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Selection counteracts developmental plasticity in body-size responses to climate change

Abstract

Body-size reductions are a pervasive response to climate change, and body size is a central trait linking together multiple axes of ecology, physiology and life history. Using a combination of three decades of data and controlled experiments, we show that male and female tree swallows (Tachycineta bicolor) have become smaller structurally, despite chicks growing larger under warmer nest temperatures and larger chicks being more likely to return as adults. We find that adult structural size trends are associated with warmer overwintering conditions, rather than the nestling period. Further, adult male body mass trends depend on climate conditions during spring migration; male breeding mass decreased by 4%, whereas female mass was unchanged. This may be explained by the demands of reproduction, as lighter females produce fewer offspring. This work highlights the complex interactions that shape relationships between traits and fitness, which will be critical for predicting evolutionary responses in future environments.

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Fig. 1: Trends in morphology of male and female tree swallows from 1986–2020.
Fig. 2: Wild tree swallow chick measurements in relation to daily average temperatures.
Fig. 3: Morphology of unsexed tree swallow chicks raised on an isocaloric diet at different experimental nest temperatures.
Fig. 4: Environmental changes in the annual cycle of tree swallows.
Fig. 5: Relationship between adult morphology and fledglings produced.

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Data availability

All datasets utilized in this study are publicly available. Daily temperature data is provided via the global historical climatology network (GHNCd) from (https://www.ncei.noaa.gov/data/global-historical-climatology-network-daily/). Geolocation data on tree swallows is provided via the Dryad online repository at (https://doi.org/10.5061/dryad.5v5b124). Data on tree swallow morphology of both adults and chicks is provided via Dryad at (https://doi.org/10.5061/dryad.hdr7sqvjf).

Code availability

The code used in the analysis to arrive at the conclusions in this manuscript are provided via Dryad at (https://doi.org/10.5061/dryad.hdr7sqvjf).

References

  1. Gardner, J. L., Peters, A., Kearney, M. R., Joseph, L. & Heinsohn, R. Declining body size: a third universal response to warming? Trends Ecol. Evol. 26, 285–291 (2011).

    Article  Google Scholar 

  2. Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).

    Article  CAS  Google Scholar 

  3. Durant, J. M., Hjermann, D. Ø., Ottersen, G. & Stenseth, N. C. Climate and the match or mismatch between predator requirements and resource availability. Clim. Res. 33, 271–283 (2007).

    Article  Google Scholar 

  4. Jirinec, V. et al. Morphological consequences of climate change for resident birds in intact Amazonian rainforest. Sci. Adv. 7, eabk1743 (2021).

    Article  Google Scholar 

  5. Weeks, B. C. et al. Shared morphological consequences of global warming in North American migratory birds. Ecol. Lett. 23, 316–325 (2019).

    Article  Google Scholar 

  6. Gardner, J. L. et al. Australian songbird body size tracks climate variation: 82 species over 50 years. Proc. R. Soc. B 286, 20192258 (2019).

    Article  Google Scholar 

  7. McNab, B. K. Extreme Measures: The Ecological Energetics of Birds and Mammals (Univ. of Chicago Press, 2012).

  8. West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, 2003).

  9. Winkler, D. W., Luo, M. K. & Rakhimberdiev, E. Temperature effects on food supply and chick mortality in tree swallows (Tachycineta bicolor). Oecologia 173, 129–138 (2013).

    Article  Google Scholar 

  10. Shipley, J. R. et al. Climate change shifts the timing of nutritional flux from aquatic insects. Curr. Biol. (2022).

  11. Monaghan, P. Early growth conditions, phenotypic development and environmental change. Philos. Trans. R. Soc. London B 363, 1635–1645 (2008).

    Article  Google Scholar 

  12. Conway, C. J. & Martin, T. E. Evolution of passerine incubation behavior: influence of food, temperature, and nest predation. Evolution 54, 670–685 (2000).

    Article  CAS  Google Scholar 

  13. Martin, T. E., Tobalske, B., Riordan, M. M., Case, S. B. & Dial, K. P. Age and performance at fledging are a cause and consequence of juvenile mortality between life stages. Sci. Adv. 4, eaar1988 (2018).

    Article  Google Scholar 

  14. Naef‐Daenzer, B. & Grüebler, M. U. Post‐fledging survival of altricial birds: ecological determinants and adaptation. J. Field Ornithol. 87, 227–250 (2016).

    Article  Google Scholar 

  15. Cox, A. R., Robertson, R. J., Fedy, B. C., Rendell, W. B., & Bonier, F. Demographic drivers of local population decline in tree swallows (Tachycineta bicolor) in Ontario, Canada. Condor Ornithol. Appl. 120, 842–851 (2018).

    Google Scholar 

  16. Sæther, B.-E. & Bakke, Ø. Avian life history variation and contribution of demographic traits to the population growth rate. Ecology 81, 642–653 (2000).

