Abstract
The information content of a sexual signal may predict its importance in a multiple signal system. Many studies have correlated sexual signal expression with the absolute levels of nutrient reserves. In contrast, the changes of nutrient reserves associated with signal expression are largely unknown in the wild due to technical limitations although they are important determinants of signal information content. We compared two visual and eight acoustic sexual traits in male collared flycatchers to see whether the nutritional correlates of expression predict the role of the signal in sexual selection. We used single point assays of plasma lipid metabolites to estimate short-term changes in nutritional state in relation to sexual trait expression during courtship. As a measure of sexual selection, we estimated the relationship with pairing latency after arrival in a 4-year dataset. Males which found a mate rapidly were characterized by large wing and forehead patches, but small song strophe complexity and small figure repertoire size. Traits more strongly related to pairing latency were also more closely related to changes in nutrient reserves. This indicates a link between signal role and information content. Small wing patches and, surprisingly, complex songs seemed to indicate poor phenotypic quality and were apparently disfavoured at mate acquisition in our population. Future studies of the information content of sexual traits, especially dynamic traits such as song, may benefit from the use of plasma metabolite profiles as non-invasive indicators of short-term changes in body condition.
Similar content being viewed by others
References
Andersson S (1994) Costs of sexual advertising in the lekking Jackson widowbird. Condor 96:1–10
Ballentine B, Hyman J, Nowicki S (2004) Vocal performance influences female response to male bird song: an experimental test. Behav Ecol 15:163–168
Balmford A, Thomas ALR, Jones IL (1993) Aerodynamics and the evolution of long tails in birds. Nature 361:628–631
Berg ML, Beintema NH, Welbergen JA, Komdeur J (2005) Singing as a handicap: the effects of food availability and weather on song output in the Australian reed warbler Acrocephalus australis. J Avian Biol 36:201–109
Birkhead TR, Fletcher F, Pellatt EJ (1998) Sexual selection in the zebra finch Taeniopygia guttata: condition, sex traits and immune capacity. Behav Ecol Sociobiol 44:179–191
Blackmer AL, Mauck RA, Ackerman JT, Huntington CE, Nevitt GA, Williams JB (2005) Exploring individual quality: basal metabolic rate and reproductive performance in storm-petrels. Behav Ecol 16:906–913
Bókony V, Lendvai ÁZ, Liker A (2006) Multiple cues in status signalling: the role of wingbars in aggressive interactions of male house sparrows. Ethology 112:947–954
Both C, Visser ME (2001) Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411:296–298
Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83
Buchanan KL, Catchpole CK (1997) Female choice in the sedge warbler, Acrocephalus schoenobaenus: multiple cues from song and territory quality. Proc Biol Sci 264:521–526
Buchanan KL, Catchpole CK, Lewis JW, Lodge A (1999) Song as an indicator of parasitism in the sedge warbler. Anim Behav 57:307–314
Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595
Cardoso GC, Atwell JA, Ketterson ED, Price TD (2007) Inferring performance in the songs of dark-eyed juncos (Junco hyemalis). Behav Ecol 18:1051–1057
Catchpole CK, Slater PJB (1995) Bird song: biological themes and variations. Cambridge University Press, Cambridge
Cohen J (1988) Statistical power analysis for the behavioural sciences, 2nd edn. Lawrence Erlbaum, Hillsdale
Cotton S, Fowler K, Pomiankowski A (2004) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc Biol Sci 271:771–783
