Female partner preferences enhance offspring ability to survive an infection

BMC Evolutionary Biology

Dustin J Penn³  Friederike Winkelser³  Attila Hettyey¹  Michaela Thoß³  Kerstin E Thonhauser³  Sanja Sutalo³  Shirley Raveh² 

[1] Present address: “Lendület” Evolutionary Ecology Research Group, Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, Herman Ottó út 15, 1022 Budapest, Hungary;Present address: Department of Environmental Sciences Zoology and Evolution, University of Basel, Vesalgasse 1, 4051 Basel, Switzerland;Konrad Lorenz Institute of Ethology, Department of Integrative Biology and Evolution, University of Veterinary Medicine Vienna, Savoyenstr. 1a, 1160 Vienna, Austria

关键词: Tolerance;    Pathogen-mediated sexual selection;    Disease resistance;    Pathogen clearance;    Salmonella;    Mus musculus musculus;    Sexual selection;    Partner preference;   

Others  :  858079
DOI  :  10.1186/1471-2148-14-14

 received in 2013-10-11, accepted in 2014-01-02,  发布年份 2014

【 摘 要 】

Background

It is often suggested that mate choice enhances offspring immune resistance to infectious diseases. To test this hypothesis, we conducted a study with wild-derived house mice (Mus musculus musculus) in which females were experimentally mated either with their preferred or non-preferred male, and their offspring were infected with a mouse pathogen, Salmonella enterica (serovar Typhimurium).

Results

We found that offspring sired by preferred males were significantly more likely to survive the experimental infection compared to those sired by non-preferred males. We found no significant differences in the pathogen clearance or infection dynamics between the infected mice, suggesting that offspring from preferred males were better able to cope with infection and had improved tolerance rather than immune resistance.

Conclusion

Our results provide the first direct experimental evidence within a single study that partner preferences enhance offspring resistance to infectious diseases.

