@article{doi:10.1139/facets-2015-0007,
author = {Guncay, Ashley and Balasubramaniam, Thiropa and Plagens, Katie and Weadge, Joel and Long, Tristan A.F.},
title = {Cross-generational effects of male reproductive success and offspring immunocompetence in Drosophila melanogaster},
journal = {FACETS},
volume = {2},
number = {},
pages = {34-52},
year = {2017},
doi = {10.1139/facets-2015-0007},

URL = { 
    
        https://doi.org/10.1139/facets-2015-0007
    
    

},
eprint = { 
    
        https://doi.org/10.1139/facets-2015-0007
    
    

}
,
    abstract = { In some species where males make no direct contribution to a female’s lifetime reproductive success, females choose mates based on the indirect benefits manifested in their offspring. One trait that may be subject to this sexual selection is immunocompetence (the ability to mount an immune response following exposure to pathogens); however, the results of previous work on its link to male attractiveness have been ambiguous. Herein we examine the life history consequences of mating with males with a history of failure or success in reproductive competitions in Drosophila melanogaster. By examining egg-to-adult survival, body weights, and bacterial loads of offspring reared in either the absence or presence of a bacterial pathogen, we were able to examine whether sire reproductive success was associated with their offsprings’ ability to respond to an immunological challenge and other life history traits. Our results are partially consistent with the predictions of the “immunocompetence handicap hypothesis”: competitively successful males (“studs”) sire male offspring that are better able to handle an immunological challenge than those sired by competitively unsuccessful males (“duds”). However, our assay also revealed the opposite pattern in female offspring, suggestive of the complicating presence of alleles with sexually antagonistic effects on the expression of this important life history trait. }
}

    @article {,
    author = {Apidianakis Y},
    author = {Rahme LG},
    title = {Drosophila melanogaster as a model host for studying Pseudomonas aeruginosa infection},
    journal = {Nature Protocols},
    volume = {4},
    pages = {1285},
    year = {2009}
    }

    @article {,
    author = {Boman HG},
    author = {Nilsson I},
    author = {Rasmuson B},
    title = {Inducible antibacterial defence system in Drosophila},
    journal = {Nature},
    volume = {237},
    pages = {232},
    year = {1972}
    }

    @article {,
    author = {Chandler JA},
    author = {Lang JM},
    author = {Bhatnagar S},
    author = {Eisen JA},
    author = {Kopp A},
    title = {Bacterial communities of diverse Drosophila species: ecological context of a host–microbe model system},
    journal = {PLoS Genetics},
    volume = {7},
    pages = {e1002272},
    year = {2011}
    }

    @article {,
    author = {Chapman T},
    title = {A cost of mating with males that do not transfer sperm in female Drosophila melanogaster},
    journal = {Journal of Insect Physiology},
    volume = {38},
    pages = {223},
    year = {1992}
    }

    @article {,
    author = {Chapman T},
    title = {Seminal fluid‐mediated fitness traits in Drosophila},
    journal = {Heredity},
    volume = {87},
    pages = {511},
    year = {2001}
    }

    @article {,
    author = {Chippindale AK},
    author = {Alipaz JA},
    author = {Chen HW},
    author = {Rose MR},
    title = {Experimental evolution of accelerated development in Drosophila. 1. Developmental speed and larval survival},
    journal = {Evolution},
    volume = {51},
    pages = {1536},
    year = {1997}
    }

    @article {,
    author = {D’Argenio DA},
    author = {Gallagher LA},
    author = {Berg CA},
    author = {Manoil C},
    title = {Drosophila as a model host for Pseudomonas aeruginosa infection},
    journal = {Journal of Bacteriology},
    volume = {183},
    pages = {1466},
    year = {2001}
    }

    @article {,
    author = {Fedorka KM},
    author = {Mousseau TA},
    title = {Female mating bias results in conflicting sex-specific offspring fitness},
    journal = {Nature},
    volume = {429},
    pages = {65},
    year = {2004}
    }

    @article {,
    author = {Fellowes MDE},
    author = {Kraaijeveld AR},
    author = {Godfray HCJ},
    title = {Association between feeding rate and parasitoid resistance in Drosophila melanogaster},
    journal = {Evolution},
    volume = {53},
    pages = {1302},
    year = {1999}
    }

    @article {,
    author = {Folstad I},
    author = {Karter AJ},
    title = {Parasites, bright males, and the immunocompetence handicap},
    journal = {American Naturalist},
    volume = {139},
    pages = {603},
    year = {1992}
    }

    @article {,
    author = {Greenspan RJ},
    author = {Ferveur J-F},
    title = {Courtship in Drosophila},
    journal = {Annual Review of Genetics},
    volume = {34},
    pages = {205},
    year = {2000}
    }

