Advertisement

Evolutionary Biology

, Volume 42, Issue 3, pp 349–358 | Cite as

Patterns of Fluctuating Selection on Morphological and Reproductive Traits in Female Tree Swallow (Tachycineta bicolor)

  • Antoine Millet
  • Fanie Pelletier
  • Marc Bélisle
  • Dany Garant
Research Article

Abstract

Temporally replicated studies are essential to describe and understand selection in natural populations. Selection patterns can differ among life stages representing different fitness components. Despite the increasing number of long-term studies, yearly estimates of fluctuation in strength and direction are mostly available from studies conducted on a limited number of years. Based on a population of Tree swallows (Tachycineta bicolor) monitored over 10,200 km2 in Southern Québec, Canada, since 2004, we investigated how patterns of selection may change across breeding stages by dividing the overall selection at the nesting stage (number of fledglings produced) into hatchling (number of hatchlings produced) and fledgling (number of hatchlings having successfully fledged) selection stages. We assessed fluctuation in selection gradients on two morphological (body mass and wing length) and two reproductive (laying date and clutch size) traits in females. We found significant positive selection gradients for body mass and clutch size and negative selection gradients for laying date, though the latter only during the fledgling selection stage. We also found that selection gradients on reproductive traits significantly fluctuated in direction and/or strength among years but only during the hatchling breeding stage. Our results thus emphasize the need to consider how selection events may be fluctuating in time and among breeding stages and the importance of these patterns for the maintenance of phenotypic variation in wild populations.

Keywords

Selection gradients Fluctuating selection Laying date Clutch size Body mass Wing length Birds 

Notes

Acknowledgments

We would like to thank all the students and field assistants who helped gathering the data over the years, as well as the 40 farms owners for providing access to their land. We thank Cédric Frenette Dussault and three anonymous reviewers for comments on a previous draft version. This work was funded by grants from the Fonds de Recherche du Québec—Nature et Technologies (FRQNT) (D. G., F. P., M. B.), by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grants (D. G., F. P., M. B.) and by the Canada Research Chairs program (F.P., M. B.).

Supplementary material

11692_2015_9333_MOESM1_ESM.docx (408 kb)
Supplementary material 1 (DOCX 407 kb)

