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Interaction between maternal effects: onset of incubation and offspring sex in two populations of a passerine bird

  • Population Ecology
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Abstract

Maternal phenotype and maternal environment can profoundly affect the phenotype and fitness of offspring. Yet the causes of variation in such maternal effects are rarely known. Embryos in avian eggs cannot develop without being incubated and this creates an opportunity for maternal control of duration and onset of offspring development. However, females might adjust the start of incubation (e.g., coincident with the first egg or delayed until after egg-laying) in response to environmental conditions that they experience at the time of breeding. We studied two populations of the house finch (Carpodacus mexicanus) that breed at the climatic extremes of the species' geographical range (Montana and Alabama) and found that in both populations, the timing of incubation onset was closely associated with the bias in the sequence in which male and female eggs were laid within a clutch. When females started incubation with the first egg, they produced sons and daughters in highly biased sequence, when females delayed the onset of incubation until after the egg-laying, the sequence of sons and daughters was not biased. Because in both populations, onset of incubation was associated with the ambient temperature, these results emphasize that maternal effects on offspring can be influenced by ecological conditions experienced by parental generation.

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References

  • Albrecht DJ (2000) Sex ratio manipulation within broods of house wrens, Troglodytes aedon. Anim Behav 59:1227–1234

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Badyaev AV (2002) Male and female growth in sexually dimorphic species: Harmony, conflict, or both? Comments Theor Biol 7:10–33

    Google Scholar 

  • Badyaev AV, Hill GE (2000) The evolution of sexual dimorphism in the house finch. I. Population divergence in morphological covariance structure. Evolution 54:1784–1794

    CAS  PubMed  Google Scholar 

  • Badyaev AV, Hill GE, Whittingham LA (2001) The evolution of sexual size dimorphism in the house finch: IV. Population divergence in ontogeny of dimorphism. Evolution 55:2534–2549

    CAS  PubMed  Google Scholar 

  • Badyaev AV, et al. (2002) Sex-biased hatching order and adaptive population divergence in a passerine bird. Science 295:316–318

    Article  CAS  PubMed  Google Scholar 

  • Badyaev AV, Beck ML, Hill GE, Whittingham LA (2003) The evolution of sexual size dimorphism in the house finch: V. Maternal effects. Evolution 57 (in press)

    Google Scholar 

  • Bernardo J (1996) Maternal effects in animal ecology. Am Zool 36:83–105

    Google Scholar 

  • Blanco G, Dávila JA, López Septiem JA, Rodríguez R, Martínez F (2002) Sex-biased initial eggs favour sons in the slightly size-dimorphic Scops owl (Otus scops). Biol J Linn Soc 76:1–7

    Article  Google Scholar 

  • Bortolotti GR (1986) Influence of sibling competition on nestling sex ratios of sexually dimorphic birds. Am Nat 127:495–507

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Crisostomo S, Guemene D, Garreau-Mills M, Morvan C, Zadworny D (1998) Prevention of incubation behavior expression in turkey hens by active immunization against prolactin. Theriogenology 50:675–690

    Article  CAS  PubMed  Google Scholar 

  • Daan S, Dijkstra C, Weissing FJ (1996) An evolutionary explanation for seasonal trends in avian sex ratio. Behav Ecol 7:426–430

    Google Scholar 

  • Eising CM, Eikenaar C, Schwabl H, Groothuis GG (2001) Maternal antrogens in black-headed gull (Larus ridibunus) eggs: consequences for chick development. Proc R Soc Biol Sci Ser B 268:839–846

    Article  CAS  Google Scholar 

  • Fairbanks LA (1996) Individual differences in maternal style: Causes and consequences for mothers and offspring. Adv Stud Behav 25:579–611

    Google Scholar 

  • Fear KK, Price T (1998) The adaptive surface in ecology. Oikos 82:440–448

    Google Scholar 

  • Griffiths R, Daan S, Dijkstra.C. (1996) Sex identification in birds using two CHD genes. Proc R Soc Biol Sci Ser B 263:1251–1256

    CAS  Google Scholar 

  • Griffiths R, Double M, Orr K, Dawson R (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1076

    CAS  PubMed  Google Scholar 

  • Hanssen SA, Engebretsen H, Erikstad KE (2002) Incubation start and egg size in relation to body reserves in the common eider. Behav Ecol Sociobiol 52:282–288

    Article  Google Scholar 

  • Hébert PN (2002) Ecological factors affecting initiation of incubation behaviour. In: Deeming DC (ed) Avian incubation: behaviour, environment, and evolution. Oxford University Press, New York, pp 271-279

    Google Scholar 

  • Henry MH, Burke WH (1999) The effects of in ovo administration of testosterone or an antiandrogen on growth of chick embryos and embryonic muscle characteristics. Poult Sci 78:1006–1013

    CAS  PubMed  Google Scholar 

  • Kirkpatrick M, Lande R (1989) The evolution of maternal effects. Evolution 43:485–503

