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Extra-pair paternity, offspring mortality and offspring sex ratio in the socially monogamous coal tit (Parus ater)

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Abstract

Females of many socially monogamous bird species commonly engage in extra-pair copulations. Assuming that extra-pair males are more attractive than the females’ social partners and that attractiveness has a heritable component, sex allocation theory predicts facultative overproduction of sons among extra-pair offspring (EPO) as sons benefit more than daughters from inheriting their father’s attractiveness traits. Here, we present a large-scale, three-year study on sex ratio variation in a passerine bird, the coal tit (Parus ater). Molecular sexing in combination with paternity analysis revealed no evidence for a male-bias in EPO sex ratios compared to their within-pair maternal half-siblings. Our main conclusion, therefore, is that facultative sex allocation to EPO is absent in the coal tit, in accordance with findings in several other species. Either there is no net selection for a deviation from random sex ratio variation (e.g. because extra-pair mating may serve goals different from striving for ‘attractiveness genes’) or evolutionary constraints preclude the evolution of precise maternal sex ratio adjustment. It is interesting to note that, however, we found broods without EPO as well as broods without mortality to be relatively female-biased compared to broods with EPO and mortality, respectively. We were unable to identify any environmental or parental variable to co-vary with brood sex ratios. There was no significant repeatability of sex ratios in consecutive broods of individual females that would hint at some idiosyncratic maternal sex ratio adjustment. Further research is needed to resolve the biological significance of the correlation between brood sex ratios and extra-pair paternity and mortality incidence, respectively.

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References

  • Arctander P (1988) Comparative studies of avian DNA by restriction fragment length polymorphism analysis: convenient procedures based on blood samples from live birds. J Ornithol 129:205–216

    Article  Google Scholar 

  • Bensch S (1999) Sex allocation in relation to parental quality. In: Adams NJ, Slotow RH (eds) 22nd International Ornithological Congress, Durban, 16–22 August 1998. BirdLife South Africa, Johannesburg, South Africa, pp 451–466

    Google Scholar 

  • Birkhead TR, Møller AP (1992) Sperm competition in birds: evolutionary causes and consequences. Academic Press, London, UK

    Google Scholar 

  • Burley N (1981) Sex ratio manipulation and selection for attractiveness. Science 221:721–722

    Article  Google Scholar 

  • Burley N (1986) Sex-ratio manipulation in color-banded populations of zebra finches. Evolution 40:1191–1206

    Article  Google Scholar 

  • Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Clutton-Brock TH (1986) Sex ratio variation in birds. Ibis 128:317–329

    Article  Google Scholar 

  • Cockburn A, Legge S, Double MC (2002) Sex ratios in birds and mammals: can the hypotheses be disentangled? In: Hardy ICW (ed) Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, UK, pp 266–286

    Google Scholar 

  • Cordero PJ, Griffith SC, Aparicio JM, Parkin DT (2000) Sexual dimorphism in house sparrow eggs. Behav Ecol Sociobiol 48:353–357

    Article  Google Scholar 

  • Dietrich V (2001) Zum Auftreten alternativer Fortpflanzungsstrategien in einer Lingener Population der Tannenmeise Parus ater. Diploma thesis, Technical University of Braunschweig, Germany

  • Dietrich VCJ, Schmoll T, Winkel W, Lubjuhn T (2003) Survival to first breeding is not sex-specific in the coal tit (Parus ater). J Ornithol 144:148–156

    Article  Google Scholar 

  • Dietrich V, Schmoll T, Winkel W, Epplen JT, Lubjuhn T (2004) Pair identity–an important factor concerning variation in extra-pair paternity in the coal tit (Parus ater). Behaviour 141:817–835

    Article  Google Scholar 

  • Dyrcz A, Sauer-Gürth H, Tkadlec E, Wink M (2004) Offspring sex ratio variation in relation to brood size and mortality in a promiscuous species: the aquatic warbler Acrocephalus paludicola. Ibis 146:269–280