【 授权许可】

   
2014 Raveh et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Clutton-Brock T, McAuliffe K: Female mate choice in mammals. Q Rev Biol 2009, 84:3-27.
• [2]Jennions MD, Petrie M: Why do females mate multiply? A review of the genetic benefits. Biol Rev 2000, 75:21-64.
• [3]Zeh JA, Zeh DW: Reproductive mode and the genetic benefits of polyandry. Anim Behav 2001, 61:1051-1063.
• [4]Hettyey A, Hegyi G, Puurtinen M, Hoi H, Török J, Penn DJ: Mate choice for genetic benefits: time to put the pieces together. Ethology 2010, 116:1-9. 10.1111/j.1439-0310.2009.01704.x
• [5]Jennions MD, Kahn A, Kelly C, Kokko H: Meta-analysis and sexual selection: past studies and future possibilities. Evol Ecol 2012, 26:1119-1151. 10.1007/s10682-012-9567-1
• [6]Kotiaho JS, Puurtinen M: Mate choice for indirect genetic benefits: scrutiny of the current paradigm. Funct Ecol 2007, 21:638-644. 10.1111/j.1365-2435.2007.01286.x
• [7]Petrie M, Williams A: Peahens lay more eggs for peacocks with larger trains. Proc R Soc Lond B Biol Sci 1993, 251:127-131.
• [8]Petrie M, Halliday T, Sanders C: Peahens prefer peacocks with elaborate trains. Anim Behav 1991, 41:323-331.
• [9]Drickamer LC, Gowaty PA, Holmes CM: Free female mate choice in house mice affects reproductive success and offspring viability and performance. Anim Behav 2000, 59:371-378. 10.1006/anbe.1999.1316
• [10]Malo D, Skamene E: Genetic control of host resistance to infection. Trends Genet 1994, 10:365-371.
• [11]Hill AVS: The immunogenetics of human infectious diseases. Annu Rev Immunol 1998, 16:593-617.
• [12]Hurst LD, Smith NG: Do essential genes evolve slowly? Curr Biol 1999, 9:747-750.
• [13]Hamilton WD, Zuk M: Heritable true fitness and bright birds: a role for parasites? Science 1982, 218:384-386.
• [14]Folstad I, Karter AJ: Parasites, bright males, and the immunocompetence handicap. Am Nat 1992, 139:603-622.
• [15]Penn D, Potts W: The evolution of mating preferences and major histocompatibility genes. Am Nat 1999, 153:145-164. 10.1086/303166
• [16]Møller AP, Christe P, Lux E: Parasitism, host immune function, and sexual selection. Q Rev Biol 1999, 74(74):20-73.
• [17]Hamilton WJ, Poulin R: The Hamilton and Zuk hypothesis revisited: a meta-analytical approach. Behaviour 1997, 134:299-320.
• [18]Kavaliers M, Choleris E, Pfaff DW: Genes, odours and the recognition of parasitized individuals by rodents. Trends Parasitol 2005, 21:423-429.
• [19]Ehman KD, Scott M: Female mice mate preferentially with non-parasitized males. Parasitology 2002, 125:461-466. 10.1017}S003118200200224X
• [20]Penn D, Potts WK: Chemical signals and parasite-mediated sexual selection. Trends Ecol Evol 1998, 13:391-396. 10.1016/S0169-5347(98)01473-6
• [21]Zala SM, Potts WK, Penn DJ: Scent-marking displays provide honest signals of health and infection. Behav Ecol 2004, 15:338-344. 10.1093/beheco/arh022
• [22]Johnsen A, Andersen V, Sunding C, Lifjeld JT: Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 2000, 406:296-299.
• [23]Penn DJ: The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 2002, 108:1-21. 10.1046/j.1439-0310.2002.00768.x
• [24]Barber I, Arnott SA, Braithwaite VA, Andrew J, Huntingford FA: Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proc R Soc Lond B Biol Sci 2001, 268:71-76. 10.1098/rspb.2000.1331
• [25]Penn DJ, Damjanovich K, Potts WK: MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc Natl Acad Sci USA 2002, 99:11260-11264. 10.1073/pnas.162006499
• [26]Caron J, Loredo-Osti J, Laroche L, Skamene E, Morgan K, Malo D: Identification of genetic loci controlling bacterial clearance in experimental Salmonella enteritidis infection: an unexpected role of Nramp1 (Slc11a1) in the persistence of infection in mice. Genes Immun 2002, 3:196-204.
• [27]Mathur R, Oh H, Zhang D, Park SG, Seo J, Koblansky A, Hayden MS, Ghosh S: A mouse model of Salmonella typhi infection. Cell 2012, 151:590-602.
• [28]Roy MF, Malo D: Genetic regulation of host responses to Salmonella infection in mice. Genes Immun 2002, 3:381-393.
• [29]Burley N: The differential allocation hypothesis: an experimental test. Am Nat 1988, 132:612-628.
• [30]Harris WE, Uller T: Reproductive investment when mate quality varies: differential allocation versus reproductive compensation. Philos Trans R Soc Lond B Biol Sci 2009, 364:1039-1048.
• [31]Sheldon BC: Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 2000, 15:397-401.
• [32]Bluhm CK, Gowaty PA: Reproductive compensation for offspring viability deficits by female mallards, Anas platyrhynchos. Anim Behav 2004, 68:985-992.
• [33]Gowaty PA, Drickamer LC, Schmid-Holmes S: Male house mice produce fewer offspring with lower viability and poorer performance when mated with females they do not prefer. Anim Behav 2003, 65:95-103. 10.1006/anbe.2002.2026