References

  1. Arnold, S. J., & Duvall, D. (1994). Animal mating systems: A synthesis based on selection theory. The American Naturalist, 143(2), 317–348. doi: 10.2307/2462646.CrossRefGoogle Scholar
  2. Arnold, S. J., & Wade, M. J. (1984). On the measurement of natural and sexual selection: Applications. Evolution, 38(4), 720–734. doi: 10.2307/2408384.CrossRefGoogle Scholar
  3. Bell, G. (2010). Fluctuating selection: The perpetual renewal of adaptation in variable environments. Philosophical Transactions of the Royal Society B: Biological Sciences, 365(1537), 87–97. doi: 10.1098/rstb.2009.0150.CrossRefGoogle Scholar
  4. Both, C., Bouwhuis, S., Lessells, C. M., & Visser, M. E. (2006). Climate change and population declines in a long-distance migratory bird. Nature, 441(7089), 81–83. doi: 10.1038/nature04539.CrossRefPubMedGoogle Scholar
  5. Bowlin, M. S., & Winkler, D. W. (2004). Natural variation in flight performance is related to timing of breeding in three swallows (Tachycineta bicolor) in New York. The Auk, 121(2), 345–353. doi:10.1642/0004-8038(2004)121[0345:nvifpi]2.0.co;2.CrossRefGoogle Scholar
  6. Carroll, S. P., Hendry, A. P., Reznick, D. N., & Fox, C. W. (2007). Evolution on ecological time-scales. Functional Ecology, 21(3), 387–393. doi: 10.1111/j.1365-2435.2007.01289.x.CrossRefGoogle Scholar
  7. Charmantier, A., McCleery, R. H., Cole, L. R., Perrins, C., Kruuk, L. E. B., & Sheldon, B. C. (2008). Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science, 320(5877), 800–803. doi: 10.1126/science.1157174.CrossRefPubMedGoogle Scholar
  8. Chenoweth, S. F., & Blows, M. W. (2005). Contrasting mutual sexual selection on homologous signal traits in Drosophila serrata. The American Naturalist, 165(2), 281–289. doi: 10.1086/427271.CrossRefPubMedGoogle Scholar
  9. Darimont, C. T., Carlson, S. M., Kinnison, M. T., Paquet, P. C., Reimchen, T. E., & Wilmers, C. C. (2009). Human predators outpace other agents of trait change in the wild. Proceedings of the National Academy of Sciences, 106(3), 952–954. doi: 10.1073/pnas.0809235106.CrossRefGoogle Scholar
  10. Dunn, P. O., Winkler, D. W., Whittingham, L. A., Hannon, S. J., & Robertson, R. J. (2011). A test of the mismatch hypothesis: How is timing of reproduction related to food abundance in an aerial insectivore? Ecology, 92(2), 450–461. doi: 10.1890/10-0478.1.CrossRefPubMedGoogle Scholar
  11. Endler, J. A. (1986). Natural selection in the wild. Princeton: Princeton University Press.Google Scholar
  12. Garant, D., Hadfield, J. D., Kruuk, L. E. B., & Sheldon, B. C. (2008). Stability of genetic variance and covariance for reproductive characters in the face of climate change in a wild bird population. Molecular Ecology, 17(1), 179–188. doi: 10.1111/j.1365-294X.2007.03436.x.CrossRefPubMedGoogle Scholar
  13. Garant, D., Kruuk, L. E. B., McCleery, R. H., & Sheldon, B. C. (2007). The effects of environmental heterogeneity on multivariate selection on reproductive traits in female great tits. Evolution, 61(7), 1546–1559. doi: 10.1111/j.1558-5646.2007.00128.x.CrossRefPubMedGoogle Scholar
  14. Ghalambor, C. K., McKay, J. K., Carroll, S. P., & Reznick, D. N. (2007). Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology, 21(3), 394–407. doi: 10.1111/j.1365-2435.2007.01283.x.CrossRefGoogle Scholar
  15. Ghilain, A., & Bélisle, M. (2008). Breeding success of tree swallows along a gradient of agricultural intensification. Ecological Applications, 18(5), 1140–1154. doi: 10.1890/07-1107.1.CrossRefPubMedGoogle Scholar
  16. Gienapp, P., Teplitsky, C., Alho, J. S., Mills, J. A., & Merilä, J. (2008). Climate change and evolution: Disentangling environmental and genetic responses. Molecular Ecology, 17(1), 167–178. doi: 10.1111/j.1365-294X.2007.03413.x.CrossRefPubMedGoogle Scholar
  17. Grant, P. R., & Grant, B. R. (2002). Unpredictable evolution in a 30-year study of Darwin’s finches. Science, 296(5568), 707–711.CrossRefPubMedGoogle Scholar
  18. Heaney, V., & Monaghan, P. (1996). Optimal allocation of effort between reproductive phases: The trade-off between incubation costs and subsequent brood rearing capacity. Proceedings of the Royal Society of London. Series B: Biological Sciences, 263(1377), 1719–1724. doi: 10.1098/rspb.1996.0251.CrossRefGoogle Scholar
  19. Hendry, A. P., Farrugia, T. J., & Kinnison, M. T. (2008). Human influences on rates of phenotypic change in wild animal populations. Molecular Ecology, 17(1), 20–29. doi: 10.1111/j.1365-294X.2007.03428.x.CrossRefPubMedGoogle Scholar
  20. Husby, A., Hille, S. M., & Visser, M. E. (2011a). Testing mechanisms of Bergmann’s rule: Phenotypic decline but no genetic change in body size in three passerine bird populations. The American Naturalist, 178(2), 202–213. doi: 10.1086/660834.CrossRefPubMedGoogle Scholar
