 2007 Nov;45(2):564-75
17689987
Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10539-44
12149450
Evolution. 2002 Oct;56(10):1902-8
12449477
Bioinformatics. 2001 Dec;17(12):1244-5
11751241
J Mol Evol. 2007 Nov;65(5):605-15
17938991
Mol Biol Evol. 2003 Jun;20(6):914-23
12716986
Genetics. 1990 Apr;124(4):967-78
2323559
Philos Trans R Soc Lond B Biol Sci. 1988 Jul 6;319(1196):541-55
2905491
BMC Evol Biol. 2008 Apr 16;8:113
18416833
Nat Genet. 2007 Dec;39(12):1461-8
17987029
Biochim Biophys Acta. 2000 Nov 30;1543(1):95-105
11087945
Genetics. 1997 Jul;146(3):1197-206
9215920
Nature. 1999 Aug 12;400(6745):667-71
10458161
Evolution. 2003 Aug;57(8):1707-22
14503614
J Evol Biol. 2005 Nov;18(6):1387-94
16313451
Virology. 2004 Jun 1;323(2):268-75
15193922
Ann N Y Acad Sci. 2002 Oct;969:323-39
12381613
Bioinformatics. 2003 Dec 12;19(18):2496-7
14668244
Dev Comp Immunol. 1999 Sep;23(6):459-72
10512457
Genetics. 1983 Nov;105(3):767-79
17246175
Evolution. 2004 Jan;58(1):145-59
15058727
Nature. 2003 May 1;423(6935):74-7
12721627
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6585-90
10841558
Mol Ecol. 2006 Aug;15(9):2627-41
16842432
Plant Cell. 2006 Aug;18(8):1803-18
16798885
J Mol Evol. 2005 Oct;61(4):445-55
16155748
Science. 2004 Mar 19;303(5665):1873-6
15031506
Peptides. 2008 Jul;29(7):1094-101
18440670
Trends Genet. 2006 Dec;22(12):662-70
17011664
Lancet Infect Dis. 2001 Oct;1(3):156-64
11871492
Dis Aquat Organ. 2005 Nov 9;67(1-2):9-14
16385802
Genetics. 1989 Nov;123(3):585-95
2513255
PLoS Genet. 2006 Apr;2(4):e64
16683038
Dev Comp Immunol. 2005;29(7):589-98
15784290
Oecologia. 2006 Jan;146(4):531-40
16205955
Eur J Biochem. 2000 Feb;267(3):894-900
10651828
Proc Natl Acad Sci U S A. 1999 Aug 17;96(17):9710-5
10449759