Dale S, Slagsvold T (1996) Plumage colouration and conspicuousness in birds: experiments with the pied flycatcher. Auk 113:849–857
Eens M, Pinxten R, Verheyen RF (1991) Male song as a cue for mate choice in European starlings. Behaviour 116:210–238
Forstmeier W, Kempenaers B, Meyer A, Leisler B (2002) A novel song parameter correlates with extra-pair paternity and reflects male longevity. Proc Biol Sci 269:1479–1485
Garamszegi LZ (2006) Comparing effect sizes across variables: generalization without the need for Bonferroni correction. Behav Ecol 17:682–687
Garamszegi LZ, Boulinier T, Møller AP, Török J, Michl G, Nichols JD (2002) The estimation of size and change in composition of avian song repertoires. Anim Behav 63:623–630
Garamszegi LZ, Møller AP, Török J, Michl G, Péczely P, Richard M (2004) Immune challenge mediates vocal communication in a passerine bird: an experiment. Behav Ecol 15:148–157
Garamszegi LZ, Heylen D, Møller AP, Eens M, de Lope F (2005) Age-dependent health status and song characteristics in the barn swallow. Behav Ecol 16:580–591
Garamszegi LZ, Hegyi G, Heylen D, Ninni P, de Lope F, Eens M, Møller AP (2006a) The design of complex sexual traits in male barn swallows: associations between signal attributes. J Evol Biol 19:2052–2066
Garamszegi LZ, Rosivall B, Hegyi G, Szöllősi E, Török J, Eens M (2006b) Determinants of male territorial behaviour in a Hungarian collared flycatcher population: plumage traits of residents and challengers. Behav Ecol Sociobiol 60:663–671
Garamszegi LZ, Calhim S, Dochtermann N, Hegyi G, Hurd PL, Jørgensen C, Kutsukake N, Lajeunesse MJ, Pollard KA, Schielzeth H, Symonds MRE, Nakagawa S (2009) Changing philosophies and tools for statistical inferences in behavioural ecology. Behav Ecol 20:1363–1375
Gil D, Gahr M (2002) The honesty of bird song: multiple constraints for multiple traits. Trends Ecol Evol 17:133–141
Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546
Hanssen SA, Folstad I, Erikstad KE (2006) White plumage reflects individual quality in female eiders. Anim Behav 71:337–343
Hegyi G, Török J, Tóth L (2002) Qualitative population divergence in proximate determination of a sexually selected trait in the collared flycatcher. J Evol Biol 15:710–719
Hegyi G, Török J, Tóth L, Garamszegi LZ, Rosivall B (2006) Rapid temporal change in the expression and age-related information content of a sexually selected trait. J Evol Biol 19:228–238
Hegyi G, Török J, Garamszegi LZ, Rosivall B, Szöllősi E, Hargitai R (2007) Dynamics of multiple sexual signals in relation to climatic conditions. Evol Ecol Res 9:905–920
Hill GE (1991) Plumage colouration is a sexually selected indicator of male quality. Nature 350:337–339
Hill GE, Montgomerie R (1994) Plumage colour signals nutritional condition in the house finch. Proc Biol Sci 258:47–52
Houle D, Kondrashov AS (2002) Coevolution of costly mate choice and condition-dependent display of good genes. Proc Biol Sci 269:97–104
Höglund J, Eriksson M, Lindell E (1990) Females of the lek-breeding great snipe, Gallinago media, prefer males with white tails. Anim Behav 40:23–32
Hunt J, Bussiére LC, Jennions MD, Brooks R (2004) What is genetic quality? Trends Ecol Evol 19:329–333
Jenni L, Jenni-Eiermann S (1996) Metabolic responses to diurnal feeding patterns during the postbreeding, moulting and migratory periods in passerine birds. Funct Ecol 10:73–80
Jenni L, Schwilch R (2001) Plasma metabolite levels indicate change in body mass in reed warblers Acrocephalus scirpaceus. Avian Sci 1:55–65
Jenni-Eiermann S, Jenni L (1994) Plasma metabolite levels predict individual body mass changes in a small long-distance migrant, the garden warbler. Auk 111:888–899