    @article {,
    author = {Hall JC},
    title = {The mating of a fly},
    journal = {Science},
    volume = {264},
    pages = {1702},
    year = {1994}
    }

    @article {,
    author = {Hamilton WD},
    author = {Zuk M},
    title = {Heritable true fitness and bright birds: a role for parasites?},
    journal = {Science},
    volume = {218},
    pages = {384},
    year = {1982}
    }

    @article {,
    author = {Hihara F},
    title = {Effects of the male accessory gland secretion on oviposition and remating in females of Drosophila melanogaster},
    journal = {Zoological Magazine},
    volume = {90},
    pages = {307},
    year = {1981}
    }

    @article {,
    author = {Hoffmann JA},
    title = {The immune response of Drosophila},
    journal = {Nature},
    volume = {426},
    pages = {33},
    year = {2003}
    }

    @article {,
    author = {Holland B},
    author = {Rice WR},
    title = {Perspective: chase-away sexual selection: antagonistic seduction versus resistance},
    journal = {Evolution},
    volume = {52},
    pages = {1},
    year = {1998}
    }

    @article {,
    author = {Hosken DJ},
    title = {Sex and death: microevolutionary trade-offs between reproductive and immune investment in dung flies},
    journal = {Current Biology},
    volume = {11},
    pages = {R379},
    year = {2001}
    }

    @article {,
    author = {Houle D},
    title = {Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters},
    journal = {Evolution},
    volume = {45},
    pages = {630},
    year = {1991}
    }

    @article {,
    author = {Ingman-Baker J},
    author = {Candido EPM},
    title = {Proteins of the Drosophila melanogaster male reproductive system: two-dimensional gel patterns of proteins synthesized in the XO, XY, and XYY testis and paragonial gland and evidence that the Y chromosome does not code for structural sperm proteins},
    journal = {Biochemical Genetics},
    volume = {18},
    pages = {809},
    year = {1980}
    }

    @article {,
    author = {Kamimura Y},
    title = {Twin intromittent organs of Drosophila for traumatic insemination},
    journal = {Biology Letters},
    volume = {3},
    pages = {401},
    year = {2007}
    }

    @article {,
    author = {Khush RS},
    author = {Lemaitre B},
    title = {Genes that fight infection: what the Drosophila genome says about animal immunity},
    journal = {Trends in Genetics},
    volume = {16},
    pages = {442},
    year = {2000}
    }

    @article {,
    author = {Kirkpatrick M},
    author = {Ryan MJ},
    title = {The evolution of mating preferences and the paradox of the lek},
    journal = {Nature},
    volume = {350},
    pages = {33},
    year = {1991}
    }

    @article {,
    author = {Knell RJ},
    author = {Webberley KM},
    title = {Sexually transmitted diseases of insects: distribution, evolution, ecology and host behavior},
    journal = {Biological Reviews},
    volume = {79},
    pages = {557},
    year = {2004}
    }

    @article {,
    author = {Kokko H},
    author = {Jennions MD},
    author = {Brooks R},
    title = {Unifying and testing models of sexual selection},
    journal = {Annual Review of Ecology, Evolution, and Systematics},
    volume = {37},
    pages = {43},
    year = {2006}
    }

    @article {,
    author = {Kotiaho JS},
    author = {Simmons LW},
    author = {Hunt J},
    author = {Tomkins JL},
    title = {Males influence maternal effects that promote sexual selection: a quantitative genetic experiment with dung beetles Onthophagus taurus},
    journal = {American Naturalist},
    volume = {161},
    pages = {852},
    year = {2003}
    }

    @article {,
    author = {Kraaijeveld AR},
    author = {Godfray HCJ},
    title = {Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster},
    journal = {Nature},
    volume = {389},
    pages = {278},
    year = {1997}
    }

    @article {,
    author = {Kuijper B},
    author = {Stewart AD},
    author = {Rice WR},
    title = {The cost of mating rises nonlinearly with copulation frequency in a laboratory population of Drosophila melanogaster},
    journal = {Journal of Evolutionary Biology},
    volume = {19},
    pages = {1795},
    year = {2006}
    }

    @article {,
    author = {Lawniczak MK},
    author = {Barnes AI},
    author = {Linklater JR},
    author = {Boone JM},
    author = {Wigby S},
    author = {Chapman T},
    title = {Mating and immunity in invertebrates},
    journal = {Trends in Ecology \& Evolution},
    volume = {22},
    pages = {48},
    year = {2007}
    }

    @article {,
    author = {Lefranc A},
    author = {Bundgaard J},
    title = {The influence of male and female body size on copulation duration and fecundity in Drosophila melanogaster},
    journal = {Hereditas},
    volume = {132},
    pages = {243},
    year = {2000}
    }

