Abstract
The selective pressures acting on phenotypes are complex and can vary both spatially and temporally. To elucidate relationships among environmental conditions and selection on a complex morphological trait, we explored spatial and temporal variation in avian bill structure in a common generalist songbird, the Dark-eyed Junco (Junco hyemalis). We measured bill length, width, and depth, and calculated bill surface area for >800 museum specimens collected in California from 1905 to 1980. We then determined which environmental variables (precipitation, temperature, habitat type) acting over which temporal scales (seasonal, annual, hemi-decadal, decadal) explained variation in these measures of bill morphology. Although we had predicted that relationships between environmental parameters and selection on the bill structure would reflect either foraging ecology or thermoregulatory needs, the patterns that we found were more complex and varied with season and among the different bill traits examined. Temperature was consistently a more important predictor of bill morphology than precipitation, although overall support for temperature was still weak. While bill surface area was related to habitat type, linear measures of bill morphology were related to temperature maxima, minima, and variability. Bill morphology was related to temperature maxima in summer; in contrast, both temperature maxima and minima were supported in winter models. Of the climate variables identified as important in our analyses, support was strongest for the measure of decadal temperature variability. The strong relationship between vegetative community and bill surface area revealed by our analyses as well as the unexpected role of decadal temperature variability indicate that consideration of the large-scale context—ecology and climate—in which complex phenotypic traits occur may reveal important patterns of selection that are not evident from studies of more isolated components of natural systems.
Similar content being viewed by others
References
Alcántara JM, Rey PJ (2003) Conflicting selection pressures on seed size: evolutionary ecology of fruit size in a bird-dispersed tree, Olea europaea. J Evol Biol 16:1168–1176
Alexander HJ, Taylor JS, Wu SS, Breden F (2006) Parallel evolution and vicariance in the guppy (Poecilia reticulata) over multiple spatial and temporal scales. Evolution 60(11):2352–2369
American Ornithologists’ Union (1998) Check-list of North American birds, 7th edn. American Ornithologists’ Union, Washington, DC
Andersson M (1982) Sexual selection, natural selection and quality advertisement. Biol J Linn Soc 17:375–393
Babin-Fenske J, Anand M, Alarie Y (2008) Rapid morphological change in stream beetle museum specimens correlates with climate change. Ecol Entomol 33:646–651
Badyaev AV, Young RL, Oh KP, Addison C (2008) Evolution on a local scale: developmental, functional, and genetic bases of divergence in bill form and associated changes in song structure between adjacent habitats. Evolution 62(8):1951–1964
Ballentine B (2006) Morphological adaptation influences the evolution of a mating signal. Evolution 60(9):1936–1944
Balmford A (1996) Extinction filters and current resilience: the significance of past selection pressures for conservation biology. Trends Ecol Evol 5347(5):193–196
Bartoń K (2015) MuMIn: multi-model inference. R package version 1.13.4. http://CRAN.R-project.org/package=MuMIn
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57(1):289–300
Brooks R, Endler JA (2001) Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution 55(5):1002–1015
Burnham KP, Anderson DR (2002) Model selection and multimodal inference: a practical information—theoretic approach, 2nd edn. Springer, New York
Burns KJ, Hackett SJ, Klein NK (2003) Phylogenetic relationships of Neotropical honeycreepers and the evolution of feeding morphology. J Avian Biol 34:360–370
Cardilini APA, Buchanan KL, Sherman CDH, Cassey P, Symonds MRE (2016) Tests of ecogeographical relationships in a non-native species: what rules avian morphology? Oecologia 181(3):783–793
Chandler CR, Ketterson ED, Nolan V, Ziegenfus C (1994) Effects of testosterone on spatial activity in free-ranging male dark-eyed juncos, Junco hyemalis. Anim Behav 47:1445–1455
Danner RM, Greenberg R (2015) A critical season approach to Allen’s rule: bill size declines with winter temperature in a cold temperate environment. J Biogeogr 42(1):114–120
Desrochers A (2010) Morphological response of songbirds to 100 years of landscape change in North America. Ecology 91(6):1577–1582
Endler JA (1983) Natural and sexual selection on color patterns in poeciliid fishes. Environ Biol Fish 9(2):173–190
Fleming IA, Gross MR (1994) Breeding competition in a Pacific salmon (Coho: Oncorhynchus kisutch): measures of natural and sexual selection. Evolution 48(3):637–657
Freed LA, Conant S, Fleischer RC (1987) Evolutionary ecology and radiation of Hawaiian passerine birds. Trends Ecol Evol 2(7):196–203
Freed LA, Medeiros MCI, Cann RL (2016) Multiple reversals of bill length over 1.7 million years in a Hawaiian bird lineage. Am Nat 187(3):363–371
Gómez JM (2004) Bigger is not always better: conflicting selective pressures on seed size in Quercus ilex. Evolution 58(1):71–80
Goodman KR, Kelley JP, Welter SC, Roderick GK, Elias DO (2015) Rapid diversification of sexual signals in Hawaiian Nesosydne planthoppers (Hemiptera: Delphacidae): the relative role of neutral and selective forces. J Evol Biol 28:415–427
Gosler AG (1986) Pattern and process in the bill morphology of the Great Tit Parus major. Ibis 129:451–476
