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Paternal age and offspring growth: separating the intrinsic quality of young from rearing effects

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Abstract

Younger individuals are often less successful in reproduction than older ones. This might be because of improving breeding skills with age or because the genetic quality of young or early maternal effects on them vary with parental age. However, no attempt has been made to experimentally separate these processes in vertebrates. We conducted a cross-fostering experiment in collared flycatchers (Ficedula albicollis) in three breeding seasons to disentangle origin- and rearing-related effects of paternal age on chick growth, while controlling for date-specific environmental conditions as well as differences in clutch and brood size. The age of the male at the nest of origin, but not that of the rearing male, had a year-dependent effect on nestling body mass and tarsus length. In two seasons, young of subadult males grew slower in the early linear phase of growth than young of adult males. There was no compensatory growth in the final asymptotic phase, so both body mass and tarsus length before fledging reflected the differential early development. In the remaining year, the age of the male at the nest of origin had no significant effect on chick growth. The environment-dependent origin effect we detected was unexplained by incubation times, hatching asynchrony, chick masses at swapping or previously described age-dependent egg quality patterns. Our results therefore suggest a genotype × environment interaction on the relative development of offspring sired by subadult and adult males. Our results also raise the possibility that female birds may gain genetic benefits by mating with older males. Further studies should identify general patterns of male age-dependent female mate choice and offspring quality in different environmental conditions.

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References

  • Alatalo RV, Lundberg A, Glynn C (1986) Female pied flycatchers choose territory quality and not male characteristics. Nature 323:152–153

    Google Scholar 

  • van Balen JH, Booy CJH, van Franeker JA, Osieck ER (1982) Studies on hole-nesting birds in natural nest sites I. Availability and occupation of natural nest sites. Ardea 70:1–24

    Google Scholar 

  • Berrow SD, Humpidge R, Croxall JP (2000) Influence of adult breeding experience on growth and provisioning of wandering albatross Diomedea exulans chicks at South Georgia. Ibis 142:199–207

    Google Scholar 

  • Bize P, Roulin A, Bersier L-F, Pfluger D, Richner H (2003) Parasitism and developmental plasticity in Alpine swift nestlings. J Anim Ecol 72:633–639

    Google Scholar 

  • 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

    Google Scholar 

  • Bradley JS, Wooller RD, Skira IJ, Serventy DL (1989) Age-dependent survival of breeding short-tailed shearwaters Puffinus tenuirostris. J Anim Ecol 58:175–188

    Google Scholar 

  • Brandt CA (1984) Age and hunting success in the brown pelican: influences of skill and patch choice on foraging efficiency. Oecologia 62:132–137

    Google Scholar 

  • Brooks R, Kemp DJ (2001) Can older males deliver the good genes? Trends Ecol Evol 16:308–313

    PubMed  Google Scholar 

  • Cam E, Monnat J-Y (2000) Stratification based on reproductive state reveals contrasting patterns of age-related variation in demographic parameters in the kittiwake. Oikos 90:560–574

    Google Scholar 

  • Carranza J, Alarcos S, Sánchez-Prieto CB, Valencia J, Mateos C (2004) Disposable-soma senescence mediated by sexual selection in an ungulate. Nature 432:215–218

    PubMed  CAS  Google Scholar 

  • Cichon M (2003) Does prior breeding experience improve reproductive success in collared flycatcher females? Oecologia 134:78–81

    PubMed  Google Scholar 

  • Clutton-Brock TH (1988) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago

    Google Scholar 

  • Daunt F, Wanless S, Harris MP, Monaghan P (1999) Experimental evidence that age-specific reproductive success is independent of environmental effects. Proc R Soc Lond B 266:1489–1493

    Google Scholar 

  • Daunt F, Monaghan P, Wanless S, Harris MP, Griffiths R (2001) Sons and daughters: age-specific differences in parental rearing capacities. Funct Ecol 15:211–216

    Google Scholar 

  • David P, Bjorksten T, Fowler K, Pomiankowski A (2000) Condition-dependent signalling of genetic variation in stalk-eyed flies. Nature 406:186–188

    PubMed  CAS  Google Scholar 

  • DeForest LN, Gaston AJ (1996) The effect of age on timing of breeding and reproductive success in the thick-billed murre. Ecology 77:1501–1511

    Google Scholar 

  • Desrochers A (1992a) Age and foraging success in European blackbirds: variation between and within individuals. Anim Behav 43:885–894