Johnstone RA (1996) Multiple displays in animal communication: ‘Backup signals’ and ‘multiple messages’. Phil Trans R Soc B 351:329–338
Kern MD, Bacon W, Long D, Cowie RJ (2007) Blood metabolite levels in normal and handicapped pied flycatchers rearing broods of different sizes. Comp Biochem Physiol A 147:70–76
Kodric-Brown A (1993) Female choice of multiple male criteria in guppies: interacting effects of dominance, colouration and courtship. Behav Ecol Sociobiol 32:415–420
Kokko H (2001) Fisherian and “good genes” benefits of mate choice: how (not) to distinguish between them. Ecol Lett 4:322–326
Kokko H, Brooks R, McNamara JM, Houston AI (2002) The sexual selection continuum. Proc Biol Sci 269:1331–1340
Kose M, Møller AP (1999) Sexual selection, feather breakage and parasites: the importance of white spots in the tail of the barn swallow (Hirundo rustica). Behav Ecol Sociobiol 45:430–436
Kose M, Mänd R, Møller AP (1999) Sexual selection for white tail spots in the barn swallow in relation to habitat choice by feather lice. Anim Behav 58:1201–1205
Lampe HM, Saetre G-P (1995) Female pied flycatchers prefer males with larger song repertoires. Proc Biol Sci 262:163–167
Masello JF, Quillfeldt P (2004) Are haematological parameters related to body condition, ornamentation and breeding success in wild burrowing parrots Cyanoliseus patagonus? J Avian Biol 35:445–454
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 59:658–671
McGlothlin JW, Duffy DL, Henry-Freeman JL, Ketterson ED (2007) Diet quality affects an attractive white plumage pattern in dark-eyed juncos (Junco hyemalis). Behav Ecol Sociobiol 61:1391–1399
Mennill DJ, Doucet SM, Montgomerie R, Ratcliffe LM (2003) Achromatic colour variation in black-capped chickadees, Poecile atricapilla: black and white signals of sex and rank. Behav Ecol Sociobiol 53:350–357
Møller AP, Mousseau TA (2003) Mutation and sexual selection: a test using barn swallows from Chernobyl. Evolution 57:2139–2146
Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments? Behav Ecol Sociobiol 32:167–176
Møller AP, Christe P, Lux E (1999) Parasitism, host immune function, and sexual selection. Q Rev Biol 74:3–20
Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605
Nowicki S, Searcy WA, Peters S (2002) Brain development, song learning and mate choice in birds: a review and experimental test of the “nutritional stress hypothesis”. J Comp Physiol A 188:1003–1014
O’Loghlen AL, Rothstein SI (1995) Culturally correct song dialects are associated with male age and female song preferences in wild populations of brown-headed cowbirds. Behav Ecol Sociobiol 36:251–259
Otis DL, Burnham KP, White GC, Anderson DR (1978) Statistical inference from capture data on closed animal populations. Wildl Monogr 62:1–135
Owen JC, Sogge MK, Kern MD (2005) Habitat and sex differences in physiological condition of breeding southwestern willow flycatchers (Empidonax traillii extimus). Auk 122:1261–1270
Palleroni A, Miller CT, Hauser M, Marler P (2005) Predation: prey plumage adaptation against falcon attack. Nature 434:973–974
Pryke SR, Andersson S, Lawes MJ (2001) Sexual selection of multiple handicaps in the red-collared widowbird: female choice of tail length but not carotenoid display. Evolution 55:1452–1463
Qvarnström A (1997) Experimentally increased badge size increases male competition and reduces male parental care in the collared flycatcher. Proc Biol Sci 264:1225–1231
Qvarnström A, Pärt T, Sheldon BC (2000) Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature 405:344–347
Rehsteiner U, Geisser H, Reyer H-U (1998) Singing and mating success in water pipits: one specific song element makes all the difference. Anim Behav 55:1471–1481
Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239