Gotanda KM, Hendry AP (2014) Using adaptive traits to consider potential consequences of temporal variation in selection: male guppy colour through time and space. Biol J Linn Soc 112:108–122
Graber JW, Graber RR (1979) Severe winter weather and bird populations in southern Illinois. Wilson Bull 91(1):88–103
Grant BR, Grant PR (1989) Natural selection in a population of Darwin’s finches. Am Nat 133(3):377–393
Grant BR, Grant PR (1993) Evolution of Darwin’s finches caused by a rare climatic event. Proc R Soc Lond B Biol Sci 251(1331):111–117
Grant BR, Grant PR (1996) High survival of Darwin’s finch hybrids: effects of beak morphology and diets. Ecology 77(2):500–509
Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296:707–712
Greenberg R, Danner RM (2012) The influence of the California marine layer on bill size in a generalist songbird. Evolution 66(12):3825–3835
Greenberg R, Cadena V, Danner RM, Tattersall G (2012) Heat loss may explain bill size differences between birds occupying different habitats. PLoS ONE 7(7):e40933
Greenberg R, Etterson M, Danner RM (2013) Seasonal dimorphism in the horny bills of sparrows. Ecol Evol 3(2):389–398
Guo Q, Hu ZM, Li SG, Li XR, Li XM, Yu GR (2012) Spatial variations in aboveground net primary productivity along a climate gradient in Eurasian temperate grassland: effects of mean annual precipitation and its seasonal distribution. Glob Change Biol 18:3624–3631
Hansen TF, Orzack SH (2005) Assessing current adaptation and phylogenetic inertia as explanations of trait evolution: the need for controlled comparisons. Evolution 59(10):2063–2072
Heinen-Kay JL, Morris KE, Ryan NA, Byerley SL, Venezia RE, Peterson MN, Langerhans RB (2015) A trade-off between natural and sexual selection underlies diversification of a sexual signal. Behav Ecol 26(2):533–542
Herrel A, Podos J, Huber SK, Hendry AP (2005) Bite performance and morphology in a population of Darwin’s finches: implications for the evolution of beak shape. Funct Ecol 19(1):43–48
Jepson Flora Project (ed) (2013) Jepson eFlora. http://ucjeps.berkeley.edu/IJM.html. Accessed 11 Dec 2013
Jønsson KA, Fabre P, Fritz SA, Etienne RS, Ricklefs RE, Jørgensen TB, Fjeldså J, Rahbek C, Ericson PGP, Woog F, Pasquet E, Irestedt M (2012) Ecological and evolutionary determinants for the adaptive radiation of the Madagascan vangas. Proc Nat Acad Sci 109(17):6620–6625
Keiser JT, Ziegenfus CWS, Cristol DA (2005) Homing success of migrant versus nonmigrant dark-eyed juncos (Junco hyemalis). Auk 122(2):608–617
Matthysen E (1989) Seasonal variation in bill morphology of nuthatches Sitta europaea: dietary adaptations or consequences? Ardea 77:117–125
McGlothlin JW, Parker PG, Nolan V, Ketterson ED (2005) Correlational selection leads to genetic integration of body size and an attractive plumage trait in dark-eyed juncos. Evolution 59(3):658–671
McKechnie AE, Wolf BO (2010) Climate change increases the likelihood of catastrophic avian mortality events during extreme heat waves. Biol Lett 6:253–256
Nolan V, Ketterson ED, Cristol DA, Rogers CM, Clotfelter ED, Titus RC, Schoech SJ, Snajdr E (2002) Dark-eyed junco (Junco hyemalis). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca. http://bna.birds.cornell.edu/bna/species/716. Accessed 10 Jul 2015
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421(6918):37–42
Price T (1987) Diet variation in a population of Darwin’s finches. Ecology 68(4):1015–1028
PRISM Climate Group (2015) Oregon State University. http://prism.oregonstate.edu. Accessed 3 Feb 2015
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Rohr JR, Madison DM, Sullivan AM (2003) On temporal variation and conflicting selection pressures: a test of theory using newts. Ecology 84(7):1816–1826
Schluter D, Price TD, Rowe L (1991) Conflicting selection pressures and life history trade-offs. Proc R Soc Lond B Biol Sci 246(1315):11–17
Smith TB, Freed LA, Lepson JK, Carothers JH (1995) Evolutionary consequences of extinctions in populations of a Hawaiian honeycreeper. Conserv Biol 9(1):107–113
Summers RW (1976) The value of bill lengths of museum specimens in biometric studies. Wader Study Group Bull 17:10–11
Symonds MRE, Tattersall GJ (2010) Geographical variation in bill size across bird species provides evidence for Allen’s rule. Am Nat 176(2):188–197
Tattersall GJ, Arnaout B, Symonds MRE (2016) The evolution of the avian bill as a thermoregulatory organ. Biol Rev. doi:10.1111/brv.12299
Templeton CN, Shriner WM (2004) Multiple selection pressures influence Trinidadian guppy (Poecilia reticulata) antipredator behavior. Behav Ecol 15(4):673–678
Tilgar V, Mänd R, Kilgas P, Mägi M (2010) Long-term consequences of early ontogeny in free-living Great Tits Parus major. J Ornithol 151:61–68
Tingley MW, Koo MS, Moritz C, Rush AC, Beissinger SR (2012) The push and pull of climate change causes heterogeneous shifts in avian elevational ranges. Glob Change Biol 18:3279–3290
Acknowledgements
We thank Carla Cicero, Rauri Bowie, Moe Flannery and the California Academy of Sciences, Doug Renwick, Trent Pingenot, HostGIS, Steve Beissinger and the Beissinger lab group, Damian Elias, Quintin Stedman, the Jepson Herbarium, and PRISM for their time, advice, and aid with this project. Three anonymous reviewers provided valuable feedback. KL was supported by an NSF pre-doctoral fellowship (Fellow ID 2010096907).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
LaBarbera, K., Hayes, K.R., Marsh, K.J. et al. Complex relationships among environmental conditions and bill morphology in a generalist songbird. Evol Ecol 31, 707–724 (2017). https://doi.org/10.1007/s10682-017-9906-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-017-9906-3