Effects of heterozygosity and MHC diversity on patterns of extra-pair paternity in the socially monogamous scarlet rosefinch

详细信息    查看全文

• 作者：J. C. Winternitz (1) (2) (7)
  M. Promerova (1) (3)
  R. Polakova (4)
  M. Vinker (4)
  J. Schnitzer (4)
  P. Munclinger (4)
  W. Babik (5)
  J. Radwan (6)
  J. Bryja (1)
  T. Albrecht (1) (4)
  
• 关键词：Extra ; pair copulation ; Mate choice ; Sexual selection ; Major histocompatibility complex ; Indirect benefits ; Erythrina erythrina
• 刊名：Behavioral Ecology and Sociobiology
• 出版年：2015
• 出版时间：March 2015
• 年：2015
• 卷：69
• 期：3
• 页码：459-469
• 全文大小：497 KB
• 参考文献：1. Aeschlimann P, H盲berli M, Reusch T, Boehm T, Milinski M (2003) Female sticklebacks / Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection. Behav Ecol Sociobiol 54:119鈥?26
  2. Agudo R, Carrete M, Alcaide M, Rico C, Hiraldo F, Don谩zar JA (2012) Genetic diversity at neutral and adaptive loci determines individual fitness in a long-lived territorial bird. Proc R Soc Lond B 279:3241鈥?249 CrossRef
  3. Ak莽ay E, Roughgarden J (2007) Extra-pair paternity in birds: review of the genetic benefits. Evol Ecol Res 9:855
  4. Albrecht T (2004) Edge effect in wetland-arable land boundary determines nesting success of scarlet rosefinches ( / Carpodacus erythrinus) in the Czech Republic. Auk 121:361鈥?71 CrossRef
  5. Albrecht T, Schnitzer J, Kreisinger J, Exnerov谩 A, Bryja J, Munclinger P (2007) Extrapair paternity and the opportunity for sexual selection in long-distant migratory passerines. Behav Ecol 18:477鈥?86 m001" target="_blank" title="It opens in new window">CrossRef
  6. Albrecht T, Vinkler M, Schnitzer J, Pol脕Kov脕 R, Munclinger P, Bryja J (2009) Extra-pair fertilizations contribute to selection on secondary male ornamentation in a socially monogamous passerine. J Evol Biol 22:2020鈥?030 j.1420-9101.2009.01815.x" target="_blank" title="It opens in new window">CrossRef
  7. Amos W, Wilmer JW, Fullard K, Burg T, Croxall J, Bloch D, Coulson T (2001) The influence of parental relatedness on reproductive success. Proc R Soc Lond B 268:2021鈥?027 CrossRef
  8. Arnqvist G, Kirkpatrick M (2005) The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behavior in females. Am Nat 165:S26鈥揝37 CrossRef
  9. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1鈥?, ject.org/package=lme4" class="a-plus-plus">http://CRAN.R-project.org/package=lme4
  10. Bollmer JL, Dunn PO, Freeman-Gallant CR, Whittingham LA (2012) Social and extra-pair mating in relation to major histocompatibility complex variation in common yellowthroats. Proc R Soc Lond B 279:4778鈥?785 CrossRef
  11. Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60鈥?5 CrossRef
  12. Brown JL, Eklund A (1994) Kin recognition and the major histocompatibility complex: an integrative review. Am Nat 143:435鈥?61 CrossRef
  13. Calcagno V, de Mazancourt C (2010) glmulti: an R package for easy automated model selection with (generalized) linear models. J Stat Softw 34:1鈥?9
  14. Coltman D, Slate J (2003) Microsatellite measures of inbreeding: a meta鈥恆nalysis. Evolution 57:971鈥?83 j.0014-3820.2003.tb00309.x" target="_blank" title="It opens in new window">CrossRef
  15. Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53:1259鈥?267 CrossRef
  16. Consuegra S, Garcia de Leaniz C (2008) MHC-mediated mate choice increases parasite resistance in salmon. Proc R Soc Lond B 275:1397鈥?403 CrossRef
  17. Croft DP, Madden JR, Franks DW, James R (2011) Hypothesis testing in animal social networks. Trends Ecol Evol 26:502鈥?07 j.tree.2011.05.012" target="_blank" title="It opens in new window">CrossRef
  18. David P, Pujol B, Viard F, Castella V, Goudet J (2007) Reliable selfing rate estimates from imperfect population genetic data. Mol Ecol 16:2474鈥?487 j.1365-294X.2007.03330.x" target="_blank" title="It opens in new window">CrossRef
  19. Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760鈥?72 j.1365-2435.2008.01467.x" target="_blank" title="It opens in new window">CrossRef
  20. Dunn PO, Bollmer JL, Freeeman鈥怗allant CR, Whittingham LA (2012) MHC variation is related to a sexually selected ornament, survival, and parasite resistance in common yellowthroats. Evolution 67:679鈥?87 j.1558-5646.2012.01799.x" target="_blank" title="It opens in new window">CrossRef
  21. Eliassen S, Kokko H (2008) Current analyses do not resolve whether extra-pair paternity is male or female driven. Behav Ecol Sociobiol 62:1795鈥?804 CrossRef
