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Maternal Natal Environment and Breeding Territory Predict the Condition and Sex Ratio of Offspring

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Abstract

Females in a variety of taxa adjust offspring sex ratios to prevailing ecological conditions. However, little is known about whether conditions experienced during a female’s early ontogeny influence the sex ratio of her offspring. We tested for past and present ecological predictors of offspring sex ratios among known-age females that were produced as offspring and bred as adults in a population of house wrens. The body condition of offspring that a female produced and the proportion of her offspring that were male were negatively correlated with the size of the brood in which she herself was reared. The proportion of sons within broods was negatively correlated with maternal hatching date, and varied positively with the quality of a female’s current breeding territory as predicted. However, females producing relatively more sons than daughters were less likely to return to breed in the population the following year. Although correlative, our results suggest that the rearing environment can have enduring effects on later maternal investment and sex allocation. Moreover, the overproduction of sons relative to daughters may increase costs to a female’s residual reproductive value, constraining the extent to which sons might be produced in high-quality breeding conditions. Sex allocation in birds remains a contentious subject, largely because effects on offspring sex ratios are small. Our results suggest that offspring sex ratios are shaped by various processes and trade-offs that act throughout the female life history and ultimately reduce the extent of sex-ratio adjustment relative to classic theoretical predictions.

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References

  • Auer, S. K., Arendt, J. D., Chandramouli, R., & Reznick, D. N. (2010). Juvenile compensatory growth has negative consequences for reproduction in Trinidadian guppies (Poecilia reticulata). Ecology Letters, 13, 998–1007.

    PubMed  Google Scholar 

  • Badyaev, A. V., Hamstra, T. L., Oh, K. P., & Acevedo Seaman, D. A. (2006). Sex-biased maternal effects reduce ectoparasite-induced mortality in a passerine bird. Proceedings of the National Academy of Sciences of the USA, 103, 14406–14411.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badyaev, A. V., Hill, G. E., Beck, M. L., Dervan, A. A., Duckworth, R. A., McGraw, K. J., et al. (2002). Sex-biased hatching order and adaptive population divergence in a passerine bird. Science, 295, 316–318.

    Article  CAS  PubMed  Google Scholar 

  • Belles-Isles, J.-C., & Picman, J. (1987). Suspected adult intraspecific killing by house wrens. Wilson Bulletin, 99, 497–498.

    Google Scholar 

  • Bensch, S., & Hasselquist, D. (1991). Territory infidelity in the polygynous great reed warbler Acrocephalus arundinaceus: the effect of variation in territory attractiveness. Journal of Animal Ecology, 60, 857–871.

    Article  Google Scholar 

  • Bouwhuis, S., Charmantier, A., Verhulst, S., & Sheldon, B. C. (2010). Individual variation in rates of senescence: natal origin effects and disposable soma in a wild bird population. Journal of Animal Ecology, 79, 1251–1261.

    Article  PubMed  Google Scholar 

  • Bowers, E. K., Hodges, C. J., Forsman, A. M., Vogel, L. A., Masters, B. S., Johnson, B. G. P., et al. (2014a). Neonatal body condition, immune responsiveness, and hematocrit predict longevity in a wild bird population. Ecology, 95, 3027–3034.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bowers, E. K., Munclinger, P., Bureš, S., Nádvorník, P., Uvírová, L., & Krist, M. (2013a). Cross-fostering eggs reveals that female collared flycatchers adjust clutch sex ratios according to parental ability to invest in offspring. Molecular Ecology, 22, 215–228.

    Article  PubMed  Google Scholar 

  • Bowers, E. K., Nietz, D., Thompson, C. F., & Sakaluk, S. K. (2014b). Parental provisioning in house wrens: effects of varying brood size and consequences for offspring. Behavioral Ecology, 25, 1485–1493.

    Article  Google Scholar 

  • Bowers, E. K., Sakaluk, S. K., & Thompson, C. F. (2011). Adaptive sex allocation in relation to hatching synchrony and offspring quality in house wrens. American Naturalist, 177, 617–629.

    Article  PubMed  Google Scholar 

  • Bowers, E. K., Sakaluk, S. K., & Thompson, C. F. (2013b). Sibling cooperation influences the age of nest-leaving in an altricial bird. American Naturalist, 181, 775–786.