    Article  Google Scholar 

  17. Karasov, W. H. & del Rio, C. M. Physiological Ecology (Princeton Univ. Press, 2007).

  18. Ricklefs, R. The energetics of reproduction in birds. Avian Energetics 15, 152–297 (1974).

    Google Scholar 

  19. Mainwaring, M. C. & Hartley, I. R. The energetic costs of nest building in birds. Avian Biol. Res. 6, 12–17 (2013).

    Article  Google Scholar 

  20. Williams, J. B. Energetics of Avian Incuation. in Avian Energetics and Nutritional Ecology (ed Carey, C.) 375–415 (Springer, Boston, 1996).

  21. Williams, T. D. Mechanisms underlying the costs of egg production. Bioscience 55, 39–48 (2005).

    Article  Google Scholar 

  22. Riddell, E. A., Iknayan, K. J., Wolf, B. O., Sinervo, B. & Beissinger, S. R. Cooling requirements fueled the collapse of a desert bird community from climate change. Proc. Natl Acad. Sci. USA 116, 21609–21615 (2019).

    Article  CAS  Google Scholar 

  23. Dawson, R. D., Lawrie, C. C. & O’Brien, E. L. The importance of microclimate variation in determining size, growth and survival of avian offspring: experimental evidence from a cavity nesting passerine. Oecologia 144, 499–507 (2005).

    Article  Google Scholar 

  24. Andrew, S., Hurley, L., Mariette, M. & Griffith, S. Higher temperatures during development reduce body size in the zebra finch in the laboratory and in the wild. J. Evol. Biol. 30, 2156–2164 (2017).

    Article  CAS  Google Scholar 

  25. Andreasson, F., Nord, A. & Nilsson, J.-Å. Experimentally increased nest temperature affects body temperature, growth and apparent survival in blue tit nestlings. J. Avian Biol. 49 https://doi.org/10.1111/jav.01620 (2018).

  26. Nilsson, J. F., Stjernman, M. & Nilsson, J. Å. Experimental reduction of incubation temperature affects both nestling and adult blue tits Cyanistes caeruleus. J. Avian Biol. 39, 553–559 (2008).

    Article  Google Scholar 

  27. Ardia, D. R., Pérez, J. H. & Clotfelter, E. D. Experimental cooling during incubation leads to reduced innate immunity and body condition in nestling tree swallows. Proc. R. Soc. B https://doi.org/10.1098/rspb.2009.2138 (2010).

  28. Marra, P. P. et al. Non-breeding season habitat quality mediates the strength of density-dependence for a migratory bird. Proc. R. Soc. B 282, 20150624 (2015).

    Article  Google Scholar 

  29. Shipley, J. R. et al. Birds advancing lay dates with warming springs face greater risk of chick mortality. Proc. Natl Acad. Sci. USA (2020).

  30. Robinson, R. A., Baillie, S. R. & Crick, H. Q. Weather‐dependent survival: implications of climate change for passerine population processes. Ibis 149, 357–364 (2007).

    Article  Google Scholar 

  31. Winkler, D. W. et al. Full lifetime perspectives on the costs and benefits of lay date variation in tree swallows. Ecology (2020).

  32. Twining, C. W., Shipley, J. R. & Winkler, D. W. Aquatic insects rich in omega‐3 fatty acids drive breeding success in a widespread bird. Ecol. Lett. 21, 1812–1820 (2018).

    Article  Google Scholar 

  33. Millet, A., Pelletier, F., Bélisle, M. & Garant, D. Patterns of fluctuating selection on morphological and reproductive traits in female tree swallow (Tachycineta bicolor). Evolut. Biol. 42, 349–358 (2015).

    Article  Google Scholar 

  34. Bitton, P.-P., O’Brien, E. L. & Dawson, R. D. Plumage brightness and age predict extrapair fertilization success of male tree swallows, Tachycineta bicolor. Anim. Behav. 74, 1777–1784 (2007).

    Article  Google Scholar 

  35. Whittingham, L. A. & Dunn, P. O. Experimental evidence that brighter males sire more extra‐pair young in tree swallows. Mol. Ecol. 25, 3706–3715 (2016).

    Article  Google Scholar 

  36. Kempenaers, B., Everding, S., Bishop, C., Boag, P. & Robertson, R. J. Extra-pair paternity and the reproductive role of male floaters in the tree swallow (Tachycineta bicolor). Behav. Ecol. Sociobiol. 49, 251–259 (2001).

    Article  Google Scholar 

  37. Lessard, A., Bourret, A., Bélisle, M., Pelletier, F. & Garant, D. Individual and environmental determinants of reproductive success in male tree swallow (Tachycineta bicolor). Behav. Ecol. Sociobiol. 68, 733–742 (2014).

    Article  Google Scholar 

  38. Jetz, W. et al. Biological Earth observation with animal sensors. Trends Ecol. Evol. 37, 293–298 (2022).

    Article  Google Scholar 

  39. Williams, H. J. et al. Future trends in measuring physiology in free-living animals. Philos. Trans. R. Soc. B 376, 20200230 (2021).

    Article  CAS  Google Scholar 

  40. Twining, C. W. et al. Omega-3 long-chain polyunsaturated fatty acids support aerial insectivore performance more than food quantity. Proc. Natl Acad. Sci. (2016).