  22. Fitzpatrick JL, Evans JP (2009) Reduced heterozygosity impairs sperm quality in endangered mammals. Biol Lett 5:320鈥?23 CrossRef
  23. Forstmeier W (2007) Do individual females differ intrinsically in their propensity to engage in extra-pair copulations? PLoS ONE 2:e952 journal.pone.0000952" target="_blank" title="It opens in new window">CrossRef
  24. Fromhage L, Kokko H, Reid JM (2009) Evolution of mate choice for genome-wide heterozygosity. Evolution 63:684鈥?94 j.1558-5646.2008.00575.x" target="_blank" title="It opens in new window">CrossRef
  25. Gage M, Surridge A, Tomkins J, Green E, Wiskin L, Bell D, Hewitt G (2006) Reduced heterozygosity depresses sperm quality in wild rabbits, / Oryctolagus cuniculus. Curr Biol 16:612鈥?17 j.cub.2006.02.059" target="_blank" title="It opens in new window">CrossRef
  26. Garc铆a-Navas V, Ortego J, Sanz JJ (2009) Heterozygosity-based assortative mating in blue tits ( / Cyanistes caeruleus): implications for the evolution of mate choice. Proc R Soc Lond B 276:2931鈥?940 CrossRef
  27. Goudet J (2001) FSTAT, version 2.9.3, a program to estimate and test gene diversities and fixation indices. Lausanne University, Lausanne
  28. Griffith SC (2007) The evolution of infidelity in socially monogamous passerines: neglected components of direct and indirect selection. Am Nat 169:274鈥?81 CrossRef
  29. Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195鈥?212 j.1365-294X.2002.01613.x" target="_blank" title="It opens in new window">CrossRef
  30. Griggio M, Biard C, Penn D, Hoi H (2011) Female house sparrows 鈥渃ount on鈥?male genes: experimental evidence for MHC-dependent mate preference in birds. BMC Evol Biol 11:44 CrossRef
  31. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384鈥?87 CrossRef
  32. Herdegen M, Dudka K, Radwan J (2014) Heterozygosity and orange coloration are associated in the guppy ( / Poecilia reticulata). J Evol Biol 27:220鈥?25 jeb.12290" target="_blank" title="It opens in new window">CrossRef
  33. Hothorn T, Hornik K, van de Wiel MAV, Zeileis A (2008) Implementing a class of permutation tests: the Coin package. J Stat Softw 28:1鈥?3
  34. Hui W, Gel YR, Gastwirth JL (2008) lawstat: an R package for law, public policy and biostatistics. J Stat Softw 28:1鈥?6
  35. Ilmonen P, Stundner G, Thoss M, Penn DJ (2009) Females prefer the scent of outbred males: good-genes-as-heterozygosity? BMC Evol Biol 9:104 CrossRef
  36. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099鈥?106 j.1365-294X.2007.03089.x" target="_blank" title="It opens in new window">CrossRef
  37. Kempenaers B (2007) Mate choice and genetic quality: a review of the heterozygosity theory. Adv Study Behav 37:189鈥?78 CrossRef
  38. Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New York
  39. Konovalov DA, Manning C, Henshaw MT (2004) KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol Ecol Notes 4:779鈥?82 j.1471-8286.2004.00796.x" target="_blank" title="It opens in new window">CrossRef
  40. Milinski M (2006) The major histocompatibility complex, sexual selection, and mate choice. Ann Rev Ecol Evol Syst 37:159鈥?86 CrossRef
  41. Nowak MA, Tarczy-Hornoch K, Austyn JM (1992) The optimal number of major histocompatibility complex molecules in an individual. Proc Natl Acad Sci U S A 89:10896鈥?0899 CrossRef
  42. Pavlova A, Zink RM, Rohwer S (2005) Evolutionary history, population genetics, and gene flow in the common rosefinch ( / Carpodacus erythrinus). Mol Phylogenet Evol 36:669鈥?81 j.ympev.2005.02.010" target="_blank" title="It opens in new window">CrossRef
  43. Pol谩kov谩 R, Vysko膷ilov谩 M, Marton J-F, Mays HL, Hill GE, Bryja J, Albrecht T (2007) A multiplex set of microsatellite markers for the scarlet rosefinch ( / Carpodacus erythrinus). Mol Ecol Notes 7:1375鈥?378 j.1471-8286.2007.01892.x" target="_blank" title="It opens in new window">CrossRef
  44. Promerov谩 M, Vinkler M, Bryja J, Pol谩kov谩 R, Schnitzer J, Munclinger P, Albrecht T (2011) Occurrence of extra鈥恜air paternity is connected to social male鈥檚 MHC鈥恦ariability in the scarlet rosefinch / Carpodacus erythrinus. J Avian Biol 42:5鈥?0 j.1600-048X.2010.05221.x" target="_blank" title="It opens in new window">CrossRef
  45. Promerova M, Babik W, Bryja J, Albrecht T, Stuglik M, Radwan J (2012) Evaluation of two approaches to genotyping major histocompatibility complex class I in a passerine鈥擟E鈥怱SCP and 454 pyrosequencing. Mol Ecol Resour 12:285鈥?92 j.1755-0998.2011.03082.x" target="_blank" title="It opens in new window">CrossRef
