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
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
Birkhead TR, Møller AP (1992) Sperm competition in birds: evolutionary causes and consequences. Academic Press, London, UK
Burley N (1981) Sex ratio manipulation and selection for attractiveness. Science 221:721–722
Burley N (1986) Sex-ratio manipulation in color-banded populations of zebra finches. Evolution 40:1191–1206
Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton, New Jersey
Clutton-Brock TH (1986) Sex ratio variation in birds. Ibis 128:317–329
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
Cordero PJ, Griffith SC, Aparicio JM, Parkin DT (2000) Sexual dimorphism in house sparrow eggs. Behav Ecol Sociobiol 48:353–357
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
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
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
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
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
Fiala KL (1980) On estimating the primary sex ratio from incomplete data. Am Nat 115:442–444
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
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
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
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
Hardy ICW (1997) Possible factors influencing vertebrate sex ratios: an introductory overview. Appl Anim Behav Sci 51:217–241
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
Hunter, FM, Burke T, Watts SE (1992) Frequent copulations as a method of paternity assurance in the northern fulmar. Anim Behav 44:149–156
Jenni L, Winkler R (1994) Moult and ageing of European passerines. Academic Press, London, UK
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64
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
King JR, Griffiths R (1994) Sexual dimorphism of plumage and morphology in the coal tit Parus ater. Bird Study 41:7–14
Koenig WD, Dickinson JL (1996) Nestling sex-ratio variation in Western bluebirds. Auk 113:902–910
Kokko H, Brooks R, McNamara JM, Houston AI (2002) The sexual selection continuum. Proc R Soc Lond B 269:1331–1340
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
Krackow S (2002) Why parental sex ratio manipulation is rare in higher vertebrates. Ethology 108:1041–1056
Krackow S, Tkadlec E (2001) Analysis of brood sex ratios: implications of offspring clustering. Behav Ecol Sociobiol 50:293–301
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
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
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
Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121
Lessells CM, Mateman AC, Visser J (1996) Great tit hatchling sex ratios. J Avian Biol 27:135–142
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
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
Magrath MJL, Green DJ, Komdeur J (2002) Sex allocation in the sexually monomorphic fairy martin. J Avian Biol 33:260–268
McCullagh P, Nelder JA (1989) Generalized linear models, vol 37. Chapman and Hall, London, UK
Møller AP, Ninni P (1998) Sperm competition and sexual selection: a meta-analysis of paternity studies of birds. Behav Ecol Sociobiol 43:345–358
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
Neuhäuser M (2004) Test for a biased sex ratio when the data are clustered. Env Ecol Stat 11:295–304
Oddie KR, Reim C (2002) Egg sex ratio and paternal traits: using within individual comparisons. Behav Ecol 13:503–510
Pen I, Weissing FJ (2000) Sexual selection and the sex ratio: an ESS analysis. Selection 1:59–69
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
Radford AN, Blakey JK (2000) Is variation in brood sex ratios adaptive in the great tit (Parus major)? Behav Ecol 11:294–298
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
Risch M, Brinkhof MWG (2002) Sex ratios of sparrowhawk (Accipiter nisus) broods: the importance of age in males. Ornis Fenn 79:49–59
Rosenfield RN, Bielefeldt J, Vos SM (1996) Skewed sex ratios in Cooper’s hawk offspring. Auk 113:957–960
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
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
SAS Institute Inc. (1989) SAS/STAT user’s guide: Version 6, vol 1. SAS Institute Inc., Cary, North Carolina
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
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
Sheldon BC, Ellegren H (1996) Offspring sex and paternity in the collared flycatcher. Proc R Soc Lond B 263:1017–1021
Sheldon BC, Andersson S, Griffith SC, Örnborg J, Sendecka J (1999) Ultraviolet colour variation influences blue tit sex ratios. Nature 402:874–877
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
Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–91
Verboven N, Käkelä M, Orell M (2002) Absence of seasonal variation in great tit offspring sex ratios. J Avian Biol 33:138–142
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
Westneat DF (1990) Genetic parentage in the indigo bunting: a study using DNA fingerprinting. Behav Ecol Sociobiol 27:67–76
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
Whittingham LA, Dunn PO (2000) Offspring sex ratios in tree swallows: females in better condition produce more sons. Mol Ecol 9:1123–1129
Williams GC (1979) The question of adaptive sex ratio in outcrossed vertebrates. Proc R Soc Lond B 205:567–580
Winkel W (1970) Hinweise zur Art- und Altersbestimmung von Nestlingen höhlenbrütender Vogelarten anhand ihrer Körperentwicklung. Vogelwelt 91:52–59
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
Winkel W, Winkel D (1980) Zum Paarzusammenhalt bei Kohl-, Blau- und Tannenmeise (Parus major, P. caeruleus und P. ater). Vogelwarte 30:325–333
Winkel W, Winkel D (1997) Zum Einfluß der Populationsdichte auf die Zweitbrutrate von Tannenmeisen. Jahresber Inst Vogelforsch 3:29
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
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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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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DOI: https://doi.org/10.1007/s00265-006-0201-5