    Article  Google Scholar 

  • Ellegren H, Gustafsson L, Sheldon BC (1996) Sex ratio adjustment in relation to paternal attractiveness in a wild bird population. Proc Natl Acad Sci USA 93:11723–11728

    Article  PubMed  CAS  Google Scholar 

  • Epplen JT (1992) The methodology of multilocus DNA fingerprinting using radioactive or nonradioactive oligonucleotide probes specific for simple repeat motifs. In: Chrambach A, Dunn MJ, Radola BJ (eds) Advances in electrophoresis, vol 5. VCH, Weinheim, Germany, pp 59–112

    Google Scholar 

  • Fiala KL (1980) On estimating the primary sex ratio from incomplete data. Am Nat 115:442–444

    Article  Google Scholar 

  • Gerken T (2001) Kopulationen außerhalb des Paarbundes bei der Kohlmeise (Parus major)–proximate Einflüsse und ultimate Faktoren. Ph.D. thesis, University of Bonn, Germany

  • Glutz von Blotzheim UN, Bauer KM (1993) Handbuch der Vögel Mitteleuropas, Band 13/I, Passeriformes (4. Teil). Aula, Wiesbaden, Germany

    Google Scholar 

  • Griffith SC, Owens IPF, Thuman KA (2002) Extra-pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212

    Article  PubMed  CAS  Google Scholar 

  • Griffith SC, Örnborg J, Russell AF, Andersson S, Sheldon BC (2003) Correlations between ultraviolet coloration, overwinter survival and offspring sex ratio in the blue tit. J Evol Biol 16:1045–1054

    Article  PubMed  CAS  Google Scholar 

  • Grindstaff JL, Buerkle CA, Casto JM, Nolan V, Ketterson ED (2001) Offspring sex ratio is unrelated to male attractiveness in dark-eyed juncos (Junco hyemalis). Behav Ecol Sociobiol 50:312–316

    Article  Google Scholar 

  • Hardy ICW (1997) Possible factors influencing vertebrate sex ratios: an introductory overview. Appl Anim Behav Sci 51:217–241

    Article  Google Scholar 

  • Hartley IR, Griffith SC, Wilson K, Shepherd M, Burke T (1999) Nestling sex ratios in the polygynously breeding corn bunting Miliaria calandra. J Avian Biol 30:7–14

    Article  Google Scholar 

  • Hunter, FM, Burke T, Watts SE (1992) Frequent copulations as a method of paternity assurance in the northern fulmar. Anim Behav 44:149–156

    Article  Google Scholar 

  • Jenni L, Winkler R (1994) Moult and ageing of European passerines. Academic Press, London, UK

    Google Scholar 

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • King JR, Griffiths R (1994) Sexual dimorphism of plumage and morphology in the coal tit Parus ater. Bird Study 41:7–14

    Article  Google Scholar 

  • Koenig WD, Dickinson JL (1996) Nestling sex-ratio variation in Western bluebirds. Auk 113:902–910

    Google Scholar 

  • Kokko H, Brooks R, McNamara JM, Houston AI (2002) The sexual selection continuum. Proc R Soc Lond B 269:1331–1340

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Krackow S (2002) Why parental sex ratio manipulation is rare in higher vertebrates. Ethology 108:1041–1056

    Article  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 

  • Krackow S, Meelis E, Hardy ICW (2002) Analysis of sex ratio variances and sex allocation sequences. In: Hardy ICW (ed) Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, UK, pp 112–132

    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 

  • Leech DI, Hartley IR, Stewart IRK, Griffith SC, Burke T (2001) No effect of parental quality or extrapair paternity on brood sex ratio in the blue tit (Parus caeruleus). Behav Ecol 12:674–680

    Article  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Google Scholar 

  • Lessells CM, Mateman AC, Visser J (1996) Great tit hatchling sex ratios. J Avian Biol 27:135–142

    Article  Google Scholar 

  • Lubjuhn T, Sauer KP (1999) DNA fingerprinting and profiling in behavioural ecology. In: Epplen JT, Lubjuhn T (eds) DNA profiling and DNA fingerprinting. Birkhäuser, Basel, Switzerland, pp 39–52