  21. Husby, A., Visser, M. E., & Kruuk, L. E. B. (2011b). Speeding up microevolution: The effects of increasing temperature on selection and genetic variance in a wild bird population. PLoS Biology, 9(2), e1000585. doi: 10.1371/journal.pbio.1000585.PubMedCentralCrossRefPubMedGoogle Scholar
  22. Kawecki, T. J., & Ebert, D. (2004). Conceptual issues in local adaptation. Ecology Letters, 7(12), 1225–1241.CrossRefGoogle Scholar
  23. Kingsolver, J. G., Diamond, S. E., Siepielski, A. M., & Carlson, S. M. (2012). Synthetic analyses of phenotypic selection in natural populations: Lessons, limitations and future directions. Evolutionary Ecology, 26(5), 1101–1118. doi: 10.1007/s10682-012-9563-5.CrossRefGoogle Scholar
  24. Lande, R., & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution, 37(6), 1210–1226. doi: 10.2307/2408842.CrossRefGoogle Scholar
  25. Lane, J. E., Kruuk, L. E. B., Charmantier, A., Murie, J. O., & Dobson, F. S. (2012). Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature, 489(7417), 554–557. doi: 10.1038/nature11335.CrossRefPubMedGoogle Scholar
  26. Lebigre, C., Arcese, P., & Reid, J. M. (2013). Decomposing variation in male reproductive success: Age-specific variances and covariances through extra-pair and within-pair reproduction. Journal of Animal Ecology, 82(4), 872–883. doi: 10.1111/1365-2656.12063.CrossRefPubMedGoogle Scholar
  27. Lessard, A., Bourret, A., Bélisle, M., Pelletier, F., & Garant, D. (2014). Individual and environmental determinants of reproductive success in male tree swallow (Tachycineta bicolor). Behavioral Ecology and Sociobiology, 68(5), 733–742. doi: 10.1007/s00265-014-1686-y.CrossRefGoogle Scholar
  28. Martin, T. E., & Schwabl, H. (2008). Variation in maternal effects and embryonic development rates among passerine species. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1497), 1663–1674. doi: 10.1098/rstb.2007.0009.CrossRefGoogle Scholar
  29. McGlothlin, J. W. (2010). Combining selective episodes to estimate lifetime nonlinear selection. Evolution, 64(5), 1377–1385. doi: 10.2307/40663892.PubMedGoogle Scholar
  30. Møller, A. P. (2013). Long-term trends in wind speed, insect abundance and ecology of an insectivorous bird. Ecosphere, 4(1), 6. doi: 10.1890/es12-00310.1.CrossRefGoogle Scholar
  31. Møller, A. P., Chabi, Y., Cuervo, J. J., De Lope, F., Kilpimaa, J., Kose, M., et al. (2006). An analysis of continent-wide patterns of sexual selection in a passerine bird. Evolution, 60(4), 856–868. doi: 10.1111/j.0014-3820.2006.tb01162.x.CrossRefPubMedGoogle Scholar
  32. Møller, A. P., & Szép, T. (2002). Survival rate of adult barn swallos Hirundo rustica in relation to sexual selection and reproduction. Ecology, 83(8), 2220–2228. doi:10.1890/0012-9658(2002)083[2220:sroabs]2.0.co;2.CrossRefGoogle Scholar
  33. Morrissey, M. B., & Hadfield, J. D. (2012). Directional selection in temporally replicated studies is remarkably consistent. Evolution, 66(2), 435–442. doi: 10.1111/j.1558-5646.2011.01444.x.CrossRefPubMedGoogle Scholar
  34. Nooker, J. K., Dunn, P. O., Whittingham, L. A., & Murphy, M. T. (2005). Effects of food abundance, weather, and female condition on reproduction in tree swallows (Tachycineta bicolor). The Auk, 122(4), 1225–1238. doi:10.1642/0004-8038(2005)122[1225:eofawa]2.0.co;2.CrossRefGoogle Scholar
  35. Perrins, C. M. (1970). The timing of birds’ breeding seasons. Ibis, 112(2), 242–255. doi: 10.1111/j.1474-919X.1970.tb00096.x.CrossRefGoogle Scholar
  36. Pischedda, A., & Rice, W. R. (2012). Partitioning sexual selection into its mating success and fertilization success components. Proceedings of the National Academy of Sciences, 109(6), 2049–2053. doi: 10.1073/pnas.1110841109.CrossRefGoogle Scholar
  37. Porlier, M., Charmantier, A., Bourgault, P., Perret, P., Blondel, J., & Garant, D. (2012). Variation in phenotypic plasticity and selection patterns in blue tit breeding time: Between- and within-population comparisons. Journal of Animal Ecology, 81(5), 1041–1051. doi: 10.1111/j.1365-2656.2012.01996.x.CrossRefPubMedGoogle Scholar
  38. Przybylo, R., Sheldon, B. C., & Merilä, J. (2000). Patterns of natural selection on morphology of male and female collared flycatchers (Ficedula albicollis). Biological Journal of the Linnean Society, 69(2), 213–232. doi: 10.1111/j.1095-8312.2000.tb01199.x.CrossRefGoogle Scholar
  39. R Development Core Team. (2013). R: A language and environment for statistical computing. Vienna: Austria.Google Scholar
  40. Reed, T. E., Jenouvrier, S., & Visser, M. E. (2013). Phenological mismatch strongly affects individual fitness but not population demography in a woodland passerine. Journal of Animal Ecology, 82(1), 131–144. doi: 10.1111/j.1365-2656.2012.02020.x.CrossRefPubMedGoogle Scholar