    Article  PubMed  Google Scholar 

  • Bowers, E. K., Thompson, C. F., & Sakaluk, S. K. (2014c). Offspring sex ratio varies with clutch size for female house wrens induced to lay supernumerary eggs. Behavioral Ecology, 25, 165–171.

    Article  Google Scholar 

  • Bowers, E. K., Thompson, C. F., & Sakaluk, S. K. (2015). Persistent sex-by-environment effects on offspring fitness and sex-ratio adjustment in a wild bird population. Journal of Animal Ecology, 84, 473–486.

    Article  PubMed  Google Scholar 

  • Bowers, E. K., Thompson, C. F., & Sakaluk, S. K. (2016). Within-female plasticity in sex allocation in associated with a behavioural polyphenism in house wrens. Journal of Evolutionary Biology, 29, 602–616.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clutton-Brock, T. H., Albon, S. D., & Guinness, F. E. (1984). Maternal dominance, breeding success and birth sex ratios in red deer. Nature, 308, 358–360.

    Article  Google Scholar 

  • Cockburn, A., Legge, S., & Double, M. C. (2002). Sex-ratios in birds and mammals: can the hypotheses be disentangled? In I. C. W. Hardy (Ed.), Sex-ratios: concepts and research methods (pp. 266–286). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Cordero, P. J., Viñuela, J., Aparicio, J. M., & Veiga, J. P. (2001). Seasonal variation in sex ratio and sexual egg dimorphism favouring daughters in first clutches of the spotless starling. Journal of Evolutionary Biology, 14, 829–834.

    Article  Google Scholar 

  • DeMory, M. L., Thompson, C. F., & Sakaluk, S. K. (2010). Male quality influences male provisioning in house wrens independent of attractiveness. Behavioral Ecology, 21, 1156–1164.

    Article  Google Scholar 

  • Dijkstra, C., Daan, S., & Buker, J. B. (1990). Adaptive seasonal variation in the sex ratio of kestrel broods. Functional Ecology, 4, 143–147.

    Article  Google Scholar 

  • Dobbs, R. C., Styrsky, J. D., & Thompson, C. F. (2006). Clutch size and the costs of incubation in the house wren. Behavioral Ecology, 17, 849–856.

    Article  Google Scholar 

  • Douhard, M., Gaillard, J.-M., Delorme, D., Capron, G., Duncan, P., Klein, F., & Bonenfant, C. (2013). Variation in adult body mass of roe deer: early environmental conditions influence early and late body growth of females. Ecology, 94, 1805–1814.

    Article  PubMed  Google Scholar 

  • Drilling, N. A., & Thompson, C. F. (1988). Natal and breeding dispersal in house wrens (Troglodytes aedon). Auk, 105, 480–491.

    Google Scholar 

  • Drummond, H., & Ancona, S. (2015). Observational field studies reveal wild birds responding to early-life stresses with resilience, plasticity, and intergenerational effects. Auk, 132, 563–576.

    Article  Google Scholar 

  • Eckerle, K. P., & Thompson, C. F. (2006). Mate choice in house wrens: nest cavities trump male characteristics. Behaviour, 143, 253–271.

    Article  Google Scholar 

  • Finke, M. A., Milinkovich, D. J., & Thompson, C. F. (1987). Evolution of clutch size: an experimental test in the house wren (Troglodytes aedon). Journal of Animal Ecology, 56, 99–114.

    Article  Google Scholar 

  • Fisher, R. A. (1930). The genetical theory of natural selection. Oxford: Clarendon Press.

    Book  Google Scholar 

  • Gaukler, S. M., Ruff, J. S., & Potts, W. K. (2016). Paroxetine exposure skews litter sex ratios in mice suggesting a Trivers–Willard process. Behavioral Ecology. doi:10.1093/beheco/arw017.

    PubMed  Google Scholar 

  • Grana, S. C., Sakaluk, S. K., Bowden, R. M., Doellman, M. A., Vogel, L. A., & Thompson, C. F. (2012). Reproductive allocation in female house wrens is not influenced by experimentally altered male attractiveness. Behavioral Ecology and Sociobiology, 66, 1247–1258.

