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Dissecting direct and indirect parental effects on reproduction in a wild bird of prey: dad affects when but not how much

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Abstract

Males can through their behavior (e.g., courtship feeding) exert an indirect effect on their partner’s reproductive traits, such as the seasonal timing and size of her clutch. Evidence for such indirect (male) effect on reproduction is starting to accumulate. We quantify female and male effects on reproduction in the tawny owl Strix aluco using a hierarchical mixed model on data collected in 1978–2013. We find that differences between males explain 7 % of the phenotypic variance in laying date (females 5 %). In contrast, females have a clear (11 %) effect on clutch size, whereas males have no effect. Based on multivariate hierarchical modeling, we find an individual-level correlation between the male-specific effect on laying date and his body mass (but not his plumage color or wing length). Heavy males may be able to affect their partner’s seasonal timing of laying because of an advantage in providing courtship feeding prior to reproduction. Our findings illustrate that males can be an important determinant of variation in reproduction and that multivariate mixed models present a general approach to pinpoint which individual characteristics could be associated with such indirect effects.

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References

  • Ah-King M, Ahnesjö I (2013) The “sex role” concept: an overview and evaluation. Evol Biol 40:461–470

    Article  Google Scholar 

  • Ahola K, Niiranen S (1986) Lehtopöllön iän määrittäminen (age determination of the tawny owl). Lintumies 21:81–85

    Google Scholar 

  • Auld JR, Perrins CM, Charmantier A (2013) Who wears the pants in a mute swan pair? Deciphering the effects of male and female age and identity on breeding success. J Anim Ecol 82:826–835

    Article  PubMed  Google Scholar 

  • Bentler PM (1980) Multivariate analysis with latent variables. Causal modelling. Annu Rev Psychol 31:419–456

    Article  Google Scholar 

  • Bergsma R, Kanis E, Knol EF, Bijma P (2008) The contribution of social effects to heritable variation in finishing traits of domestic pigs (Sus scrofa). Genetics 178:1559–1570

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bijma P (2014) The quantitative genetics of indirect genetic effects: a selective review of modelling issues. Heredity 112:61–69

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bijma P, Wade MJ (2008) The joint effects of kin, multilevel selection and indirect genetic effects on response to genetic selection. J Evol Biol 21:1175–1188

    Article  CAS  PubMed  Google Scholar 

  • Bijma P, Muir WM, Ellen ED, Wolf JB, Van Arendonk JAM (2007a) Multilevel selection 2: estimating the genetic parameters determining inheritance and response to selection. Genetics 175:289–299

    Article  PubMed Central  PubMed  Google Scholar 

  • Bijma P, Muir WM, van Arendonk JAM (2007b) Multilevel selection 1: quantitative genetics of inheritance and response to selection. Genetics 175:277–288

    Article  PubMed Central  PubMed  Google Scholar 

  • Bleakley BH, Brodie ED III (2009) Indirect genetic effects influence antipredator behavior in guppies: estimates of the coefficient of interaction psi and the inheritance of reciprocity. Evolution 63:1796–1806

    Article  PubMed  Google Scholar 

  • Brommer JE (2013) On between-individual and residual (co)variances in the study of animal personality: are you willing to make the individual gambit? Behav Ecol Sociobiol 67:1027–1032

    Article  Google Scholar 

  • Brommer JE, Rattiste K (2008) ‘Hidden’ reproductive costs between mates in a wild bird population. Evolution 62:2326–2333

    Article  PubMed  Google Scholar 

  • Brommer JE, Ahola K, Karstinen T (2005) The colour of fitness: plumage coloration and lifetime reproductive success in the tawny owl. Proc R Soc Lond B 272:935–940

    Article  Google Scholar 

  • Brommer JE, Kontiainen P, Pietiäinen H (2012) Selection on plasticity of seasonal life-history traits using random regression mixed model analysis. Ecol Evol 2:695–704

    Article  PubMed Central  PubMed  Google Scholar 

  • Brommer JE, Karell P, Ahola K, Karstinen T (2014) Residual correlations, and not intrinsic properties of the individuals, determine a nest defense boldness syndrome in tawny owls. Behav Ecol 25:802–812

    Article  Google Scholar 

  • Browne WJ, McCleery RH, Sheldon BC, Pettifor RA (2007) Using cross-classified multivariate mixed response models with application to life history traits in great tits (Parus major). Stat Model 7:217–238

    Google Scholar 

  • Butler DG, Cullis BR, Gilmour AR, Gogel BJ (2009) ASReml-R reference manual version 3. Department of Primary Industries and Fisheries, State of Queensland, Australia

  • Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47

    Article  Google Scholar 

  • Charmantier A, Perrins C, McCleery RH, Sheldon BC (2006) Evolutionary response to selection in clutch size in a long-term study of the mute swan. Am Nat 167:453–465

    Article  PubMed  Google Scholar 

  • Da Silva A, van den Brink V, Emaresi G, Luzio E, Bize P, Dreiss AN, Roulin A (2013) Melanin-based colour polymorphism signals aggressive personality in nest and territory defence in the tawny owl (Strix aluco). Behav Ecol Sociobiol 67:1041–1052

    Article  Google Scholar 

  • Dingemanse NJ, Dochtermann NA, Nakagawa S (2012) Defining behavioural syndromes and the role of ‘syndrome deviation’ in understanding their evolution. Behav Ecol Sociobiol 66:1543–1548

    Article  Google Scholar 

  • Ducrest AL, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510

    Article  PubMed  Google Scholar 

  • Edward DA, Poissant J, Wilson AJ, Chapman T (2014) Sexual conflict and interacting phenotypes: a quantitative genetic analysis of fecundity and copula duration in Drosophila melanogaster. Evolution 68:1651–1660

    Article  PubMed  Google Scholar 

  • Ellen ED, Visscher J, van Arendonk JAM, Bijma P (2008) Survival of laying hens: genetic parameters for direct and associative effects in three purebred layer lines. Poult Sci 87:233–239

    Article  CAS  PubMed  Google Scholar 

  • Forstmeier W (2004) Female resistance to male seduction in zebra finches. Anim Behav 68:1005–1015

    Article  Google Scholar 

  • Gasparini J, Bize P, Piault R, Wakamatsu K, Blount JD, Ducrest AL, Roulin A (2009) Strength and cost of an induced immune response are associated with a heritable melanin‐based colour trait in female tawny owls. J Anim Ecol 78:608–616

    Article  PubMed  Google Scholar 

  • Gienapp P, Postma E, Visser ME (2006) Why breeding time has not responded to selection for earlier breeding in a songbird population. Evolution 60:2381–2388

    Article  PubMed  Google Scholar 

  • Griffing B (1967) Selection in reference to biological groups. I. Individual and group selection applied to populations of unordered groups. Aust J Biol Sci 20:127–139

    CAS  PubMed  Google Scholar 

  • Griffing B (1981) A theory of natural selection incorporating interaction among individuals. I. The modeling process. J Theor Biol 89:635–658

    Article  CAS  PubMed  Google Scholar 

  • Gwynne DT (2008) Sexual conflict over nuptial gifts in insects. Annu Rev Entomol 53:83–101

    Article  CAS  PubMed  Google Scholar 

  • Hadfield JD, Wilson AJ (2007) Multilevel selection 3: modeling the effects of interacting individuals as a function of group size. Genetics 17:667–668

    Article  Google Scholar 

  • Hakkarainen H, Huhta E, Lahti K, Lundvall P, Mappes T, Tolonen P, Wiehn J (1996) A test of male mating and hunting success in the kestrel: the advantages of smallness? Behav Ecol Sociobiol 39:375–380

    Article  Google Scholar 

  • Hall MD, Lailvaux SP, Brooks RC (2013) Sex-specific evolutionary potential of pre- and postcopulatory reproductive interactions in the field cricket Teleogryphus commodus. Evolution 67:1831–1837

    Article  PubMed  Google Scholar 

  • Hirons GJM (1985) The importance of body reserves for successful reproduction in the tawny owl (Strix aluco). J Zool Lond B 1:1–20

    Article  Google Scholar 

  • Horvathova T, Nakagawa S, Uller T (2012) Strategic female reproductive investment in response to male attractiveness in birds. Proc R Soc Lond B 279:163–170

    Article  Google Scholar 

  • Karell P, Kontiainen P, Pietiäinen H, Siitari H, Brommer JE (2008) Maternal effects on offspring Igs and egg size in relation to natural and experimentally improved food supply. Funct Ecol 22:682–690

    Article  Google Scholar 

  • Karell P, Ahola K, Karstinen T, Zolei A, Brommer JE (2009) Population dynamics in a cyclic environment. Consequences of cyclic food abundance on tawny owl reproduction and survival. J Anim Ecol 78:1050–1062

    Article  PubMed  Google Scholar 

  • Karell P, Ahola K, Karstinen T, Brommer JE (2013) Brown tawny owls moult more flight feathers than grey ones. J Avian Biol 44:235–244

