Abstract
Maternal effects, such as investment in eggs, have profound effects on offspring fitness. Mothers are expected to skew their investment depending on the laying order and sex when unequal sibling competition occurs within a brood because of sex-specific vulnerability and age hierarchy caused by asynchronous hatching. The Bengalese finch hatches asynchronously and shows a moderate reversed sexual size dimorphism. However, contrary to commonly accepted assumptions of size-dependent vulnerability, the smaller sex (male) is more vulnerable to developmental stress caused by sibling competition. We investigated whether maternal investment would be biased by the position in laying order and the sex of eggs, and also explored the possible differences in growth patterns depending on sex, laying order, and age hierarchy by observing chicks fostered to experimentally manipulated broods where brood composition was controlled and age hierarchy was more enhanced than in natural breeding conditions. We found that overall patterns of maternal investment favored the disadvantageous sectors of sibling competition, i.e., eggs of later laying order and sons over those of early laying order and daughters. We also examined the effect of laying order on adult body size and sex differences in growth patterns. When reared in the subordinate age hierarchy, females could compensate for the deficit of decreased growth rate by taking longer to mature, whereas males could not. We suggest that this sex-specific growth pattern could be the cause of sex differences in vulnerability to early developmental stress.
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References
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723
Amundsen T, Stokland JN (1988) Adaptive significance of asynchronous hatching in the shag: a test of the brood reduction hypothesis. J Anim Ecol 57:329–344
Anderson DJ, Reeve J, Bird DM (1997) Sexually dimorphic eggs, nestling growth and sibling competition in American kestrels, Falco sparverius. Funct Ecol 11:331–335
Anderson DR, Burnham KP, Thompson WL (2000) Null hypothesis testing: problems, relevance, and an alternative. J Wildl Manage 64:912–923
Becker PHM, Wink MM (2003) Influences of sex, sex composition of brood and hatching order on mass growth in common terns, Sterna hirundo. Behav Ecol Sociobiol 54:136–146
Bernardo J (1996) The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Am Zool 36:216–236
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York, New York, USA
Clutton-Brock TH, Albon SD, Guinness FE (1985) Parental investment and sex differences in juvenile mortality in birds and mammals. Nature 313:131–133
Cockburn A, Legge S, Double MC (2002) Sex ratios in birds and mammals: can the hypotheses be disentangled? In: Hardy I (ed) The sex ratio handbook. Cambridge University Press, Cambridge, UK
Cordero PJ, Griffith SC, Aparicio JM, Parkin DT (2000) Sexual dimorphism in house sparrow eggs. Behav Ecol Sociobiol 48:353–357
Cordero PJ, Vinuela J, Aparicio JM, Veiga JP (2001) Seasonal variation in sex ratio and sexual egg dimorphism favouring daughters in first clutches of the spotless starling. J Evol Biol 14:829–834
Eising CM, Eikenaar C, Schwabl H, Groothuis TGG (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond B 268:839–846
Ellegren H (1996) First gene on the avian W chromosome (CHD) provides a tag for universal sexing of non-ratite birds. Proc Biol Sci 263:1635–1641
Forstmeier W, Coltman DW, Birkhead TR (2004) Maternal effects influence the sexual behavior of sons and daughters in the zebra finch. Evolution 58:2574–2583
Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128
Gilbert L, Rutstein AN, Hazon N, Graves JA (2005) Sex-biased investment in yolk androgens depends on female quality and laying order in zebra finches (Taeniopygia guttata). Naturwissenschaften 92:178–181
Godfray HCJ, Partridge L, Harvey PH (1991) Clutch size. Ann Rev Ecol Syst 22:409–429
Groothuis TG, Schwabl H (2002) Determinants of within- and among-clutch variation in levels of maternal hormones in black-headed gull eggs. Funct Ecol 16:281–289
Gwinner H, Schwabl H (2005) Evidence for sexy sons in European starling (Sturnus vulgaris). Behav Ecol Sociobiol 58:375–382
Hillström L (1999) Variation in egg mass in the pied flycatcher, Ficedula hypoleuca: an experimental test of the brood survival and brood reduction hypotheses. Evol Ecol Res 1:753–768
Hipkiss T, Hörnfeldt B, Eklund U, Berlin S (2002) Year-dependent sex-biased mortality in supplementary-fed Tengmalm’s owl nestlings. J Anim Ecol 71:693–699
Johnson DH (1999) The insignificance of statistical significance testing. J Wildl Manage 63:763–772
Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108
Kalmbach E, Furness RW, Griffiths R (2005) Sex-biased environmental sensitivity: natural and experimental evidence from a bird species with larger females. Behav Ecol 16:442–449
Krebs EA (1999) Last but not least: nestling growth and survival in asynchronously hatching crimson rosella. J Anim Ecol 68:266–281
Lindsey JK (1999) Models for repeated measurements. Oxford University Press, Oxford, UK
Lipar JL, Ketterson ED (2000) Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc Biol Sci 267:2005–2010
Lipar JL, Ketterson ED, Nolan V Jr (1999) Intraclutch variation in testosterone content of red-winged blackbird eggs. Auk 116:231–235
Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260
Magrath RD (1990) Hatching asynchrony in altricial birds. Biol Rev 65:587–622
Magrath RD (1992) Roles of egg mass and incubation pattern in establishment of hatching hierarchies in the blackbird (Turdus merula). Auk 109:474–487
Magrath MJL, Brouwer L, Komdeur J (2003) Egg size and laying order in relation to offspring sex in the extreme sexually size dimorphic brown songlark, Cinclorhamphus cruralis. Behav Ecol Sociobiol 54:240–248
Martin TE (1987) Food as a limit on breeding birds: a life-history perspective. Ann Rev Ecol Syst 18:453–487
Mead PS, Morton ML, Fish BE (1987) Sexual dimorphism in egg size and implications regarding facultative manipulation of sex in mountain white-crowned sparrows. Condor 89:798–803
Müller W, Kalmbach E, Eising CM, Groothuis TGG, Dijkstra C (2005) Experimentally manipulated brood sex ratios: growth and survival in the black-headed gull (Larus ridibundus), a sexually dimorphic species. Behav Ecol Sociobiol 59:313–320
Oddie KR (2000) Size matters: competition between male and female great tit offspring. J Anim Ecol 69:903–912
Okanoya K (2004) Song syntax in Bengalese finches: proximate and ultimate analyses. Adv Stud Behav 34:297–346
Okanoya K, Kimura T (1993) Acoustical and perceptual structures of sexually dimorphic distance calls in Bengalese finch. J Comp Psychol 107:386–394
Parker TH (2002) Maternal condition, reproductive investment, and offspring sex ratio in captive red jungle fowl (Gallus gallus). Auk 119:840–845
Petrie M, Schwabl H, Brande-Lavridsen N, Burke T (2001) Maternal investment. Sex differences in avian yolk hormone levels. Nature 412:498–499
Pilz KM, Smith HG, Sandell, MI, Schwabl H (2003) Interfemale variation in egg yolk androgen allocation in the European starling: do high-quality females invest more? Anim Behav 65:841–850
Pinheiro J, Bates M (2000) Mixed-effects models in S and S-PLUS. Springer, New York, NY, USA
Qvarnström A, Price TD (2001) Maternal effects, paternal effects and sexual selection. Trends Ecol Evol 16:95–100
R Development Core Team (2004) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org.
Råberg L, Stjernman M, Nilsson JÅ (2005) Sex and environmental sensitivity in blue tit nestlings. Oecologia 145:496–503
Reed WL, Vleck CM (2001) Functional significance of variation in egg-yolk androgens in the American coot. Oecologia 128:164–171
Ricklefs RE (1967) A graphical method of fitting equations to growth curves. Ecology 48:978–983
Royle NJ, Surai PF, Hartley IR (2001) Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav Ecol 12:381–385
Royle NJ, Surai PF, Hartley IR (2003) The effect of variation in dietary intake on maternal deposition of antioxidants in zebra finch eggs. Funct Ecol 17:472–481
Rutkowska J, Cichoń M (2002) Maternal investment during egg laying and offspring sex: an experimental study of zebra finches. Anim Behav 64:817–822
Rutkowska J, Cichoń M (2005) Egg size, offspring sex and hatching asynchrony in zebra finches Taeniopygia guttata. J Avian Biol 36:12–17
Rutkowska J, Wilk T, Cichoń M (2007) Androgen-dependent maternal effects on offspring fitness in zebra finches. Behav Ecol Sociobiol DOI 10.1007/s00265-007-0351-0
Rutstein AN, Gilbert L, Slater PJB, Graves JA (2005) Sex-specific patterns of yolk androgen allocation depend on maternal diet in the zebra finch. Behav Ecol 16:62–69
Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R (2002) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc R Soc Lond B 269:1729–1733
Schew WA, Ricklefs RE (1998) Developmental plasticity. In: Starck JM, Ricklefs RE (eds) Avian growth and development. Oxford University Press, New York, US, pp 288–304
Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450
Schwabl H (1996) Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol A 114:271–276
Schwabl H, Mock DW, Gieg JA (1997) A hormonal mechanism for parental favouritism. Nature 386:231
Sockman KW, Schwabl H (2000) Yolk androgens reduce offspring survival. Proc R Soc Lond B 267:1451–1456
Soma M, Hasegawa T, Okanoya K (2005) The evolution of song learning: a review from a biological perspective. Cogn Study 12:166–176
Soma M, Takahasi M, Ikebuchi M, Yamada H, Suzuki M, Hasegawa T, Okanoya K (2006) Early rearing conditions affect the development of body size and song in Bengalese finches. Ethology 112:1071–1078
Williams TD (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev 68:35–59
Acknowledgments
We thank the members of the Biolinguistics team for the help in maintaining the birds and the members of National Science Museum, Tokyo for helping with laboratory work. We are also deeply grateful to two anonymous referees and to Nobuyuki Kutsukake and Yoshimasa Seki for the helpful comments on this manuscript. This work was financially supported by a JSPS Research Fellowship for Young Scientists. The experiment was performed under proper legislation by Japanese law.
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Soma, M., Saito, D.S., Hasegawa, T. et al. Sex-specific maternal effect on egg mass, laying order, and sibling competition in the Bengalese finch (Lonchura striata var. domestica). Behav Ecol Sociobiol 61, 1695–1705 (2007). https://doi.org/10.1007/s00265-007-0400-8
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DOI: https://doi.org/10.1007/s00265-007-0400-8