    Google Scholar 

  • Desrochers A (1992b) Age-related differences in reproduction by European blackbirds: restraint or constraint? Ecology 73:1128–1131

    Google Scholar 

  • Desrochers A, Magrath RD (1993) Age-specific fecundity of European blackbirds (Turdus merula): individual and population trends. Auk 110:255–263

    Google Scholar 

  • Dhondt AA (1989) The effect of old age on the reproduction of great tits Parus major and blue tits Parus caeruleus. Ibis 131:268–280

    Google Scholar 

  • Dickinson JL (2001) Extrapair copulations in western bluebirds (Sialia mexicana): female receptivity favors older males. Behav Ecol Sociobiol 50:423–429

    Google Scholar 

  • Doligez B, Danchin E, Clobert J, Gustafsson L (1999) The use of conspecific reproductive success for breeding habitat selection in a non-colonial, hole-nesting species, the collared flycatcher. J Anim Ecol 68:1193–1206

    Google Scholar 

  • Doligez B, Danchin E, Clobert J (2002) Public information and breeding habitat selection in a wild bird population. Science 297:1168–1170

    PubMed  CAS  Google Scholar 

  • Engqvist L, Sauer KP (2002) A life-history perspective on strategic mating effort in male scorpionflies. Behav Ecol 13:632–636

    Google Scholar 

  • Enoksson B (1993) Effects of female age on reproductive success in European nuthatches breeding in natural cavities. Auk 110:215–221

    Google Scholar 

  • Enstrom DA (1993) Female choice for age-specific plumage in the orchard oriole: implications for delayed plumage maturation. Anim Behav 45:435–442

    Google Scholar 

  • Fair JM, Hansen ES, Ricklefs RE (1999) Growth, developmental stability, and immune response in juvenile Japanese quails (Coturnix coturnix japonica). Proc R Soc Lond B 266:1735–1742

    CAS  Google Scholar 

  • Fox CW, Bush ML, Wallin WG (2003) Maternal age affects offspring lifespan of the seed beetle, Callosobruchus maculatus. Funct Ecol 17:811–820

    Google Scholar 

  • Galbraith H, Hatch JJ, Nisbet ICT, Kunz TH (1999) Age-related changes in efficiency among breeding common terns Sterna hirundo: measurement of energy expenditure using doubly labelled water. J Avian Biol 30:85–96

    Google Scholar 

  • Garamszegi LZ, Török J, Michl G, Møller AP (2004) Female survival, lifetime reproductive success and mating status in a passerine bird. Oecologia 138:48–56

    PubMed  Google Scholar 

  • Gil D, Cobb JLS, Slater PJB (2001) Song characteristics are age dependent in the willow warbler, Phylloscopus trochilus. Anim Behav 62:689–694

    Google Scholar 

  • Gorman HE, Nager RG (2004) Prenatal developmental conditions have long-term effects on offspring fecundity. Proc R Soc Lond B 271:1923–1928

    Google Scholar 

  • Gray EM (1997) Female red-winged blackbirds accrue material benefits from copulating with extra-pair males. Anim Behav 53:625–639

    Google Scholar 

  • Green DJ (2001) The influence of age on reproductive performance in the brown thornbill. J Avian Biol 32:6–14

    Google Scholar 

  • Gustafsson L (1989) Collared flycatcher. In: Newton I (ed) Lifetime reproduction in birds. Academic, London, pp 75–88

    Google Scholar 

  • Gustafsson L, Pärt T (1990) Acceleration of senescence in the collared flycatcher Ficedula albicollis by reproductive costs. Nature 347:279–281

    Google Scholar 

  • Hamer KC, Furness RW (1991) Age-specific breeding performance and reproductive effort in great skuas Catharacta skua. J Anim Ecol 60:693–704

    Google Scholar 

  • Hargitai R, Török J, Tóth L, Hegyi G, Rosivall B, Szigeti B, Szöllősi E (2005) Effects of environmental conditions and parental quality on the inter- and intraclutch egg size variation in the collared flycatcher. Auk 122:509–522

    Google Scholar 

  • Harvey PH, Stenning MJ, Campbell B (1985) Individual variation in seasonal breeding success of pied flycatchers (Ficedula hypoleuca). J Anim Ecol 54:391–398

    Google Scholar 

  • Hegyi G, Török J, Tóth L, Garamszegi LZ, Rosivall B (2006) Rapid temporal change in the expression and age-related information content of a sexually selected trait. J Evol Biol 19(1):228-238

