title: Effects of spring temperatures on the strength of selection on timing of reproduction in a long-distance migratory bird.
abstract: Climate change has differentially affected the timing of seasonal events for interacting trophic levels, and this has often led to increased selection on seasonal timing. Yet, the environmental variables driving this selection have rarely been identified, limiting our ability to predict future ecological impacts of climate change. Using a dataset spanning 31 years from a natural population of pied flycatchers (Ficedula hypoleuca), we show that directional selection on timing of reproduction intensified in the first two decades (1980-2000) but weakened during the last decade (2001-2010). Against expectation, this pattern could not be explained by the temporal variation in the phenological mismatch with food abundance. We therefore explored an alternative hypothesis that selection on timing was affected by conditions individuals experience when arriving in spring at the breeding grounds: arriving early in cold conditions may reduce survival. First, we show that in female recruits, spring arrival date in the first breeding year correlates positively with hatch date; hence, early-hatched individuals experience colder conditions at arrival than late-hatched individuals. Second, we show that when temperatures at arrival in the recruitment year were high, early-hatched young had a higher recruitment probability than when temperatures were low. We interpret this as a potential cost of arriving early in colder years, and climate warming may have reduced this cost. We thus show that higher temperatures in the arrival year of recruits were associated with stronger selection for early reproduction in the years these birds were born. As arrival temperatures in the beginning of the study increased, but recently declined again, directional selection on timing of reproduction showed a nonlinear change. We demonstrate that environmental conditions with a lag of up to two years can alter selection on phenological traits in natural populations, something that has important implications for our understanding of how climate can alter patterns of selection in natural populations.
authors.affiliation: Department of Animal Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.
authors.forename: Marcel E
authors.initials: ME
authors.lastname: Visser
authors.affiliation: Department of Animal Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.
authors.forename: Phillip
authors.initials: P
authors.lastname: Gienapp
authors.affiliation: Centre for Biodiversity Dynamics, Department of Biology, Norwegian University of Science and Technology, Trondheim, Norway; Department of Biosciences, University of Helsinki, Helsinki, Finland.
authors.forename: Arild
authors.initials: A
authors.lastname: Husby
authors.affiliation: Dyers Brae House, School of Biology, University of St Andrews, St Andrews, Fife, United Kingdom.
authors.forename: Michael
authors.initials: M
authors.lastname: Morrisey
authors.affiliation: Department of Animal Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands; Department of Zoology and Animal Cell Biology, Universidad del País Vasco (UPV/EHU), Vitoria-Gasteiz, Spain.
authors.forename: Iván
authors.initials: I
authors.lastname: de la Hera
authors.affiliation: Department of Animal Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands; Department of Zoology and Physical Anthropology, Complutense University of Madrid, Madrid, Spain.
authors.forename: Francisco
authors.initials: F
authors.lastname: Pulido
authors.affiliation: Department of Animal Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands; Animal Ecology Group, Center for Ecological and Evolutionary Studies, University of Groningen, Groningen, The Netherlands.