    Article  Google Scholar 

  • Gustafsson, L., & Sutherland, W. J. (1988). The costs of reproduction in the collared flycatcher Ficedula albicollis. Nature, 355, 813–815.

    Article  Google Scholar 

  • Harmsen, R., & Cooke, F. (1983). Binomial sex-ratio distribution in the lesser snow goose: a theoretical enigma. American Naturalist, 121, 1–8.

    Article  Google Scholar 

  • Harrison, X. A., Blount, J. D., Inger, R., Norris, R. D., & Bearhop, S. (2011). Carry-over effects as drivers of fitness differences in animals. Journal of Animal Ecology, 80, 4–18.

    Article  PubMed  Google Scholar 

  • Haywood, S., & Perrins, C. M. (1992). Is clutch size in birds affected by environmental conditions during growth? Proceedings of the Royal Society of London B, 249, 195–197.

    Article  CAS  Google Scholar 

  • Helle, H., Koskela, E., & Mappes, T. (2012). Life in varying environments: experimental evidence for delayed effects of juvenile environment on adult life history. Journal of Animal Ecology, 81, 573–582.

    Article  PubMed  Google Scholar 

  • Hewison, A. J. M., & Gaillard, J.-M. (1999). Successful sons or advantaged daughters? The Trivers–Willard model and sex-biased maternal investment in ungulates. Trends in Ecology & Evolution, 14, 229–234.

    Article  CAS  Google Scholar 

  • Hodges, C. J., Bowers, E. K., Thompson, C. F., & Sakaluk, S. K. (2015). Cascading costs of reproduction in female house wrens induced to lay larger clutches. Journal of Evolutionary Biology, 28, 1383–1393.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoover, J. P. (2003). Decision rules for site fidelity in a migratory bird, the prothonotary warbler. Ecology, 84, 416–430.

    Article  Google Scholar 

  • Janiszewski, T., Minias, P., & Wojciechowski, Z. (2013). Occupancy reliably reflects territory quality in a long-lived migratory bird, the white stork. Journal of Zoology, 291, 178–184.

    Article  Google Scholar 

  • Johnson, L. S. (2014). House wren (Troglodytes aedon), 2nd edn. In A. Poole (Ed.), The birds of North America online. Cornell Lab of Ornithology and American Ornithologists’ Union: Ithaca, NY. doi:10.2173/bna.380.

    Google Scholar 

  • Johnson, L. S., & Kermott, L. H. (1990). Possible causes of territory takeovers in a north-temperate population of house wrens. Auk, 107, 781–784.

    Article  Google Scholar 

  • Johnson, L. S., & Searcy, W. A. (1993). Nest site quality, female mate choice, and polygyny in the house wren. Ethology, 95, 265–277.

    Article  Google Scholar 

  • Kendeigh, S. C. (1941). Territorial and mating behavior of the house wren. Illinois Biological Monographs, 18, 1–120.

    Google Scholar 

  • Komdeur, J. (2012). Sex allocation. In N. J. Royle, P. R. Smiseth, & M. Kölliker (Eds.), The evolution of parental care (pp. 171–188). Oxford: Oxford University Press.

    Chapter  Google Scholar 

  • Krist, M. (2006). Should mothers in poor condition invest more in daughter than in son? Ethology Ecology and Evolution, 18, 241–246.

    Article  Google Scholar 

  • Lambrechts, M. M., Adriaensen, F., Ardia, D. R., Artemyev, A. V., Atiénzar, F., Bańbura, J., et al. (2010). The design of artificial nestboxes for the study of secondary hole-nesting birds: a review of methodological inconsistencies and potential biases. Acta Ornithologica, 45, 1–26.

    Article  Google Scholar 

  • Leimar, O. (1996). Life-history analysis of the Trivers and Willard sex-ratio problem. Behavioral Ecology, 7, 316–325.

    Article  Google Scholar 

  • Lindström, J. (1999). Early development and fitness in birds and mammals. Trends in Ecology & Evolution, 14, 343–348.

    Article  Google Scholar 

  • Merkling, T., Welcker, J., Hewison, A. J. M., Hatch, S. A., Kitaysky, A. S., Speakman, J. R., et al. (2015). Identifying the selective pressures underlying offspring sex-ratio adjustments: a case study in a wild seabird. Behavioral Ecology, 26, 916–925.