    Google Scholar 

  • Komdeur J, Pen I (2002) Adaptive sex allocation in birds: the complexities of linking theory and practice. Philos Trans R Soc Lond B Biol Sci 357:373–380

    Article  PubMed  Google Scholar 

  • Komdeur J, Daan S, Tinbergen J, Mateman C (1997) Extreme adaptive modification in sex ratio of the Seychelles warbler's eggs. Nature 385:522–525

    CAS  Google Scholar 

  • Komdeur J, Magrath MJL, Krackow S (2002) Pre-ovulation control of hatchling sex ratio in the Seychelles warbler. Proc R Soc Lond Ser B 269:1067–1072

    Article  Google Scholar 

  • Krackow S (1995) Potential mechanisms for sex ratio adjustment in mammals and birds. Biol Rev 70:225–241

    PubMed  Google Scholar 

  • Krackow S, Tkadlec E (2001) Analysis of brood sex ratios: implications of offspring clustering. Behav Ecol Sociobiol 50:293–301

    Article  Google Scholar 

  • Krebs EA, Green DJ, Double MC, Griffiths R (2002) Laying date and laying sequence influence the sex ratio of crimson rosella broods. Behav Ecol Sociobiol 51:447–454

    Article  Google Scholar 

  • Legge S, Hensohn R, Double M, Griffiths R, Cockburn A (2001) Complex sex allocation in the laughing kookaburra. Behav Ecol 12:524–533

    Article  Google Scholar 

  • Martin TE (2002) A new view of avian life-history evolution tested on an incubation paradox. Proc R Soc Lond Ser B 269:309–316

    Article  Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407

    Article  Google Scholar 

  • Price T (1998) Maternal and paternal effects in birds: Effects on offspring fitness. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, New York, pp 202–226

  • Reece SE, Broderick AC, Godley BJ, West SA (2002) The effects of incubation environment, sex and pedigree on the hatching phenotype in a natural population of loggerhead turtles. Evol Ecol Res 4:737–748

    Google Scholar 

  • Reed WL, Vleck CM (2001) Functional significance of variation in egg-yolk androgens in the American coot. Oecologia 128:164–171

    Article  Google Scholar 

  • Royle N, Surai PF, Hartley IR (2001) Maternally derived androgens and antioxidants in bird eggs: complementary but opposite effects? Behav Ecol 12:380–385

    Article  Google Scholar 

  • Schwabl H (1996a) Environment modifies the testosterone levels of a female bird and its eggs. J Exper Zool 276:157–163

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Schwabl H (1999) Maternal hormonal effects on postnatal development. In: Adams NJ, Slotow RH (eds) Proc Int Ornithol Congr 22:2807–2816

    Google Scholar 

  • Sheldon BC, Merila J, Lindgren G, Ellegren H (1998) Gender and environmental sensitivity in nestling collared flycatchers. Ecology 79:1939–1948

    Google Scholar 

  • Slagsvold T, Lifjeld JT (1989) Hatching asynchrony in birds: the hypothesis of sexual conflict over parental investment. Am Nat 134:239–253

    Article  Google Scholar 

  • Sockman KW, Schwabl H (2002) Covariation of clutch size, laying date and incubation tendency in the American Kestrel. Condor 103:570–578

    Google Scholar 

  • Sockman KW, Schwabl H, Sharp PJ (2000) The role of prolactin in the regulation of clutch size and onset of incubation behavior in the American Kestrel. Horm Behav 38:168–178

    Article  CAS  PubMed  Google Scholar 

  • Stoleson SH, Beissinger SR (1995) Hatching asynchrony and the onset of incubation in birds, revisited: when is the crucial period? Curr Ornithol 12:191–270

    Google Scholar 

  • Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–91

    CAS  PubMed  Google Scholar 

  • Vleck CM (2002) Hormonal control of incubation behaviour. In: Deeming DC (ed) Avian incubation: behaviour, environment, and evolution. Oxford University Press, New York, pp 54–62

    Google Scholar 

  • West SA, Sheldon BC (2002) Constraints in the evolution of sex ratio adjustment. Science 295:1685–1688

    Article  CAS  PubMed  Google Scholar 

  • Wolf JB, Wade M (2001) On the assignment of fitness to parents and offspring: whose fitness is it and when does it matter? J Evol Biol 14:347–356

    Article  Google Scholar 

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Acknowledgments

We thank B. Sheldon, B. Lyon, R. Duckworth, F. James, L. Oring, M. Mangel, E. Snell-Rood, M. Smith, B. Young, and an anonymous reviewer for discussion and the comments on the manuscript, personnel of the Vigilante MiniStorage in Missoula for allowing us to work on their property, L.A. Whittingham and H. Mays for sexing nestlings, and the NSF (DEB-0075388, DEB-0077804, IBN-9722171) for funding this work.

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Correspondence to Alexander V. Badyaev.

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Badyaev, A.V., Hill, G.E. & Beck, M.L. Interaction between maternal effects: onset of incubation and offspring sex in two populations of a passerine bird. Oecologia 135, 386–390 (2003). https://doi.org/10.1007/s00442-003-1203-x

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