• [34]Gowaty PA, Anderson WW, Bluhm CK, Drickamer LC, Kim YK, Moore AJ: The hypothesis of reproductive compensation and its assumptions about mate preferences and offspring viability. Proc Natl Acad Sci USA 2007, 104:15023-15027. 10.1073/pnas.0706622104
• [35]Johanns TM, Ertelt JM, Rowe JH, Way SS: Regulatory T cell suppressive potency dictates the balance between bacterial proliferation and clearance during persistent Salmonella infection. PLoS pathogens 2010, 6:e1001043.
• [36]Ilmonen P, Penn DJ, Damjanovich K, Morrison L, Ghotbi L, Potts WK: Major histocompatibility complex heterozygosity reduces fitness in experimentally infected mice. Genetics 2007, 176:2501-2508. 10.1534/genetics.107.074815
• [37]Ilmonen P, Penn DJ, Damjanovich K, Clarke J, Lamborn D, Morrison L, Ghotbi L, Potts WK: Experimental infection magnifies inbreeding depression in house mice. J Evol Biol 2008, 21:834-841. 10.1111/j.1420-9101.2008.01510.x
• [38]Schneider DS, Ayres JS: Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat Rev Immunol 2008, 8:889-895. 10.1038/Nri2432
• [39]Read AF, Graham AL, Råberg L: Animal defenses against infectious agents: is damage control more important than pathogen control. PLoS biology 2008, 6:e1000004.
• [40]Medzhitov R, Schneider DS, Soares MP: Disease tolerance as a defense strategy. Science 2012, 335:936-941.
• [41]Zala S, Potts W, Penn DJ: Exposing males to female scent increases the cost of controlling Salmonella infection in wild house mice. Behav Ecol Sociobiol 2008, 62:895-900. 10.1007/s00265-007-0513-0
• [42]Råberg L, Grahn M, Hasselquist D, Svensson E: On the adaptive significance of stress-induced immunosuppression. Proc R Soc Lond B 1998, 265:1637-1641.
• [43]Viney ME, Riley EM, Buchanan KL: Optimal immune responses: immunocompetence revisited. Trends Ecol Evol 2005, 20:665-669.
• [44]Westneat D, Birkhead T: Alternative hypotheses linking the immune system and mate choice for good genes. Proc R Soc Lond B Biol Sci 1998, 265:1065-1073. 10.1098/rspb.1996.0041 1471-2954
• [45]Blanchet S, Rey O, Loot G: Evidence for host variation in parasite tolerance in a wild fish population. Evol Ecol Res 2010, 24:1129-1139.
• [46]Råberg L, Sim D, Read AF: Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 2007, 318:812-814. 10.1126/science.1148526
• [47]Hõrak P, Tegelmann L, Ots I, Møller AP: Immune function and survival of great tit nestlings in relation to growth conditions. Oecologia 1999, 121:316-322.
• [48]Ilmonen P, Hakkarainen H, Koivunen V, Korpimäki E, Mullie A, Shutler D: Parental effort and blood parasitism in Tengmalm’s owl: effects of natural and experimental variation in food abundance. Oikos 1999, 86:79-86.
• [49]Moret Y, Schmid-Hempel P: Survival for immunity: the price of immune system activation for bumblebee workers. Science 2000, 290:1166-1168.
• [50]Merilä J, Andersson MS: Reproductive effort and success are related to haematozoan infections in blue tits. Ecoscience 1999, 6:421-428.
• [51]Adamo SA, Spiteri RJ: He’s healthy, but will he survive the plague? Possible constraints on mate choice for disease resistance. Anim Behav 2009, 77:67-78.
• [52]Rowe L, Houle D: The lek paradox and the capture of genetic variance by condition dependent traits. Proc R Soc Lond B Biol Sci 1996, 263:1415-1421.
• [53]Lorch PD, Proulx S, Rowe L, Day T: Condition-dependent sexual selection can accelerate adaptation. Evol Ecol Res 2003, 5:867-881.
• [54]Trivers RL, Willard DE: Natural selection of parental ability to vary sex-ratio of offspring. Science 1973, 179:90-92. 10.1126/science.179.4068.90
• [55]Medina E, Goldmann O, Rohde M, Lengeling A, Chhatwals GS: Genetic control of susceptibility to group A streptococcal infection in mice. J Infect Dis 2001, 184:846-852. 10.1086/323292
• [56]Poulin R, Forbes MR: Meta-analysis and research on host-parasite interactions: past and future. Evol Ecol 2012, 26:1169-1185.
• [57]Greenblatt HC, Diggs CL, Rosenstreich DL: Trypanosoma rhodesiense: analysis of the genetic control of resistance among mice. Infect Immun 1984, 44:107.
• [58]Grossman CJ: Interactions between the gonadal steroids and the immune system. Science 1985, 227:257-261.
• [59]Duckworth RA, Mendonca MT, Hill GE: A condition dependent link between testosterone and disease resistance in the house finch. Proc R Soc Lond B 2001, 268:2467-2472.
• [60]Roberts ML, Buchanan KL, Evans MR: Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 2004, 68:227-239. 10.1016/j.anbehav.2004.05.001
• [61]Kita EY, Yagyu Y, Nishikawa F, Hamuro A, Oku D, Emoto M, Katsui N, Kashiba S: Alterations of host resistance to mouse typhoid infection by sex hormones. J Leukoc Biol 1989, 46:538-546.
• [62]García-Gómez E, González-Pedrajo B, Camacho-Arroyo I: Role of sex steroid hormones in bacterial-host interactions. BioMed Res Int 2013, 2013:10. 928290
• [63]Grafen A, Hails R: Modern statistics for the life sciences. New York: Oxford University Press; 2002.
• [64]Engqvist L: The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 2005, 70:967-971.