    Article  Google Scholar 

  • Millon, A., Petty, S. J., Little, B., & Lambin, X. (2011). Natal conditions alter age-specific reproduction but not survival or senescence in a long-lived bird of prey. Journal of Animal Ecology, 80, 968–975.

    Article  PubMed  Google Scholar 

  • Myers, J. H. (1978). Sex ratio adjustment under food stress: maximization of quality or numbers of offspring? American Naturalist, 112, 381–388.

    Article  Google Scholar 

  • Naguib, M., & Gil, D. (2005). Transgenerational effects on body size caused by early developmental stress in zebra finches. Biology Letters, 1, 95–97.

    Article  PubMed  PubMed Central  Google Scholar 

  • Naguib, M., Nemitz, A., & Gil, D. (2006). Maternal developmental stress reduces reproductive success of female offspring in zebra finches. Proceedings of the Royal Society B, 273, 1901–1905.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakagawa, S., & Cuthill, I. C. (2007). Effect size, confidence interval and statistical significance: a practical guide for biologists. Biological Reviews, 82, 591–605.

    Article  PubMed  Google Scholar 

  • Pärt, T., & Gustafsson, L. (1989). Breeding dispersal in the collared flycatcher (Ficedula albicollis): possible causes and reproductive consequences. Journal of Animal Ecology, 58, 305–320.

    Article  Google Scholar 

  • Peig, J., & Green, A. J. (2009). New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos, 118, 1883–1891.

    Article  Google Scholar 

  • Pen, I., Weissing, F. J., & Daan, S. (1999). Seasonal sex ratio trend in the European kestrel: an evolutionarily stable strategy analysis. American Naturalist, 153, 384–397.

    Article  Google Scholar 

  • Poirier, N. E., Whittingham, L. A., & Dunn, P. O. (2004). Males achieve greater reproductive success through multiple broods than through extrapair mating in house wrens. Animal Behaviour, 67, 1109–1116.

    Article  Google Scholar 

  • Postma, E., Heinrich, F., Koller, U., Sardell, R. J., Reid, J. M., Arcese, P., & Keller, L. F. (2011). Disentangling the effect of genes, the environment and chance on sex ratio variation in a wild bird population. Proceedings of the Royal Society B, 278, 2996–3002.

    Article  PubMed  PubMed Central  Google Scholar 

  • Romano, A., Ambrosini, R., Caprioli, M., Bonisoli-Alquati, A., & Saino, N. (2012). Secondary sex ratio covaries with demographic trends and ecological conditions in the barn swallow. Evolutionary Ecology, 26, 1041–1053.

    Article  Google Scholar 

  • Rosenthal, R. (1994). Parametric measures of effect size. In H. Cooper & L. V. Hedges (Eds.), The handbook of research synthesis (pp. 231–244). New York: Russell Sage Foundation.

    Google Scholar 

  • Rutkowska, J., Koskela, E., Mappes, T., & Speakman, J. R. (2011). A trade-off between current and future sex allocation revealed by maternal energy budget in a small mammal. Proceedings of the Royal Society B, 278, 2962–2969.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sakaluk, S. K., Wilson, A. J., Bowers, E. K., Johnson, L. S., Masters, B. S., Johnson, B. G. P., et al. (2014). Genetic and environmental variation in condition, cutaneous immunity, and haematocrit in house wrens. BMC Evolutionary Biology, 14, 242.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schielzeth, H. (2010). Simple means to improve the interpretability of regression coefficients. Methods in Ecology and Evolution, 1, 103–113.

    Article  Google Scholar 

  • Schwanz, L. E., & Robert, K. A. (2014). Proximate and ultimate explanations of mammalian sex allocation in a marsupial model. Behavioral Ecology and Sociobiology, 68, 1085–1096.

    Article  Google Scholar 

  • Sokal, R. R., & Rohlf, F. J. (1995). Biometry (3rd ed.). New York: W. H. Freeman and Company.

    Google Scholar 

  • Trivers, R. L., & Willard, D. E. (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science, 179, 90–92.

    Article  CAS  PubMed  Google Scholar 

  • Uller, T. (2006). Sex-specific sibling interactions and offspring fitness in vertebrates: patterns and implications for maternal sex ratios. Biological Reviews, 81, 207–217.