    Article  Google Scholar 

  • Kekkonen J, Kolunen H, Pietiäinen H, Karell P, Brommer JE (2008) Tawny owl reproduction and offspring sex ratios under variable food conditions. J Ornith 149: 59–66

  • Korpimäki E (1986) Reversed size dimorphism in birds of prey, especially in Tengmalm’s owl Aegolius funereus: a test of the “ starvation hypothesis”. Ornis Scand 17:326–332

    Article  Google Scholar 

  • Ludwigs JD, Becker PH (2005) What do pairing patterns in common tern, Sterna hirundo, recruits reveal about the significance of sex and breeding experience? Behav Ecol Sociobiol 57:412–421

    Article  Google Scholar 

  • Lundberg A (1986) Adaptive advantages of reversed sexual size dimorphism in European owls. Ornis Scand 17:133–140

    Article  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • McCleery RH, Pettifor RA, Armbruster P, Meyer K, Sheldon BC, Perrins CM (2004) Components of variance underlying fitness in a natural population of the great tit Parus major. Am Nat 164:E62–E72

    Article  CAS  PubMed  Google Scholar 

  • McGlothlin JW, Brodie ED III (2009) How to measure indirect genetic effects: the congruence of trait-based and variance partitioning approaches. Evolution 63:1785–1795

    Article  PubMed  Google Scholar 

  • Mikkola H (1983) Owls of Europe. T & AD Poyser, Calton, UK

    Google Scholar 

  • Moore AJ, Brodie ED III, Wolf JB (1997) Interacting phenotypes and the evolutionary process: I direct and indirect genetic effects of social interactions. Evolution 51:1352–1362

    Article  Google Scholar 

  • Petty SJ (1992) A guide to age determination of tawny owl Strix aluco. In: Galbraith CA, Taylor IR, Percival S (eds) The ecology and conservation of European owls). Joint Nature Conservation Committee, UK Nature Conservation, Peterborough, pp 89–91

    Google Scholar 

  • Pietiäinen H, Kolunen H (1993) Female body condition and breeding of the Ural owl Strix uralensis. Funct Ecol 7:726–735

    Article  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed effects models in S and S-PLUS. Springer, New York

    Book  Google Scholar 

  • Rice SH (2004) Evolutionary theory. Mathematical and conceptual foundations, Sinauer, Sunderland

    Google Scholar 

  • Sasvári L, Hegyi Z, Csörgõ T, Hahn I (2000) Age-dependent diet change, parental care and reproductive costin tawny owls Strix aluco. Acta Oecol 21:267–275

    Article  Google Scholar 

  • Sheldon BC, Kruuk LEB, Merilä J (2003) Natural selection and inheritance of breeding time and clutch size in the collared flycatcher. Evolution 57:406–420

    Article  CAS  PubMed  Google Scholar 

  • Shuster SS, Wade MJ (2003) Mating systems and strategies. Princeton University Press, Princeton

    Google Scholar 

  • Teplitsky C, Mills JA, Yarrall JW, Merilä J (2010) Indirect genetic effects in a sex‐limited trait: the case of breeding time in red‐billed gulls. J Evol Biol 23:935–944

    Article  CAS  PubMed  Google Scholar 

  • van de Pol M, Heg D, Bruinzeel LW, Kuijper B, Verhulst S (2006) Experimental evidence for a causal effect of pair-bond duration on reproductive performance in oystercatchers (Haematopus ostralegus). Behav Ecol 17:982–991

    Article  Google Scholar 

  • Wilson AJ, Gelin U, Perron M-C, Réale D (2009) Indirect genetic effects and the evolution of aggression in a vertebrate system. Proc R Soc Lond B 276:533–541

    Article  Google Scholar 

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Acknowledgments

This work was supported by the Academy of Finland (to PK). All members of Kimpari Bird Projects (KBP) and Veikko Tarsa are thanked for their help in collecting field data on the tawny owls. Reviewers are thanked for their comments which improved the quality of this paper. This is publication nr 17 from KBP.

Ethical standards

The procedures required to collect the data described in this work include capture of individuals, marking individuals by ringing, and measuring their morphology, which all fall under the ringing licenses of the authors, as provided by the relevant local authorities.

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Correspondence to Jon E. Brommer.

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Communicated by A. Pilastro

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Brommer, J.E., Karell, P., Aaltonen, E. et al. Dissecting direct and indirect parental effects on reproduction in a wild bird of prey: dad affects when but not how much. Behav Ecol Sociobiol 69, 293–302 (2015). https://doi.org/10.1007/s00265-014-1842-4

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