Robson TE, Goldizen AW, Green DJ (2005) The multiple signals assessed by female satin bowerbirds: could they be used to narrow down females’ choices of mates? Biol Lett 1:264–267
Rohwer S, Ewald PW (1981) The cost of dominance and advantage of subordination in a badge signalling system. Evolution 35:441–454
Rowe L, Houle D (1996) The lek paradox and the capture of genetic variance by condition-dependent traits. Proc Biol Sci 263:1415–1421
Scheuber H, Jacot A, Brinkhof MWG (2004) Female preference for multiple condition-dependent components of a sexually selected signal. Proc Biol Sci 271:2453–2457
Schluter D, Price T (1993) Honesty, perception and population divergence in sexually selected traits. Proc Biol Sci 253:117–122
Searcy WA, Nowicki S, Hughes M, Peters S (2002) Geographic song discrimination in relation to dispersal distances in song sparrows. Am Nat 159:221–230
Smith SB, McWilliams SR, Guglielmo CG (2007) Effect of diet composition on plasma metabolite profiles in a migratory songbird. Condor 109:48–58
Specht R (1999) Avisoft SasLab Pro: a PC program for sonagraphic analysis. Users guide. Avisoft Bioacoustics, Berlin
Spencer KA, Buchanan KL, Goldsmith AR, Catchpole CK (2004) Developmental stress, social rank and song complexity in the European starling (Sturnus vulgaris). Proc Biol Sci 271:S121–S123
Thomas RJ (2002) The costs of singing in nightingales. Anim Behav 63:959–966
Thomas RJ, Cuthill IC, Goldsmith AR, Cosgrove DF, Lidgate HC, Burdett Proctor SH (2003) The trade-off between singing and mass gain in a daytime-singing bird, the European robin. Behaviour 140:387–404
Tomkins JL, Radwan J, Kotiaho JS, Tregenza T (2004) Genic capture and resolving the lek paradox. Trends Ecol Evol 19:323–328
Török J, Hegyi G, Garamszegi LZ (2003) Depigmented wing patch size is a condition-dependent indicator of viability in male collared flycatchers. Behav Ecol 14:382–388
Török J, Hegyi G, Tóth L, Könczey R (2004) Unpredictable food supply modifies costs of reproduction and hampers individual optimization. Oecologia 141:432–443
Vallet E, Beme I, Kreutzer M (1998) Two-note syllables in canary songs elicit high levels of sexual display. Anim Behav 55:291–297
Vehrencamp SL (2000) Handicap, index, and conventional signal elements of bird song. In: Espmark Y, Amundsen T, Rosenqvist G (eds) Animal signals. Tapir Academic, Trondheim, pp 277–300
Veiga JP, Puerta M (1996) Nutritional constraints determine the expression of a sexual trait in the house sparrow, Passer domesticus. Proc Biol Sci 263:229–234
Weatherhead PJ, Metz KJ, Bennett GF, Irwin RE (1993) Parasite faunas, testosterone and secondary sexual traits in male red-winged blackbirds. Behav Ecol Sociobiol 33:13–23
Wilkinson GS, Taper M (1999) Evolution of genetic variation for condition-dependent traits in stalk-eyed flies. Proc Biol Sci 266:1685–1690
Williams TD, Guglielmo CD, Egeler O, Martyniuk CJ (1999) Plasma lipid metabolites provide information on mass change over several days in captive western sandpipers. Auk 116:994–1000
Acknowledgements
The authors are grateful to R. Hargitai, M. Herényi and B. Rosivall for their help in the field. This work was supported by Országos Tudományos Kutatási Alapprogramok (grant numbers T49650, T49678, PD72117 to J.T., L.Z.G. and G.H., respectively), a Bolyai János fellowship to G.H. and support from Fonds voor Wetenschapelijk Onderzoek Flanders and the University of Antwerp to M.E., L.Z.G. and G.H.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hegyi, G., Szöllősi, E., Jenni-Eiermann, S. et al. Nutritional correlates and mate acquisition role of multiple sexual traits in male collared flycatchers. Naturwissenschaften 97, 567–576 (2010). https://doi.org/10.1007/s00114-010-0672-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00114-010-0672-0