    Article  PubMed  Google Scholar 

  • Uller, T., & Olsson, M. (2010). Offspring size and timing of hatching determine survival and reproductive output in a lizard. Oecologia, 162, 663–671.

    Article  PubMed  Google Scholar 

  • Warner, D. A., Uller, T., & Shine, R. (2013). Transgenerational sex determination: the embryonic environment experienced by a male affects offspring sex ratio. Scientific Reports, 3, 2709.

    Article  PubMed  PubMed Central  Google Scholar 

  • West, S. A. (2009). Sex allocation. Princeton: Princeton University Press.

    Book  Google Scholar 

  • West, S. A., & Sheldon, B. C. (2002). Constraints in the evolution of sex ratio adjustment. Science, 295, 1685–1688.

    Article  CAS  PubMed  Google Scholar 

  • Whittingham, L. A., Valkenaar, S. M., Poirier, N. E., & Dunn, P. O. (2002). Maternal condition and nestling sex ratio in house wrens. Auk, 119, 125–131.

    Google Scholar 

  • Wild, G., & West, S. A. (2007). A sex allocation theory for vertebrates: combining local resource competition and condition-dependent allocation. American Naturalist, 170, E112–E128.

    Article  PubMed  Google Scholar 

  • Wilkin, T. A., & Sheldon, B. C. (2009). Sex differences in the persistence of natal environmental effects on life histories. Current Biology, 19, 1998–2002.

    Article  CAS  PubMed  Google Scholar 

  • Williams, G. C. (1966). Natural selection, the costs of reproduction, and a refinement of Lack’s principle. American Naturalist, 100, 687–690.

    Article  Google Scholar 

  • Williams, G. C. (1979). The question of adaptive sex ratio in outcrossed vertebrates. Proceedings of the Royal Society of London B, 205, 567–580.

    Article  CAS  Google Scholar 

  • Wilson, A. J., & Nussey, D. H. (2010). What is individual quality? An evolutionary perspective. Trends in Ecology & Evolution, 25, 207–214.

    Article  Google Scholar 

  • Wong, J. W. Y., & Kölliker, M. (2014). Effects of food restriction across stages of juvenile and early adult development on body weight, survival and adult life history. Journal of Evolutionary Biology, 27, 2420–2430.

    Article  CAS  PubMed  Google Scholar 

  • Zedrosser, A., Pelletier, R., Bischof, R., Festa-Bianchet, M., & Swenson, J. E. (2013). Determinants of lifetime reproduction in female brown bears: early body mass, longevity, and hunting regulations. Ecology, 94, 231–240.

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank the 1999–2013 Wren Crews for field assistance and the ParkLands Foundation (Merwin Preserve) and the Sears and Butler families for the use of their properties for this work. Financial support was provided by the School of Biological Sciences, Illinois State University; National Science Foundation Grants IBN-0316580, IOS-0718140 and IOS-1118160; National Institutes of Health Grant R15HD076308-01; and student research grants from the Sigma Xi Society, the Animal Behavior Society, the American Ornithologists’ Union, the American Museum of Natural History’s Frank M. Chapman Memorial Fund, the Champaign County Audubon Society, and the Beta Lambda Chapter of the Phi Sigma Biological Sciences Honor Society.

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  1. E. Keith Bowers

    Present address: Department of Biological Sciences, University of Memphis, Memphis, TN, 38152, USA

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  1. Behavior, Ecology, Evolution, and Systematics Section, School of Biological Sciences, Illinois State University, Normal, IL, 61790-4120, USA

    E. Keith Bowers, Charles F. Thompson & Scott K. Sakaluk

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All research activities complied with current laws of the United States of America, and were performed in accordance with Illinois State University Institutional Animal Care and Use Committee permits 10-2009, 05-2010, 04-2013; U. S. Geological Survey banding permit 09211; and U. S. Fish and Wildlife Service collecting permit MB692148-0.

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Bowers, E.K., Thompson, C.F. & Sakaluk, S.K. Maternal Natal Environment and Breeding Territory Predict the Condition and Sex Ratio of Offspring. Evol Biol 44, 11–20 (2017). https://doi.org/10.1007/s11692-016-9380-9

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