    PubMed  CAS  Google Scholar 

  • Hendry AP, Morbey YE, Berg OK, Wenburg JK (2004) Adaptive variation in senescence: reproductive lifespan in a wild salmon population. Proc R Soc Lond B 271:259–266

    Google Scholar 

  • Hepp GR, Kennamer RA (1993) Effects of age and experience on reproductive performance of wood ducks. Ecology 74:2027–2036

    Google Scholar 

  • Hipfner JM, Gaston AJ (2002) Growth of nestling thick-billed murres (Uria lomvia) in relation to parental experience and hatching date. Auk 119:827–832

    Google Scholar 

  • Jones TM, Balmford A, Quinnell RJ (2000) Adaptive female choice for middle-aged mates in a lekking sandfly. Proc R Soc Lond B 267:681–686

    CAS  Google Scholar 

  • Karubian J (2002) Costs and benefits of variable breeding plumage in the red-backed fairy-wren. Evolution 56:1673–1682

    PubMed  Google Scholar 

  • Kemp DJ (2002) Sexual selection constrained by life history in a butterfly. Proc R Soc Lond B 269:1341–1345

    Google Scholar 

  • Kempenaers B, Verheyen GR, Dhondt AA (1997) Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492

    Google Scholar 

  • Komers PE, Dhindsa MS (1989) Influence of dominance and age on mate choice in black-billed magpies: an experimental study. Anim Behav 37:645–655

    Google Scholar 

  • Korpimäki E (1988) Effects of age on breeding performance of Tengmalm’s owls Aegolius funereus in Western Finland. Ornis Scand 19:21–26

    Google Scholar 

  • Krokene C, Rigstad K, Dale M, Lifjeld JT (1998) The function of extrapair paternity in blue tits and great tits: good genes or fertility insurance? Behav Ecol 9:649–656

    Google Scholar 

  • Lepczyk CA, Karasov WH (2000) Effect of ephemeral food restriction on growth of house sparrows. Auk 117:164–174

    Google Scholar 

  • Lessells CM, Krebs JR (1989) Age and breeding performance of European bee-eaters. Auk 106:375–382

    Google Scholar 

  • 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

    Google Scholar 

  • Lindén M, Gustafsson L, Pärt T (1992) Selection on fledging mass in the collared flycatcher and the great tit. Ecology 73:336–343

    Google Scholar 

  • Lipar JL, Ketterson ED (2002) Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc R Soc Lond B 267:2005–2010

    Google Scholar 

  • Major RE, Christie FJ, Gowing G, Ivison TJ (1999) Age structure and density of red-capped robin populations vary with habitat size and shape. J Appl Ecol 36:901–908

    Google Scholar 

  • Mauck RA, Huntington CE, Grubb TC (2004) Age-specific reproductive success: evidence for the selection hypothesis. Evolution 58:880–885

    PubMed  CAS  Google Scholar 

  • Merilä J, Wiggins DA (1997) Mass loss in breeding blue tits: the role of energetic stress. J Anim Ecol 66:452–460

    Google Scholar 

  • Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    PubMed  Google Scholar 

  • Michl G, Török J, Péczely P, Garamszegi LZ, Schwabl H (2005) Female collared flycatchers adjust yolk testosterone to male age, but not to attractiveness. Behav Ecol 16:383–388

    Google Scholar 

  • Naef-Daenzer B, Widmer F, Nuber M (2001) Differential post-fledging survival of great and coal tits in relation to their condition and fledging date. J Anim Ecol 70:730–738

    Google Scholar 

  • Nager RG, van Noordwijk AJ (1995) Proximate and ultimate aspects of phenotypic plasticity in timing of great tit breeding in a heterogeneous environment. Am Nat 146:454–474

    Google Scholar 

  • Nol E, Smith JNM (1987) Effects of age and breeding experience on seasonal reproductive success in the song sparrow. J Anim Ecol 56:301–313

    Google Scholar 

  • Ollason JC, Dunnet GM (1978) Age, experience and other factors affecting breeding success of fulmar, Fulmarus glacialis, in Orkney. J Anim Ecol 47:961–976

    Google Scholar 

  • Olsson M, Shine R (1996) Does reproductive success increase with age or with size in species with indeterminate growth? A case study using sand lizards (Lacerta agilis). Oecologia 105:175–178

    Google Scholar 

  • Parish DMB, Thompson PS, Coulson JC (2001) Effects of age, cohort and individual on breeding performance in the lapwing Vanellus vanellus. Ibis 143:288–295