    Google Scholar 

  • Lubjuhn T, Gerken T, Brün J, Epplen JT (1999) High frequency of extra-pair paternity in the coal tit. J Avian Biol 30:229–233

    Article  Google Scholar 

  • Magrath MJL, Green DJ, Komdeur J (2002) Sex allocation in the sexually monomorphic fairy martin. J Avian Biol 33:260–268

    Article  Google Scholar 

  • McCullagh P, Nelder JA (1989) Generalized linear models, vol 37. Chapman and Hall, London, UK

    Google Scholar 

  • Møller AP, Ninni P (1998) Sperm competition and sexual selection: a meta-analysis of paternity studies of birds. Behav Ecol Sociobiol 43:345–358

    Article  Google Scholar 

  • Molenberghs G (2002) Model families. In: Aerts M, Geys H, Molenberghs G, Ryan LM (eds) Topics in modelling of clustered data. Chapman and Hall/CRC, Boca Raton, Florida, pp. 47–75

    Google Scholar 

  • Neuhäuser M (2004) Test for a biased sex ratio when the data are clustered. Env Ecol Stat 11:295–304

    Article  Google Scholar 

  • Oddie KR, Reim C (2002) Egg sex ratio and paternal traits: using within individual comparisons. Behav Ecol 13:503–510

    Article  Google Scholar 

  • Pen I, Weissing FJ (2000) Sexual selection and the sex ratio: an ESS analysis. Selection 1:59–69

    Google Scholar 

  • Questiau S, Escaravage N, Eybert MC, Taberlet P (2000) Nestling sex ratios in a population of bluethroats Luscinia svecica inferred from AFLPTM analysis. J Avian Biol 31:8–14

    Article  Google Scholar 

  • Radford AN, Blakey JK (2000) Is variation in brood sex ratios adaptive in the great tit (Parus major)? Behav Ecol 11:294–298

    Article  Google Scholar 

  • Ramsay SM, Mennill DJ, Otter KA, Ratcliffe LM, Boag PT (2003) Sex allocation in black-capped chickadees Poecile atricapilla. J Avian Biol 34:134–139

    Article  Google Scholar 

  • Risch M, Brinkhof MWG (2002) Sex ratios of sparrowhawk (Accipiter nisus) broods: the importance of age in males. Ornis Fenn 79:49–59

    Google Scholar 

  • Rosenfield RN, Bielefeldt J, Vos SM (1996) Skewed sex ratios in Cooper’s hawk offspring. Auk 113:957–960

    Google Scholar 

  • Rutstein AN, Gorman HE, Arnold KE, Gilbert L, Orr KJ, Adam A, Nager R, Graves JA (2005) Sex allocation in response to paternal attractiveness in the zebra finch. Behav Ecol 16:763–769

    Article  Google Scholar 

  • Saino N, Ellegren H, Møller AP (1999) No evidence for adjustment of sex allocation in relation to paternal ornamentation and paternity in barn swallows. Mol Ecol 8:399–406

    Article  Google Scholar 

  • SAS Institute Inc. (1989) SAS/STAT user’s guide: Version 6, vol 1. SAS Institute Inc., Cary, North Carolina

    Google Scholar 

  • Schmoll T, Dietrich V, Winkel W, Lubjuhn T (2004) Blood-sampling does not affect fledging success and fledgling local recruitment in coal tits (Parus ater). J Ornithol 145:79–80

    Article  Google Scholar 

  • Schmoll T, Dietrich V, Winkel W, Epplen JT, Schurr F, Lubjuhn T (2005) Paternal genetic effects on offspring fitness are context-dependent within the extra-pair mating system of a socially monogamous passerine. Evolution 59:645–657

    PubMed  Google Scholar 

  • Sheldon BC, Ellegren H (1996) Offspring sex and paternity in the collared flycatcher. Proc R Soc Lond B 263:1017–1021

