Abstract
According to the differential investment hypothesis, females paired with attractive mates are expected to invest more in the current reproduction relative to females paired with unattractive males. We experimentally tested this hypothesis in the peafowl (Pavo cristatus) by providing females with males that differed in sexual attractiveness. In agreement with the differential allocation hypothesis, females paired with more ornamented males laid larger eggs, and deposited higher amounts of testosterone into the egg yolk, independently of the sex of the embryo. These results show that the association between paternal phenotype and offspring quality could arise via a differential maternal investment. They also suggest that, if ornamented males do transmit good genes to the progeny, the maternal differential investment can amplify the effect of such good genes on the offspring fitness.
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References
Able DJ (1996) The contagion indicator hypothesis for parasite-mediated sexual selection. Proc Natl Acad Sci USA 93:2229–2233
Andersson M (1994) Sexual selection. Princeton University Press, Princeton, NJ
Barber I, Arnott SA, Braithwaite VA, Andrew J, Huntingford FA (2001) Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proc R Soc Lond B 268:71–76
Blomqvist D, Johansson OC, Götmark F (1997) Parental quality and egg size affect chick survival in a precocial bird, the lapwing Vanellus vanellus. Oecologia 110:18–24
Borgia G, Collis K (1989) Female choice for parasite-free male satin bowerbirds and the evolution of bright male plumage. Behav Ecol Sociobiol 25:445–454
Burley N (1986) Sexual selection for aesthetic traits in species with biparental care. Am Nat 127:415–445
Burley N (1988) The differential allocation hypothesis: an experimental test. Am Nat 132:611–628
Carey C, Rahn H, Parisi P (1980) Calories, water, lipid and yolk in avian eggs. Condor 82:335–343
Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton, NJ
Colegrave N (2001) Differential allocation and ‘good genes’: male-manipulation. Trends Ecol Evol 16:22–23
Cunningham EJA, Russell AF (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404:74–76
Cunningham EJA, Russell AF (2001) Differential allocation and ‘good genes’: other explanations. Trends Ecol Evol 16:21
Doty GV, Welch AM (2001) Advertisement call duration indicates good genes for offspring feeding rate in gray tree frogs (Hyla versicolor). Behav Ecol Sociobiol 49:150–156
Eising CM, Eikenaar C, Schwabl H, Groothuis TG (2001) Maternal androgens in black headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond B 268:839–846
Eising CM, Müller W, Dijkstra C, Groothuis TGG (2003) Maternal androgens in egg yolks: relation with sex, incubation time and embryonic growth. Gen Comp Endocrinol 132:241–247
Elf PK, Fivizzani AJ (2002) Changes in sex steroid levels in yolks of the Leghorn chicken, Gallus domesticus, during embryonic development. J Exp Zool 293:594–600
Evans J, Kelley JL, Bisazza A, Finazzo E, Pilastro A (2004) Sire attractiveness influences offspring performance in guppies. Proc R Soc Lond B 271:2035–2042
Fernandes Martins TL (2004) Sex-specific growth rates in zebra finch nestlings: a possible mechanism for sex ratio adjustment. Behav Ecol 15:174–180
Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, Oxford, UK
Gadagkar R (2003) Is the peacock merely beautiful or also honest? Curr Sci 85:1012–1020
Gasparini J, McCoy KD, Haussy C, Tveraa T, Boulinier T (2001) Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla. Proc R Soc Lond B 268:647–650
Gil D, Graves J (2001) Differential allocation and ‘good genes’: pangloss once again. Trends Ecol Evol 16:21–22
Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128
Gil D, Leboucher G, Lacroix A, Cue R, Kreutzer M (2004) Females canaries produce eggs with greater amount of testosterone when exposed to preferred male song. Horm Behav 45:64–70
Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:475–518
Grindstaff JL, Brodie ED, Ketterson ED (2003) Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc R Soc Lond B 270:2309–2319
Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075
Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites. Science 218:384–387
Haq A-U, Bailey CA, Chinnah A (1996) Effect of β-carotene, canthaxanthin, lutein, and vitamin E on neonatal immunity of chicks when supplemented in broiler breeder diets. Poultry Sci 75:1092–1097
Höglund J, Alatalo RV (1995) Leks. Krebs JR, Clutton-Brock T, Princeton University Press, Princeton, NJ