  46. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution:258鈥?75
  47. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, ject.org/" class="a-plus-plus">http://www.R-project.org/
  48. Reid JM, Arcese P, Cassidy ALE, Marr AB, Smith JNM, Keller LF (2005) Hamilton and Zuk meet heterozygosity? Song repertoire size indicates inbreeding and immunity in song sparrows ( / Melospiza melodia). Proc R Soc Lond B 272:481鈥?87 CrossRef
  49. Reid JM, Arcese P, Keller LF (2006) Intrinsic parent鈥恛ffspring correlation in inbreeding level in a song sparrow ( / Melospiza melodia) population open to immigration. Am Nat 168:1鈥?3 CrossRef
  50. Reusch TBH, H盲berli MA, Aeschlimann PB, Milinski M (2001) Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414:300鈥?02 CrossRef
  51. Richardson DS, Komdeur J, Burke T, von Schantz T (2005) MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. Proc R Soc Lond B 272:759鈥?67 CrossRef
  52. Rubenstein DR (2007) Female extrapair mate choice in a cooperative breeder: trading sex for help and increasing offspring heterozygosity. Proc R Soc Lond B 274:1895鈥?903 CrossRef
  53. Sandberg M, Eriksson L, Jonsson J, Sj枚str枚m M, Wold S (1998) New chemical descriptors relevant for the design of biologically active peptides. A multivariate characterization of 87 amino acids. J Med Chem 41:2481鈥?491 jm9700575" target="_blank" title="It opens in new window">CrossRef
  54. Sepil I, Lachish S, Hinks AE, Sheldon BC (2013) Mhc supertypes confer both qualitative and quantitative resistance to avian malaria infections in a wild bird population. Proc R Soc Lond B 280:20130134 CrossRef
  55. Stjernberg T (1979) Breeding biology and population dynamics of the Scarlet Rosefinch / Carpodacus erythrinus. Acta Zool Fenn 157:1鈥?8
  56. Strandh M, Westerdahl H, Pontarp M, Canb盲ck B, Dubois M-P, Miquel C, Taberlet P, Bonadonna F (2012) Major histocompatibility complex class II compatibility, but not class I, predicts mate choice in a bird with highly developed olfaction. Proc R Soc Lond B 279:4457鈥?463 CrossRef
  57. Stuglik MT, Radwan J, Babik W (2011) jMHC: software assistant for multilocus genotyping of gene families using next-generation amplicon sequencing. Mol Ecol Resour 11:739鈥?42 j.1755-0998.2011.02997.x" target="_blank" title="It opens in new window">CrossRef
  58. Szulkin M, Bierne N, David P (2010) Heterozygosity-fitness correlations: a time for reappraisal. Evolution 64:1202鈥?217
  59. Tomkins JL, Radwan J, Kotiaho JS, Tregenza T (2004) Genic capture and resolving the lek paradox. Trends Ecol Evol 19:323鈥?28 j.tree.2004.03.029" target="_blank" title="It opens in new window">CrossRef
  60. Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013鈥?027 j.1365-294x.2000.00964.x" target="_blank" title="It opens in new window">CrossRef
  61. Van Oosterhout C, Trigg R, Carvalho G, Magurran A, Hauser L, Shaw P (2003) Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots. J Evol Biol 16:273鈥?81 j.1420-9101.2003.00511.x" target="_blank" title="It opens in new window">CrossRef
  62. Vinkler M, Schnitzer J, Munclinger P, Vot媒pka J, Albrecht T (2010) Haematological health assessment in a passerine with extremely high proportion of basophils in peripheral blood. J Ornithol 151:841鈥?49 CrossRef
  63. Westerdahl H, Asghar M, Hasselquist D, Bensch S (2012) Quantitative disease resistance: to better understand parasite-mediated selection on major histocompatibility complex. Proc R Soc Lond B 279:577鈥?84 CrossRef
  64. Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Ann Rev Ecol Evol Syst 34:365鈥?96 CrossRef
  65. Wetton JH, Carter RE, Parkin DT, Walters D (1987) Demographic study of a wild house sparrow population by DNA fingerprinting. Nature 327:147鈥?49 CrossRef
  66. Whitlock MC (2005) Combining probability from independent tests: the weighted Z-method is superior to Fisher鈥檚 approach. J Evol Biol 18:1368鈥?373 j.1420-9101.2005.00917.x" target="_blank" title="It opens in new window">CrossRef
  67. Zajitschek SRK, Lindholm AK, Evans JP, Brooks RC (2009) Experimental evidence that high levels of inbreeding depress sperm competitiveness. J Evol Biol 22:1338鈥?345 j.1420-9101.2009.01738.x" target="_blank" title="It opens in new window">CrossRef
  68. Zelano B, Edwards SV (2002) An MHC component to kin recognition and mate choice in birds: predictions, progress, and prospects. Am Nat 160:S225鈥揝237 CrossRef
  