    Article  Google Scholar 

  • Sheldon BC, Andersson S, Griffith SC, Örnborg J, Sendecka J (1999) Ultraviolet colour variation influences blue tit sex ratios. Nature 402:874–877

    Article  CAS  Google Scholar 

  • Stauss M, Segelbacher G, Tomiuk J, Bachmann L (2005) Sex ratio of Parus major and P. caeruleus broods depends on parental condition and habitat quality. Oikos 109:367–373

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Verboven N, Käkelä M, Orell M (2002) Absence of seasonal variation in great tit offspring sex ratios. J Avian Biol 33:138–142

    Article  Google Scholar 

  • Westerdahl H, Bensch S, Hansson B, Hasselquist D, von Schantz T (1997) Sex ratio variation among broods of great reed warblers Acrocephalus arundinaceus. Mol Ecol 6:543–548

    Article  Google Scholar 

  • Westneat DF (1990) Genetic parentage in the indigo bunting: a study using DNA fingerprinting. Behav Ecol Sociobiol 27:67–76

    Article  Google Scholar 

  • Westneat DF, Clark AB, Rambo K (1995) Within-brood patterns of paternity and paternal behavior in red-winged blackbirds. Behav Ecol Sociobiol 37:349–356

    Article  Google Scholar 

  • Whittingham LA, Dunn PO (2000) Offspring sex ratios in tree swallows: females in better condition produce more sons. Mol Ecol 9:1123–1129

    Article  PubMed  CAS  Google Scholar 

  • Williams GC (1979) The question of adaptive sex ratio in outcrossed vertebrates. Proc R Soc Lond B 205:567–580

    Article  PubMed  CAS  Google Scholar 

  • Winkel W (1970) Hinweise zur Art- und Altersbestimmung von Nestlingen höhlenbrütender Vogelarten anhand ihrer Körperentwicklung. Vogelwelt 91:52–59

    Google Scholar 

  • Winkel W (1975) Vergleichend-brutbiologische Untersuchungen an fünf Meisenarten (Parus spp.) in einem niedersächsischen Aufforstungsgebiet mit Japanischer Lärche Larix leptolepis. Vogelwelt 96:41–63 and 104–114

    Google Scholar 

  • Winkel W, Winkel D (1980) Zum Paarzusammenhalt bei Kohl-, Blau- und Tannenmeise (Parus major, P. caeruleus und P. ater). Vogelwarte 30:325–333

    Google Scholar 

  • Winkel W, Winkel D (1997) Zum Einfluß der Populationsdichte auf die Zweitbrutrate von Tannenmeisen. Jahresber Inst Vogelforsch 3:29

    Google Scholar 

  • Yamaguchi N, Kawano KK, Eguchi K, Yahara T (2004) Facultative sex ratio adjustment in response to male tarsus length in the varied tit Parus varius. Ibis 146:108–113

    Article  Google Scholar 

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Acknowledgements

We would like to thank Sabrina Bleidissel, Anke Kalt, Maria Orland, Andrea Petzold, Tanja Meißner and Christiane Wallnisch for their help in the laboratory, Jörg Brün, Thomas Gerken, Volker Janzon, Anja Quellmalz, Jorg Welcker and Doris Winkel for assistance in the field, Karin and Herbert Körner for housing and hospitality during field work and Georg Rüppell for the provision of working facilities. We thank three anonymous referees for valuable comments on an earlier draft of the manuscript. The project was financed by the Deutsche Forschungsgemeinschaft (Lu 572/2-4) and VD-B was supported by a Ph.D. scholarship provided by the TU Braunschweig. This research was conducted under licence by the competent German authority (No. 509f–42502–46).

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Correspondence to Thomas Lubjuhn.

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Dietrich-Bischoff, V., Schmoll, T., Winkel, W. et al. Extra-pair paternity, offspring mortality and offspring sex ratio in the socially monogamous coal tit (Parus ater). Behav Ecol Sociobiol 60, 563–571 (2006). https://doi.org/10.1007/s00265-006-0201-5

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