Hoyt DF (1979) Practical methods for estimating volume and fresh weight of bird eggs. Auk 96:73–77
Iwasa Y, Pomiankowski A, Nee S (1991) The evolution of costly mate preferences. II. The “handicap” principle. Evolution 45:1431–1442
Jia F-Y, Greenfield MD (1997) When are good genes good? Variable outcomes of female choice in wax moths. Proc R Soc Lond B 264:1057–1063
Johnstone RA (1995) Sexual selection, honest advertisement and the handicap principle: reviewing the evidence. Biol Rev Camb Philos Soc 70:1–65
Kear J (1965) The internal food reserves of hatching Mallard ducklings. J Wildl Manage 29:523–528
Kirkpatrick M, Lande R (1989) The evolution of female characters. Evolution 43:485–503
Kokko H (2001) Fisherian and “good genes” benefits of mate choice: how (not) to distinguish between them. Ecol Lett 4:322–326
Kolm N (2001) Females produce larger eggs for large males in a paternal mouthbrooding fish. Proc R Soc Lond B 268:2229–2234
Lesna I, Sabelis MW (1999) Diet-dependent female choice for male with ‘good genes’ in a soil predatory mite. Nature 401:581–584
Limbourg T, Mateman AC, Andersson S, Lessells CM (2004) Female blue tits adjust parental effort to manipulated male UV attractiveness. Proc R Soc Lond B 271:1903–1908
Lipar JL, Ketterson ED (2000) Maternally derived yolk testosterone enhances the development of the hatching muscles in the red-winged blackbird Agelaius phoenicebus. Proc R Soc Lond B 267:2005–2010
Loyau A, Saint Jalme M, Sorci G (2005a) Intra- and intersexual selection for multiple traits in the peacock (Pavo cristatus). Ethology 111:810–820
Loyau A, Saint Jalme M, Cagniant C, Sorci G (2005b) Multiple sexual advertisement honestly reflect health status in peacocks (Pavo cristatus). Behav Ecol Sociobiol 58:552–557
Marshall RC, Leisler B, Catchpole CK, Schwabl H (2005) Male song quality affects circulating but not yolk steroid concentrations in female canaries (Serinus canaria). J Exp Biol 208:4493–4598
Mazuc J, Chastel O, Sorci G (2003) No evidence for differential maternal allocation to offspring in the house sparrow (Passer domesticus). Behav Ecol 14:340–346
Michl G, Török J, Péczely P, Garamszegi LZ, Schwabl H (2004) Female collared flycatchers adjust yolk testosterone to male age, but not to attractiveness. Behav Ecol 16:383–388
Møller AP, Thornhill R (1998) Male parental care, differential investment by females and sexual selection. Anim Behav 55:1507–1515
Møller AP, Alatalo RV (1999) Good-genes effects in sexual selection. Proc R Soc Lond B 266:85–91
Møller AP, Petrie M (2002) Condition dependence, multiple sexual signals, and immunocompetence in peacocks. Behav Ecol 13:248–253
Moore AJ (1994) Genetic evidence for the “good genes” process of sexual selection. Behav Ecol Sociobiol 35:235–241
Möstl E, Spendier H, Krotrschal K (2001) Concentration of immunoreactive progesterone and androgens in the yolk of hen’s egg (Gallus domesticus). Wien Tierärztl Mschr 88:62–65
Mousseau TA, Fox CW (1998) The adaptative significance of maternal effects. Trends Ecol Evol 13:403–407
Müller W, Groothuis TGG, Kasprzik A, Dijkstra C, Alatalo RV, Siitari H (2005) Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proc R Soc Lond B 272:1971–1977
Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:19–38
Palme R, Fischer P, Schildorfer H, Ismail MN (1996) Excretion of 14C-steroid hormones via faeces and urine in domestic livestock. Anim Reprod Sci 43:43–46
Parker TH (2003) Genetic benefits of mate choice separated from differential maternal investment in red junglefowl (Gallus gallus). Evolution 57:2157–2165
Petrie M (1994) Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 371:598–599
Petrie M, Williams A (1993) Peahens lay more eggs for peacocks with larger trains. Proc R Soc Lond B 251:127–131
Petrie M, Halliday T (1994) Experimental and natural changes in the peacock’s (Pavo cristatus) train can affect mating success. Behav Ecol Sociobiol 35:213–217
Petrie M, Halliday T, Sanders C (1991) Peahens prefer peacock with elaborate trains. Anim Behav 41:323–331
Petrie M, Schwabl H, Brande-Lavridsen N, Burke T (2001) Sex differences in avian yolk hormone levels. Nature 412:489
Pike TW, Petrie M (2005) Offspring sex ratio is related to paternal train elaboration and yolk corticosterone in peafowl. Biol Lett 1:204–207
Pilz KM, Adkins-Regan E, Schwabl H (2005) No sex difference in yolk steroid concentrations of avian eggs at laying. Biol Lett 1:318–321
Pomiankowski A, Iwasa Y (1998) Runaway ornament diversity caused by Fisherian sexual selection. Proc Natl Acad Sci USA 95:5106–5111