  41. Reid, J. M., Monaghan, P., & Ruxton, G. D. (2000). Resource allocation between reproductive phases: The importance of thermal conditions in determining the cost of incubation. Proceedings of the Royal Society of London. Series B: Biological Sciences, 267(1438), 37–41. doi: 10.1098/rspb.2000.0963.PubMedCentralCrossRefPubMedGoogle Scholar
  42. Rioux Paquette, S., Garant, D., Pelletier, F., & Bélisle, M. (2013). Seasonal patterns in Tree Swallow prey (Diptera) abundance are affected by agricultural intensification. Ecological Applications, 23(1), 122–133. doi: 10.1890/12-0068.1.CrossRefGoogle Scholar
  43. Rioux Paquette, S., Pelletier, F., Garant, D., & Bélisle, M. (2014). Severe recent decrease of adult body mass in a declining insectivorous bird population. Proceedings of the Royal Society B: Biological Sciences,. doi: 10.1098/rspb.2014.0649.PubMedCentralPubMedGoogle Scholar
  44. Robillard, A., Garant, D., & Bélisle, M. (2013). The Swallow and the Sparrow: How agricultural intensification affects abundance, nest site selection and competitive interactions. Landscape Ecology, 28(2), 201–215. doi: 10.1007/s10980-012-9828-y.CrossRefGoogle Scholar
  45. Schluter, D., Price, T. D., & Rowe, L. (1991). Conflicting selection pressures and life history trade-offs. Proceedings of the Royal Society of London. Series B: Biological Sciences, 246(1315), 11–17. doi: 10.1098/rspb.1991.0118.CrossRefGoogle Scholar
  46. Sheldon, B. C., Kruuk, L. E. B., & Merilä, J. (2003). Natural selection and inheritance of breeding time and clutch size in the collared flycatcher. Evolution, 57(2), 406–420. doi: 10.1111/j.0014-3820.2003.tb00274.x.CrossRefPubMedGoogle Scholar
  47. Shutler, D., Hussell, D. J. T., Norris, D. R., Winkler, D. W., Robertson, R. J., Bonier, F., et al. (2012). Spatiotemporal patterns in nest box occupancy by Tree swallows across North America. Avian Conservation and Ecology, 7(1), 3. doi: 10.5751/ace-00517-070103.CrossRefGoogle Scholar
  48. Siepielski, A. M., DiBattista, J. D., & Carlson, S. M. (2009). It’s about time: The temporal dynamics of phenotypic selection in the wild. Ecology Letters, 12(11), 1261–1276.CrossRefPubMedGoogle Scholar
  49. Siepielski, A. M., DiBattista, J. D., Evans, J. A., & Carlson, S. M. (2011). Differences in the temporal dynamics of phenotypic selection among fitness components in the wild. Proceedings of the Royal Society B: Biological Sciences, 278(1711), 1572–1580. doi: 10.1098/rspb.2010.1973.PubMedCentralCrossRefPubMedGoogle Scholar
  50. Tarka, M., Akesson, M., Hasselquist, D., & Hansson, B. (2014). Intralocus sexual conflict over wing length in a wild migratory bird. The American Naturalist, 183(1), 62–73.CrossRefPubMedGoogle Scholar
  51. Tarwater, C. E., & Beissinger, S. R. (2013). Opposing selection and environmental variation modify optimal timing of breeding. Proceedings of the National Academy of Sciences, 110(38), 15365–15370. doi: 10.1073/pnas.1303821110.CrossRefGoogle Scholar
  52. Teplitsky, C., Mouawad, N. G., Balbontin, J., De Lope, F., & Møller, A. P. (2011). Quantitative genetics of migration syndromes: A study of two barn swallow populations. Journal of Evolutionary Biology, 24(9), 2025–2039. doi: 10.1111/j.1420-9101.2011.02342.x.CrossRefPubMedGoogle Scholar
  53. Teplitsky, C., Tarka, M., Møller, A. P., Nakagawa, S., Balbontín, J., Burke, T. A., et al. (2014). Assessing multivariate constraints to evolution across ten long-term avian studies. PLoS ONE, 9(3), e90444. doi: 10.1371/journal.pone.0090444.PubMedCentralCrossRefPubMedGoogle Scholar
  54. van de Pol, M., & Wright, J. (2009). A simple method for distinguishing within-versus between-subject effects using mixed models. Animal Behaviour, 77, 753–758.CrossRefGoogle Scholar
  55. van Tienderen, P. H. (2000). Elasticities and the link between demographic and evolutionary dynamics. Ecology, 81(3), 666–679. doi:10.1890/0012-9658(2000)081[0666:eatlbd]2.0.co;2.CrossRefGoogle Scholar
  56. Verhulst, S., & Nilsson, J.-Å. (2008). The timing of birds’ breeding seasons: A review of experiments that manipulated timing of breeding. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1490), 399–410. doi: 10.1098/rstb.2007.2146.CrossRefGoogle Scholar
  57. Yeh, P. J., & Price, T. D. (2004). Adaptive phenotypic plasticity and the successful colonization of a novel environment. The American Naturalist, 164(4), 531–542. doi: 10.1086/423825.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Antoine Millet
    • 1
  • Fanie Pelletier
    • 1
  • Marc Bélisle
    • 1
  • Dany Garant
    • 1
  1. 1.Département de BiologieUniversité de SherbrookeSherbrookeCanada

Personalised recommendations