    Google Scholar 

  • Pärt T (1991) Philopatry and age as factors influencing reproductive success in the collared flycatcher (Ficedula albicollis). Ph.D. dissertation, University of Uppsala, Sweden

    Google Scholar 

  • Pärt T (1995) Does breeding experience explain increased reproductive success with age? An experiment. Proc R Soc Lond B 260:113–117

    Google Scholar 

  • Pärt T (2001a) Experimental evidence of environmental effects on age-specific reproductive success: the importance of resource quality. Proc R Soc Lond B 268:2267–2271

    Google Scholar 

  • Pärt T (2001b) The effect of territory quality on age-dependent reproductive performance in the northern wheatear, Oenanthe oenanthe. Anim Behav 62:379–388

    Google Scholar 

  • Pärt T, Gustafsson L, Moreno J (1992) ‘Terminal investment’ and a sexual conflict in the collared flycatcher (Ficedula albicollis). Am Nat 140:868–882

    Google Scholar 

  • Perrins CM, McCleery RH (1985) The effect of age and pair bond on the breeding success of great tits Parus major. Ibis 127:306–315

    Google Scholar 

  • Potti J (1998) Arrival time from spring migration in male pied flycatchers: individual consistency and familial resemblance. Condor 100:702–708

    Google Scholar 

  • Price DK, Hansen TF (1998) How does offspring quality change with age in male Drosophila melanogaster? Behav Genet 28:395–402

    PubMed  CAS  Google Scholar 

  • Pugesek BH (1981) Increased reproductive effort with age in the California gull (Larus californicus). Science 212:822–823

    PubMed  Google Scholar 

  • Pugesek BH (1984) Age-specific reproductive tactics in the California gull. Oikos 43:409–410

    Google Scholar 

  • Pugesek BH (1993) Chick growth in the California gull: relationships with hatching asynchrony and parental age. Colon Waterbirds 16:183–189

    Google Scholar 

  • Pyle P, Sydeman WJ, Hester M (2001) Effects of age, breeding experience, mate fidelity and site fidelity on breeding performance in a declining population of Cassin’s auklets. J Anim Ecol 70:1088–1097

    Google Scholar 

  • Qvarnström A, Sheldon BC, Pärt T, Gustafsson L (2003) Male ornamentation, timing of breeding, and cost of polygyny in the collared flycatcher. Behav Ecol 14:68–73

    Google Scholar 

  • Ratcliffe N, Furness RW, Hamer KC (1998) The interactive effects of age and food supply on the breeding ecology of great skuas. J Anim Ecol 67:853–862

    Google Scholar 

  • Reid JM, Bignal EM, Bignal S, McCracken DI, Monaghan P (2003) Identifying the demographic determinants of population growth rate: a case study of red-billed choughs Pyrrhocorax pyrrhocorax. J Anim Ecol 73:777–788

    Google Scholar 

  • Richardson DS, Burke T (1999) Extra-pair paternity in relation to male age in Bullock’s orioles. Mol Ecol 8:2115–2126

    PubMed  Google Scholar 

  • Rosivall B, Török J, Hasselquist D, Bensch S (2004) Brood sex ratio adjustment in collared flycatchers (Ficedula albicollis): results differ between populations. Behav Ecol Sociobiol 56:346–351

    Google Scholar 

  • Røskaft E, Espmark Y, Järvi T (1983) Reproductive effort and breeding success in relation to age in the rook Corvus frugilegus. Ornis Scand 14:169–174

    Google Scholar 

  • Sætre G-P, Dale S, Slagsvold T (1994) Female pied flycatchers prefer brightly coloured males. Anim Behav 48:1407–1416

    Google Scholar 

  • Sætre G-P, Fossnes T, Slagsvold T (1995) Food provisioning in the pied flycatcher: do females gain direct benefits by choosing bright-coloured males? J Anim Ecol 64:21–30

    Google Scholar 

  • Schwabl H (1996) Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol A 114:271–276

    CAS  Google Scholar 

  • Sheldon BC, Ellegren H (1999) Sexual selection resulting from extrapair paternity in collared flycatchers. Anim Behav 57:285–298

    PubMed  Google Scholar 

  • Sheldon BC, Merilä J, Qvarnström A, Gustafsson L, Ellegren H (1997) Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character. Proc R Soc Lond B 264:297–302