Pomiankowski A, Iwasa Y, Nee S (1991) The evolution of costly mate preferences. I. Fisher and biased mutation. Evolution 45:1422–1430
Price T, Schluter D, Heckman NE (1993) Sexual selection when the female directly benefits. Biol J Linn Soc 48:187–211
Promislow DEL, Smith EA, Pearse L (1998) Adult fitness consequences of sexual selection in Drosophila melanogaster. Proc Natl Acad Sci USA 95:10687–10692
Qvarström A, Price TD (2001) Maternal effects, paternal effects and sexual selection. Trends Ecol Evol 16:95–100
Rands MRW, Ridley MW, Lelliott AD (1984) The social organization of feral peafowl. Anim Behav 32:830–835
Rubolini D, Romano M, Martinelli R, Leoni B, Saino N (2006) Effects of prenatal yolk androgens on armaments and ornaments of the ring-necked pheasant. Behav Ecol Sociobiol 59:549–560
Rutstein AN, Gilbert L, Slater PJB, Graves J (2004) Mate attractiveness and primary resource allocation in the zebra finch. Anim Behav 68:1087–1094
Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R (2002a) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc R Soc Lond B 266:1729–1733
Saino N, Ferrari RP, Martinelli MR, Rubolini D, Møller AP (2002b) Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner. Proc R Soc Lond B 269:1005–1009
SAS (2001) SAS user’s guide: statistics. Release 8.2. SAS Institute, Cary, NC, USA
Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11449–11450
Schwabl H (1996) Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol 114:271–276
Sheldon BC (1993) Sexually transmitted disease in birds: occurrence and evolutionary significance. Phil Trans R Soc Lond B 339:491–497
Sheldon BC (2000) Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:397–402
Sheldon BC (2001) Response to: differential allocation and ‘good genes’. Trends Ecol Evol 16:23
Sheldon BC, Arponen H, Laurila A Crochet P-A, Merilä J (2003) Sire coloration influences offspring survival under predation risk in the moorfrog. J Evol Biol 16:1288–1295
Surai PF (2002) Selenium in poultry nutrition. 1. Antioxydant properties deficiency and toxicity. World´s Poultry Science Journal 58:333–347
Tanvez A, Béguin N, Chastel O, Lacroix A, Leboucher G (2004) Sexually attractive phrases increase yolk androgens deposition in Canaries (Serinus canaria). Gen Comp Endocrinol 138:113–120
Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027
Trivers RL (1972) Parental investment and sexual selection. In: Sexual selection and the descent of man. In: Campbell B (ed) Aldine, Chicago, pp 136–179
Trivers RL, Willard DE (1973) Natural selection of parental ability to vary sex-ratio of offspring. Science 179:90–92
von Engelhardt N, Carere C, Dijkstra C, Groothuis TGG (2006) Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches. Proc R Soc 273:65–70
Welch AM, Semlitsch RD, Gerhardt HC (1998) Call duration as an indicator of genetic quality in male gray tree frogs. Science 280:1928–1930
West SA, Sheldon BC (2002) Constraints in the evolution of sex ratio adjustment. Science 295:1685–1688
Williams T (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev 68:35–59
Williamson KA, Surai PF, Graves JA (2006) Yolk antioxidants and mate attractiveness in the Zebra Finch. Funct Ecol 20:354–359
Wolf JB, Brodie III ED, Cheverud JM, Moore AJ, Wade MJ (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13:64–69
Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214
Zeh JA, Zeh DW (1996) The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc R Soc Lond B 263:1711–1717
Zeh JA, Zeh DW (1997) The evolution of polyandry II: postcopulatory defences against genetic incompatibility. Proc R Soc Lond B 264:69–75
Acknowledgment
We thank Jarek Szczepaniak and the keepers for their help in catching the birds, Laetitia Girard and Camille Liaigre for their assistance in rearing the chicks, and Didier Catteville for his technical advice. Many thanks is due for all the people who adopted the chicks. We are very grateful to Tim Parker, Jeff Graves, and an anonymous referee who greatly improved this manuscript. This work was supported by the CNRS (ACI Jeunes Chercheurs to GS), MNHN, and Conseil Général de Seine Maritime. The experiment conducted herein complies with the current laws of the country in which it was performed.
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Loyau, A., Saint Jalme, M., Mauget, R. et al. Male sexual attractiveness affects the investment of maternal resources into the eggs in peafowl (Pavo cristatus). Behav Ecol Sociobiol 61, 1043–1052 (2007). https://doi.org/10.1007/s00265-006-0337-3
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DOI: https://doi.org/10.1007/s00265-006-0337-3