    @article {,
    author = {Long TAF},
    author = {Montgomerie R},
    author = {Chippindale AK},
    title = {Quantifying the gender load: can population crosses reveal interlocus sexual conflict?},
    journal = {Philosophical Transactions of the Royal Society of London Series B},
    volume = {361},
    pages = {363},
    year = {2006}
    }

    @article {,
    author = {Long TAF},
    author = {Pischedda A},
    author = {Nichols RV},
    author = {Rice WR},
    title = {The timing of mating influences reproductive success in Drosophila melanogaster: implications for sexual conflict},
    journal = {Journal of Evolutionary Biology},
    volume = {23},
    pages = {1024},
    year = {2010}
    }

    @article {,
    author = {Long TAF},
    author = {Pischedda A},
    author = {Stewart AD},
    author = {Rice WR},
    title = {A cost of sexual attractiveness to high-fitness females},
    journal = {PLoS Biology},
    volume = {7},
    pages = {e1000254},
    year = {2009}
    }

    @article {,
    author = {Markow TA},
    author = {Quaid M},
    author = {Kerr S},
    title = {Male mating experience and competitive courtship success in Drosophila melanogaster},
    journal = {Nature},
    volume = {276},
    pages = {821},
    year = {1978}
    }

    @article {,
    author = {McKean KA},
    author = {Nunney L},
    title = {Sexual selection and immune function in Drosophila melanogaster},
    journal = {Evolution},
    volume = {62},
    pages = {386},
    year = {2008}
    }

    @article {,
    author = {Miest TS},
    author = {Bloch-Qazi MC},
    title = {Sick of mating: sexual transmission of a pathogenic bacterium in Drosophila melanogaster},
    journal = {Fly},
    volume = {2},
    pages = {215},
    year = {2008}
    }

    @article {,
    author = {Modak SG},
    author = {Satish KM},
    author = {Mohan J},
    author = {Dey S},
    author = {Raghavendra N},
    author = {Shakarad M},
    title = {A possible tradeoff between developmental rate and pathogen resistance in Drosophila melanogaster},
    journal = {Journal of Genetics},
    volume = {88},
    pages = {253},
    year = {2009}
    }

    @article {,
    author = {Mueller JL},
    author = {Page JL},
    author = {Wolfner MF},
    title = {An ectopic expression screen reveals the protective and toxic effects of Drosophila seminal fluid proteins},
    journal = {Genetics},
    volume = {175},
    pages = {777},
    year = {2007}
    }

    @article {,
    author = {Nunn CL},
    author = {Lindenfors P},
    author = {Pursall ER},
    author = {Rolff J},
    title = {On sexual dimorphism in immune function},
    journal = {Philosophical Transactions of the Royal Society of London Series B},
    volume = {364},
    pages = {61},
    year = {2009}
    }

    @article {,
    author = {Oneal E},
    author = {Connallon T},
    author = {Knowles LL},
    title = {Conflict between direct and indirect benefits of female choice in desert Drosophila},
    journal = {Biology Letters},
    volume = {3},
    pages = {29},
    year = {2007}
    }

    @article {,
    author = {Partridge L},
    author = {Hoffmann A},
    author = {Jones JS},
    title = {Male size and mating success in Drosophila melanogaster and D. pseudoobscura under field conditions},
    journal = {Animal Behaviour},
    volume = {35},
    pages = {468},
    year = {1987}
    }

    @article {,
    author = {Peng J},
    author = {Zipperlen P},
    author = {Kubli E},
    title = {Drosophila sex-peptide stimulates female innate immune system after mating via the Toll and Imd pathways},
    journal = {Current Biology},
    volume = {15},
    pages = {1690},
    year = {2005}
    }

    @article {,
    author = {Perry JC},
    author = {Harrison PW},
    author = {Mank JE},
    title = {The ontogeny and evolution of sex-biased gene expression in Drosophila melanogaster},
    journal = {Molecular Biology and Evolution},
    volume = {31},
    pages = {1206},
    year = {2014}
    }

    @article {,
    author = {Pischedda A},
    author = {Chippindale AK},
    title = {Intralocus sexual conflict diminishes the benefits of sexual selection},
    journal = {PLoS Biology},
    volume = {4},
    pages = {e356},
    year = {2006}
    }

    @article {,
    author = {Qvarnström A},
    author = {Brommer JE},
    author = {Gustafsson L},
    title = {Testing the genetics underlying the co-evolution of mate choice and ornament in the wild},
    journal = {Nature},
    volume = {441},
    pages = {84},
    year = {2006}
    }

    @article {,
    author = {Rolff J},
    title = {Bateman’s principle and immunity},
    journal = {Proceedings of the Royal Society of London Series B},
    volume = {269},
    pages = {867},
    year = {2002}
    }