    Google Scholar 

  • Siikamäki P, Haimi J, Hovi M, Rätti O (1998) Properties of food loads delivered to nestlings in the pied flycatcher: effects of clutch size manipulation, year, and sex. Oecologia 115:579–585

    Google Scholar 

  • Slagsvold T, Sætre G-P (1991) Evolution of plumage color in male pied flycatchers (Ficedula hypoleuca): evidence for female mimicry. Evolution 45:910–917

    Google Scholar 

  • Smith HG (1993) Parental age and reproduction in the marsh tit Parus palustris. Ibis 135:196–201

    Google Scholar 

  • Smith HG, Ohlsson T, Wettermark KJ (1995) Adaptive significance of egg size in the European starling: experimental tests. Ecology 76:1–7

    Google Scholar 

  • Sorenson LG, Derrickson SR (1994) Sexual selection in the northern pintail (Anas acuta): the importance of female choice versus male–male competition in the evolution of sexually selected traits. Behav Ecol Sociobiol 35:389–400

    Google Scholar 

  • Stutchbury BJM, Piper WH, Neudorf DL, Tarof SA, Rhymer JM, Fuller G, Fleischer RC (1997) Correlates of extra-pair fertilization success in hooded warblers. Behav Ecol Sociobiol 40:119–126

    Google Scholar 

  • Sundberg J, Larsson C (1996) Male coloration as an indicator of parental quality in the yellowhammer, Emberiza citrinella. Anim Behav 48:885–892

    Google Scholar 

  • Svensson L (1992) Identification guide to European passerines. Stockholm

  • Sydeman WJ, Penniman JF, Penniman TM, Pyle P, Ainley DG (1991) Breeding performance in the western gull: effects of parental age, timing of breeding and year in relation to food availability. J Anim Ecol 60:135–149

    Google Scholar 

  • Török J, Tóth L (1988) Density-dependence in the collared flycatcher (Ficedula albicollis) at high population levels. J Anim Ecol 57:251–258

    Google Scholar 

  • Török J, Hegyi G, Garamszegi LZ (2003) Depigmented wing patch size is a condition-dependent indicator of viability in male collared flycatchers. Behav Ecol 14:382–388

    Google Scholar 

  • Török J, Hegyi G, Tóth L, Könczey R (2004) Unpredictable food supply modifies costs of reproduction and hampers individual optimization. Oecologia 141:432–443

    PubMed  Google Scholar 

  • Tremblay I, Thomas DW, Lambrechts MM, Blondel J, Perret P (2003) Variation in blue tit breeding performance across gradients in habitat richness. Ecology 84:3033–3043

    Google Scholar 

  • Veiga JP, Boto L (2000) Low frequency of extra-pair fertilizations in house sparrows breeding at high density. J Avian Biol 31:237–244

    Google Scholar 

  • Weathers WW, Sullivan BK (1989) Juvenile foraging proficiency, parental effort, and avian reproductive success. Ecol Monogr 59:223–246

    Google Scholar 

  • Weimerskirch H (1992) Reproductive effort in long-lived birds: age-specific patterns of condition, reproduction and survival in the wandering albatross. Oikos 64:464–473

    Google Scholar 

  • Wendeln H, Becker PH (1999) Effects of parental quality and effort on the reproduction of common terns. J Anim Ecol 68:205–214

    Google Scholar 

  • Wetton JH, Burke T, Parkin DT, Cairns E (1995) Single-locus DNA fingerprinting reveals that male reproductive success increases with age through extra-pair paternity in the house sparrow (Passer domesticus). Proc R Soc Lond B 260:91–98

    Google Scholar 

  • Yezerinac SM, Weatherhead PJ (1997) Extra-pair mating, male plumage coloration and sexual selection in yellow warblers (Dendroica petechia). Proc R Soc Lond B 264:527–532

    Google Scholar 

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Acknowledgements

We thank R. Hargitai, M. Herényi, G. Michl, B. Szigeti and E. Szöllősi for help with the fieldwork. We are grateful to A. Hettyey, J.-A. Nilsson, M. L. Leonard and two anonymous referees for constructive comments on the manuscript. This study was supported by OTKA (grant no. T34880), the Pilis Park Forestry, and the Erdők a Közjóért Alapítvány. The experiment we performed complies with the current laws of Hungary.

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Hegyi, G., Rosivall, B. & Török, J. Paternal age and offspring growth: separating the intrinsic quality of young from rearing effects. Behav Ecol Sociobiol 60, 672–682 (2006). https://doi.org/10.1007/s00265-006-0211-3

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