"Balancing" balancing selection? Assortative mating at the major histocompatibility complex despite molecular signatures of balancing selection

被引:6
作者
Slade, Joel W. G. [1 ]
Watson, Matthew J. [1 ]
MacDougall-Shackleton, Elizabeth A. [1 ]
机构
[1] Univ Western Ontario, Dept Biol, London, ON, Canada
来源
ECOLOGY AND EVOLUTION | 2019年 / 9卷 / 09期
基金
加拿大自然科学与工程研究理事会;
关键词
assortative mating; balancing selection; major histocompatibility complex; positive selection; song sparrows; trans-species polymorphism; AMINO-ACID SITES; II B GENE; MATE CHOICE; NO EVIDENCE; HETEROZYGOTE ADVANTAGE; ADAPTIVE EVOLUTION; NATURAL-SELECTION; MHC; POPULATION; ORIGIN;
D O I
10.1002/ece3.5087
中图分类号
Q14 [生态学(生物生态学)];
学科分类号
071012 ; 0713 ;
摘要
In vertebrate animals, genes of the major histocompatibility complex (MHC) determine the set of pathogens to which an individual's adaptive immune system can respond. MHC genes are extraordinarily polymorphic, often showing elevated nonsynonymous relative to synonymous sequence variation and sharing presumably ancient polymorphisms between lineages. These patterns likely reflect pathogen-mediated balancing selection, for example, rare-allele or heterozygote advantage. Such selection is often reinforced by disassortative mating at MHC. We characterized exon 2 of MHC class II, corresponding to the hypervariable peptide-binding region, in song sparrows (Melospiza melodia). We compared nonsynonymous to synonymous sequence variation in order to identify positively selected sites; assessed evidence for trans-species polymorphisms indicating ancient balancing selection; and compared MHC similarity of socially mated pairs to expectations under random mating. Six codons showed elevated ratios of nonsynonymous to synonymous variation, consistent with balancing selection, and we characterized several alleles similar to those occurring in at least four other avian families. Despite this evidence for historical balancing selection, mated pairs were significantly more similar at MHC than were randomly generated pairings. Nonrandom mating at MHC thus appears to partially counteract, not reinforce, pathogen-mediated balancing selection in this system. We suggest that in systems where individual fitness does not increase monotonically with MHC diversity, assortative mating may help to avoid excessive offspring heterozygosity that could otherwise arise from long-standing balancing selection.
引用
收藏
页码:5146 / 5157
页数:12
相关论文
共 79 条
[1]   BASIC LOCAL ALIGNMENT SEARCH TOOL [J].
ALTSCHUL, SF ;
GISH, W ;
MILLER, W ;
MYERS, EW ;
LIPMAN, DJ .
JOURNAL OF MOLECULAR BIOLOGY, 1990, 215 (03) :403-410
[2]  
[Anonymous], 2017, R LANG ENV STAT COMP
[3]   The nature of selection on the major histocompatibility complex [J].
Apanius, V ;
Penn, D ;
Slev, PR ;
Ruff, LR ;
Potts, WK .
CRITICAL REVIEWS IN IMMUNOLOGY, 1997, 17 (02) :179-224
[4]   MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? [J].
Bernatchez, L ;
Landry, C .
JOURNAL OF EVOLUTIONARY BIOLOGY, 2003, 16 (03) :363-377
[5]   Social and extra-pair mating in relation to major histocompatibility complex variation in common yellowthroats [J].
Bollmer, Jennifer L. ;
Dunn, Peter O. ;
Freeman-Gallant, Corey R. ;
Whittingham, Linda A. .
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2012, 279 (1748) :4778-4785
[6]   Extensive MHC Class II B Gene Duplication in a Passerine, the Common Yellowthroat (Geothlypis trichas) [J].
Bollmer, Jennifer L. ;
Dunn, Peter O. ;
Whittingham, Linda A. ;
Wimpee, Charles .
JOURNAL OF HEREDITY, 2010, 101 (04) :448-460
[7]   Complex Mhc-based mate choice in a wild passerine [J].
Bonneaud, C ;
Chastel, O ;
Federici, P ;
Westerdahl, H ;
Sorci, G .
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2006, 273 (1590) :1111-1116
[8]   Condition-dependent mate choice and a reproductive disadvantage for MHC-divergent male tiger salamanders [J].
Bos, David H. ;
Williams, Rod N. ;
Gopurenko, David ;
Bulut, Zafer ;
Dewoody, J. Andrew .
MOLECULAR ECOLOGY, 2009, 18 (15) :3307-3315
[9]   ORGAN-SPECIFIC AUTOIMMUNITY - A 1986 OVERVIEW [J].
BOTTAZZO, GF ;
TODD, I ;
MIRAKIAN, R ;
BELFIORE, A ;
PUJOLBORRELL, R .
IMMUNOLOGICAL REVIEWS, 1986, 94 :137-169
[10]   Heterozygosity-fitness correlation at the major histocompatibility complex despite low variation in Alpine ibex (Capra ibex) [J].
Brambilla, Alice ;
Keller, Lukas ;
Bassano, Bruno ;
Grossen, Christine .
EVOLUTIONARY APPLICATIONS, 2018, 11 (05) :631-644