    @article {,
    author = {Rolff J},
    author = {Kraaijeveld AR},
    title = {Selection for parasitoid resistance alters mating success in Drosophila},
    journal = {Proceedings of the Royal Society of London Series B},
    volume = {270},
    pages = {S154},
    year = {2003}
    }

    @article {,
    author = {Rolff J},
    author = {Siva-Jothy MT},
    title = {Invertebrate ecological immunology},
    journal = {Science},
    volume = {301},
    pages = {472},
    year = {2003}
    }

    @article {,
    author = {Rolff J},
    author = {Armitage SAO},
    author = {Coltman DW},
    title = {Genetic constraints and sexual dimorphism in immune defense},
    journal = {Evolution},
    volume = {59},
    pages = {1844},
    year = {2005}
    }

    @article {,
    author = {Rose MR},
    title = {Laboratory evolution of postponed senescence in Drosophila melanogaster},
    journal = {Evolution},
    volume = {38},
    pages = {1004},
    year = {1984}
    }

    @article {,
    author = {Rowe L},
    author = {Houle D},
    title = {The lek paradox and the capture of genetic variance by condition dependent traits},
    journal = {Proceedings of the Royal Society of London Series B},
    volume = {263},
    pages = {1415},
    year = {1996}
    }

    @article {,
    author = {Rundle HD},
    author = {Ödeen A},
    author = {Mooers AØ},
    title = {An experimental test for indirect benefits in Drosophila melanogaster},
    journal = {BMC Evolutionary Biology},
    volume = {7},
    pages = {36},
    year = {2007}
    }

    @article {,
    author = {Sheldon BC},
    author = {Verhulst S},
    title = {Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology},
    journal = {Trends in Ecology \& Evolution},
    volume = {11},
    pages = {317},
    year = {1996}
    }

    @article {,
    author = {Sirot LK},
    author = {Buehner NA},
    author = {Fiumera AC},
    author = {Wolfner MF},
    title = {Seminal fluid protein depletion and replenishment in the fruit fly, Drosophila melanogaster: an ELISA-based method for tracking individual ejaculates},
    journal = {Behavioral Ecology and Sociobiology},
    volume = {63},
    pages = {1505},
    year = {2009}
    }

    @article {,
    author = {Staubach F},
    author = {Baines JF},
    author = {Künzel S},
    author = {Bik EM},
    author = {Petrov DA},
    title = {Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment},
    journal = {PLoS ONE},
    volume = {8},
    pages = {e70749},
    year = {2013}
    }

    @article {,
    author = {van Lieshout E},
    author = {McNamara KB},
    author = {Simmons LW},
    title = {Rapid loss of behavioral plasticity and immunocompetence under intense sexual selection},
    journal = {Evolution},
    volume = {68},
    pages = {2550},
    year = {2014}
    }

    @article {,
    author = {van Noordwijk AJ},
    author = {de Jong G},
    title = {Acquisition and allocation of resources: their influence on variation in life history tactics},
    journal = {The American Naturalist},
    volume = {128},
    pages = {137},
    year = {1986}
    }

    @article {,
    author = {Vincent CM},
    author = {Gwynne DT},
    title = {Sex-biased immunity is driven by relative differences in reproductive investment},
    journal = {Proceedings of the Royal Society of London B: Biological Sciences},
    volume = {281},
    pages = {20140333},
    year = {2014}
    }

    @article {,
    author = {Vincent CM},
    author = {Sharp NP},
    title = {Sexual antagonism for resistance and tolerance to infection in Drosophila melanogaster},
    journal = {Proceedings of the Royal Society of London Series B},
    volume = {281},
    pages = {20140987},
    year = {2014}
    }

    @article {,
    author = {Westneat DF},
    author = {Birkhead TR},
    title = {Alternative hypotheses linking the immune system and mate choice for good genes},
    journal = {Proceedings of the Royal Society of London Series B},
    volume = {265},
    pages = {1065},
    year = {1998}
    }

    @article {,
    author = {Young JA},
    author = {Yourth CP},
    author = {Agrawal AF},
    title = {The effect of pathogens on selection against deleterious mutations in Drosophila melanogaster},
    journal = {Journal of Evolutionary Biology},
    volume = {22},
    pages = {2125},
    year = {2009}
    }

    @article {,
    author = {Zahavi A},
    title = {Mate selection—a selection for a handicap},
    journal = {Journal of Theoretical Biology},
    volume = {53},
    pages = {205},
    year = {1975}
    }

    @article {,
    author = {Zuk M},
    title = {Reproductive strategies and disease susceptibility: an evolutionary viewpoint},
    journal = {Parasitology Today},
    volume = {6},
    pages = {231},
    year = {1990}
    }