  41. Naef‐Daenzer, B. & Grüebler, M. U. Post‐fledging survival of altricial birds: ecological determinants and adaptation. J. Field Ornithol. 87, 227–250 (2016).

    Article  Google Scholar 

  42. Chamberlain, S., Hocking, D. & Anderson, B. rnoaa: NOAA Weather Data from R. R version 1.3.8 http://cran.auckland.ac.nz/web/packages/rnoaa/rnoaa.pdf (2021).

  43. Cumbie-Ward, R. V. & Boyles, R. P. Evaluation of a high-resolution SPI for monitoring local drought severity. J. Appl. Meteorol. Climatol. 55, 2247–2262 (2016).

    Article  Google Scholar 

  44. Guttman, N. B. Accepting the standardized precipitation index: a calculation algorithm 1. JAWRA J. Am. Water Resour. Assoc. 35, 311–322 (1999).

    Article  Google Scholar 

  45. Pinheiro, J. et al. nlme: Linear and Nonlinear Mixed Effects Models. R version 3 (2017).

  46. Canty, A. & Ripley, B. Package ‘boot’. Bootstrap Funct. Ver. 1, 3–20 (2017).

    Google Scholar 

  47. Bates, D. et al. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Software 67, 1–48 (2015).

    Article  Google Scholar 

  48. Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. lmerTest package: tests in linear mixed effects models. J. Stat. Software 82, 1–26 (2017).

    Article  Google Scholar 

  49. Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R2 from generalized linear mixed‐effects models. Methods Ecol. Evol. 4, 133–142 (2013).

    Article  Google Scholar 

  50. Johnson, P. C. Extension of Nakagawa & Schielzeth’s R2GLMM to random slopes models. Methods Ecol. Evol. 5, 944–946 (2014).

    Article  Google Scholar 

  51. Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer Science & Business Media, 2009).

  52. Allaire, J. et al. rmarkdown: Dynamic Documents for R. R version 1 (2018).

  53. Stoffel, M. A., Nakagawa, S. & Schielzeth, H. rptR: repeatability estimation and variance decomposition by generalized linear mixed‐effects models. Methods Ecol. Evol. 8, 1639–1644 (2017).

    Article  Google Scholar 

  54. Boyle, W. A., Winkler, D. W. & Guglielmo, C. G. Rapid loss of fat but not lean mass prior to chick provisioning supports the flight efficiency hypothesis in tree swallows. Funct. Ecol. 26, 895–903 (2012).

    Article  Google Scholar 

  55. Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R version 0.2 4 (2019).

  56. Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400 (2017).

    Article  Google Scholar 

  57. Arnqvist, G. Mixed models offer no freedom from degrees of freedom. Trends Ecol. Evol. (2020).

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Acknowledgements

We would like to thank the dozens of undergraduate field crew who collected data at the Ithaca field site, making this project possible. This work is supported through funding from the National Science Foundation (NSF) IBN-0131437, DEB-0717021 and DEB-1242573 (to D.W.W.) and NSF IOS-1457251 (to M.N.V.).

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Contributions

This study was conceived by J.R.S. and D.W.W. with inputs from all coauthors. Both D.W.W. and M.N.V. provided long-term data on juvenile and adult tree swallow morphology. J.R.S. analysed data with assistance from D.W.W., and J.R.S. and C.W.T. wrote the manuscript with significant contributions from C.C.T., M.N.V. and D.W.W.

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Correspondence to J. Ryan Shipley.

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Nature Climate Change thanks Jan-Åke Nilsson and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Sample sites for weather data from the global historical climatology network (GHNCd) from 1986–2020.

a) Weather stations within 100 km from the Ithaca, NY site (42.5037 N, −76.4661) used during the reproduction life history stage. b) Weather data sampled within 177 km of the overwintering habitat of Ithaca Tree Swallows (26.6503 N, −81.5003 W). c) Weather station sites sampled within 177 km of the midpoint during spring migration (36.2908 N, −78.4121 W) as they return to breed in Ithaca, NY. All points are determined via direct observation of from geolocators from Tree Swallows recaptured in Ithaca, NY.

Extended Data Fig. 2 Summary statistics of chicks sampled from 1986–2020.

a) Tree Swallow chicks gain mass rapidly post hatching; however, growth rate slows after approximately day 12. b) The majority of chicks were sampled around 10 days post hatch. c) Annual counts of chicks that were measured by year.

Extended Data Fig. 3 Tree Swallow chick body mass in relationship to survival from 1986–2020.

a) The probability of recapture increases from 75 to more than 90 percent for chicks between 15 and 20 grams at day 12 post hatch. b) In all years where chicks were recaptured, recaptured chicks were typically more than 1 standard deviation larger than the annual mean for all chicks in their hatch year. c.) When compiled across all years, both recaptured male and female chicks are consistently larger than their non recaptured counterparts.

Extended Data Table 1 Model selection of generalized linear mixed models between habitat and annual measurements of Tree Swallow adults

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Shipley, J.R., Twining, C.W., Taff, C.C. et al. Selection counteracts developmental plasticity in body-size responses to climate change. Nat. Clim. Chang. 12, 863–868 (2022). https://doi.org/10.1038/s41558-022-01457-8

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