• 作者单位：J. C. Winternitz (1) (2) (7)
  M. Promerova (1) (3)
  R. Polakova (4)
  M. Vinker (4)
  J. Schnitzer (4)
  P. Munclinger (4)
  W. Babik (5)
  J. Radwan (6)
  J. Bryja (1)
  T. Albrecht (1) (4)
  
  1. Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, v.v.i., Kv臎tn谩 8, 603 65, Brno, Czech Republic
  2. Institute of Botany, Academy of Sciences of the Czech Republic, v.v.i., Lidick谩 25/27, 657 20, Brno, Czech Republic
  7. Research Facility Studenec, Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Studenec 122, 675 02, Konesin, Czech Republic
  3. Department of Evolutionary Biology, Evolutionary Biology Center, Uppsala University, Norbyv盲gen 18D, 752 36, Uppsala, Sweden
  4. Department of Zoology, Faculty of Science, Charles University in Prague, Vinicna 7, 128 44, Prague 2, Czech Republic
  5. Institute of Environmental Sciences, Jagiellonian University, Gronostajowa 7, 30-387, Krakow, Poland
  6. Evolutionary Biology Group, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614, Poznan, Poland
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Behavioural Sciences
  Zoology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-0762

文摘

Extra-pair copulation without apparent direct benefits is an evolutionary puzzle that requires indirect fitness benefits to females to explain its ubiquity in socially monogamous mating systems. Using wild scarlet rosefinches (Carpodacus erythrinus), we tested if genetic benefits in the form of global (microsatellite) heterozygote advantage, adaptive genes (major histocompatibility complex), or complementary genes (using both markers) were responsible for female extra-pair mate choice, while considering that the benefits of mate choice may be conditional on female genotype. We found no evidence for assortative or relatedness-based mating (complementary genes), but higher MHC diversity, microsatellite heterozygosity, and condition were significantly related to male extra-pair paternity (EPP) success. In contrast, female probability of having extra-pair offspring decreased with increasing heterozygosity. Interestingly, extra-pair and within-pair males had higher heterozygosity than their female mates and extra-pair males had higher MHC supertype diversity. The only genetic difference between extra-pair and within-pair offspring was lower variance in MHC allelic diversity within extra-pair offspring, providing limited support for indirect genetic fitness benefits for the markers tested. Offspring had both higher neutral heterozygosity and number of MHC supertypes than adults, as well as significant identity disequilibrium, potentially suggesting that mates are chosen to increase offspring diversity in the period of the present study. Overall, our results point to an EPP heterozygote advantage for males, especially when involving less heterozygous females, and suggest that heterozygosity effects on reproduction may differ between the sexes.