authors.forename: Christiaan
authors.initials: C
authors.lastname: Both
mesh_terms: D025041:Animal Migration; D000818:Animals; D012098:Reproduction; D012621:Seasons; D020308:Songbirds / Q000502:physiology*; D013696:Temperature
references.citation: PLoS One. 2007 Jun 20;2(6):e539
references.pmid: 17579713
references.citation: PLoS Biol. 2011 Feb;9(2):e1000585
references.pmid: 21408101
references.citation: Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9176-81
references.pmid: 11038566
references.citation: Glob Chang Biol. 2013 Jan;19(1):149-60
references.pmid: 23504727
references.citation: Science. 2008 May 9;320(5877):800-3
references.pmid: 18467590
references.citation: J Evol Biol. 2013 Oct;26(10):2147-53
references.pmid: 23837446
references.citation: Nature. 2003 Jan 2;421(6918):57-60
references.pmid: 12511952
references.citation: Science. 1988 May 6;240(4853):798-9
references.pmid: 3363360
references.citation: PLoS Biol. 2015 Apr 07;13(4):e1002120
references.pmid: 25848856
references.citation: J Anim Ecol. 2013 Jan;82(1):131-44
references.pmid: 22862682
references.citation: Proc Natl Acad Sci U S A. 2008 Oct 21;105(42):16195-200
references.pmid: 18849475
references.citation: Ecology. 2011 Feb;92(2):450-61
references.pmid: 21618924
references.citation: J Anim Ecol. 2014 May;83(3):729-39
references.pmid: 24117440
references.citation: Nature. 2006 May 4;441(7089):81-3
references.pmid: 16672969
references.citation: J Anim Ecol. 2010 Jan;79(1):13-26
references.pmid: 20409158
references.citation: PLoS Biol. 2006 Jul;4(7):e216
references.pmid: 16756391
references.citation: J Anim Ecol. 2009 Jan;78(1):73-83
references.pmid: 18771506
references.citation: J Anim Ecol. 2010 Jan;79(1):98-108
references.pmid: 19694874
references.citation: Oecologia. 2014 Oct;176(2):595-605
references.pmid: 25024104
references.citation: Proc Biol Sci. 2006 Aug 22;273(1597):2009-16
references.pmid: 16846907
references.citation: Trends Ecol Evol. 2011 Oct;26(10):514-22
references.pmid: 21763030
references.citation: Evolution. 1989 May;43(3):485-503
references.pmid: 28568400
references.citation: Proc Biol Sci. 2014 Oct 22;281(1793):
references.pmid: 25165771
references.citation: Parasitology. 2001 May;122(Pt 5):563-9
references.pmid: 11393830
references.citation: Oecologia. 2006 Feb;147(1):164-72
references.pmid: 16328547
references.citation: J Anim Ecol. 2012 Jul;81(4):926-36
references.pmid: 22356622
references.citation: Nature. 2001 May 17;411(6835):296-8
references.pmid: 11357129
references.citation: Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1630-3
references.pmid: 10677510
references.citation: J Anim Ecol. 2013 Jan;82(1):84-95
references.pmid: 22897224
references.citation: Evolution. 1983 Nov;37(6):1210-1226
references.pmid: 28556011
references.citation: Genetics. 2011 Apr;187(4):1099-113
references.pmid: 21242534
references.citation: Anim Behav. 1997 Jul;54(1):153-61
references.pmid: 9268445
references.citation: Proc Natl Acad Sci U S A. 2013 Apr 30;110(18):7360-5
references.pmid: 23589881
references.citation: J Anim Ecol. 2007 Jan;76(1):139-48
references.pmid: 17184362
references.citation: Ecol Lett. 2005 Sep;8(9):952-958
references.pmid: 34517678
references.citation: Proc Biol Sci. 2005 Dec 22;272(1581):2561-9
references.pmid: 16321776
references.citation: Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13379-81
references.pmid: 12370424
references.citation: Evolution. 2012 Feb;66(2):435-42
references.pmid: 22276539
references.citation: Proc Biol Sci. 2008 Mar 22;275(1635):649-59
references.pmid: 18211875
references.citation: Philos Trans R Soc Lond B Biol Sci. 2008 Jul 12;363(1501):2369-75
references.pmid: 18006410
references.citation: Ecology. 2007 Oct;88(10):2620-9
references.pmid: 18027764
references.citation: PLoS Biol. 2014 Apr 01;12(4):e1001828
references.pmid: 24690936
references.citation: Evolution. 1990 Dec;44(8):1947-1955
references.pmid: 28564434
references.citation: Proc Biol Sci. 2012 Jan 7;279(1726):15-6; discussion 17-8
references.pmid: 22031755
references.citation: Proc Biol Sci. 2003 Jul 22;270(1523):1461-6
references.pmid: 12965010
references.citation: Proc Biol Sci. 2001 Feb 7;268(1464):289-94
references.pmid: 11217900
references.citation: Ecology. 2010 Feb;91(2):311-8
references.pmid: 20391994
references.citation: Evolution. 2013 Jul;67(7):2094-100
references.pmid: 23815662