Skip to main content
SpringerLink
Log in

Assortative mating by multiple skin color traits in a seabird with cryptic sexual dichromatism

  • Original Article
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

Abstract

Most seabirds are monochromatic in plumage, yet many of them show multiple colored integuments, typically modulated by sex steroids such as testosterone, which can reflect individual quality and may be under mutual sexual selection. In the Masked Booby Sula dactylatra, both sexes exhibit multiple color traits that vary in their expression either in color (feet ranging from olive to orange, yellowish bill and black mask) or size (mask). Here, we report sexual differences in skin color traits and evaluate whether their expression is related to individual body condition and plasma testosterone, whether different color traits co-vary, and whether Masked Boobies mate assortatively by color. Our results show that Masked Boobies are sexually dichromatic in foot color and monochromatic in bill and mask color. After controlling for body size and testosterone levels, mask size was larger in females than in males. We found a positive relationship between body condition and plasma testosterone in males and females, suggesting a condition-dependence of plasma androgen levels. Interestingly, foot color covaries positively with testosterone levels in individuals with good body condition and negatively in individuals with poor body condition, whereas mask size was positively related with body condition. Taken together, these results suggest that only individuals in good condition could produce more conspicuous traits. Also, we found a negative relationship between mask color and condition, probably due to the fact that melanin-based traits can pleiotropically vary with other functions, including food intake patterns. Finally, within-individual foot color and mask size were positively correlated and pairs mated assortatively with respect to foot color and mask color and size. We suggest that such a mating pattern may result from a scenario where both sexes choose mates based on traits that convey reliable information of individual quality.

Zusammenfassung

Assortative Paarung für unterschiedliche Hautfarben bei Seevögeln mit nicht eindeutigem GeschlechtsdimorphismusDie meisten Seevögel haben einfarbiges Gefieder, viele von ihnen aber Haut in unterschiedlichen Färbungen, die in der Regel durch Geschlechtshormone wie z.B. Testosteron bestimmt werden. Diese Färbungen könnten Hinweise auf individuelle Qualität geben und stünden dann vermutlich unter Selektionsdruck. Beim Maskentölpel (Sula dactylatra) entwickeln beide Geschlechter Färbungen, die in Größe (Maske) oder Farbton variieren können (die Farbe der Füße reicht von oliv bis orange, bei gelben Schnäbeln und schwarzen Masken). Wir berichten hier über Geschlechtsunterschiede in der Hautfärbung und untersuchen, ob deren Ausprägung mit der physischen Verfassung der einzelnen Individuen und ihrem Plasma-Testosteron zusammenhängt, ob unterschiedliche Färbungen kovariieren, und ob sich die Maskentölpel bei den Farben assortativ verpaaren. Unsere Ergebnisse zeigen, dass bei Maskentölpel die Füße geschlechtsabhängig in zwei Farben und die Schnäbel und Masken nur in einer Farbe vorkommen. Nach Feststellen des Geschlechts anhand von Körpergröße und Testosteron-Spiegel, zeigte es sich, dass die Weibchen größere Masken als die Männchen hatten. Wir fanden für beide Geschlechter eine positive Korrelation zwischen physischer Verfassung und Plasma-Testosteron, was auf eine Abhängigkeit der Verfassung vom Androgen-Spiegel hinweist. Interessanterweise kovariiert die Fuß-Färbung bei Individuen in guter physischer Verfassung positiv mit dem Testosteron-Spiegel, aber negativ bei Individuen in schlechter Verfassung, wohingegen die Größe der Maske stets positiv mit der physischen Verfassung korrelierte. Aus diesen Ergebnissen kann geschlossen werden, dass möglicherweise nur Individuen in guter Verfassung stärker auffallende Merkmale zeigen. Wir fanden außerdem eine negative Korrelation zwischen Masken-Färbung und physischer Verfassung, was wahrscheinlich daran liegt, dass auf Melanin basierende Merkmale pleiotropisch mit anderen Funktionen wie z. B. Mustern in der Nahrungsaufnahme zusammenhängen können. Bei Einzelindividuen waren Fuß-Färbung und Masken-Größe positiv korreliert, und in Hinblick auf Fuß- und Masken-Färbung und Masken-Größe verlief die Paarbildung assortativ. Wir denken, dass solch ein Paarbildungs-Muster auf ein Szenario zurückgeführt werden kann, in dem beide Geschlechter ihre Partner anhand von Merkmalen auswählen, die verlässliche Information über die individuelle Qualität geben.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alonso-Alvarez C, Velando A (2001) Effect of testosterone on behaviour of yellow legged gulls in a high density colony during the courtship period. Ethol Sociobiol 13:343–351

    Google Scholar 

  • Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc R Soc Lond B 274:819–825

    Article  CAS  Google Scholar 

  • Amundsen T (2000) Why are female birds ornamented? Trends Ecol Evol 15:149–155

    Article  PubMed  Google Scholar 

  • Amundsen T, Forsgren E, Hansen LTT (1997) On the function of female ornaments: male bluethroats prefer colorful females. Proc R Soc Lond B 264:1579–1586

    Article  Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

  • Blévin P, Tartu S, Angelier F, Leclaire S, Bustnes JO, Moe B, Herzke D, Gabrielsen GW, Chastel O (2014) Integument coloration in relation to persistent organic pollutants and body condition in arctic breeding black-legged kittiwakes (Rissa tridactyla). Sci Total Environ 470–471:248–254

    Article  PubMed  Google Scholar 

  • Blount JD, Surai PF, Nager RG, Houston DC, Møller AP, Trewby ML, Kennedy MW (2002) Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proc R Soc Lond B 269:29–36

    Article  CAS  Google Scholar 

  • Blums P, Nichols JD, Hines JE, Lindberg MS, Mednis A (2005) Individual quality, survival variation and patterns of phenotypic selection on body condition and timing of nesting in birds. Oecologia 143:365–376

    Article  PubMed  Google Scholar 

  • Bókony V, Garamszegi LZ, Hirschenhauser K, Liker A (2008) Testosterone and melanin-based black plumage coloration: a comparative study. Behav Ecol Sociobiol 62:1229–1238

    Article  Google Scholar 

  • Bretagnolle V (1993) Adaptive significance of seabird coloration: the case of procellariiforms. Am Nat 142(1):141–173

    Article  CAS  PubMed  Google Scholar 

  • Buchanan KL, Evans M, Goldsmith AR, Bryan DM, Rowe LV (2001) Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc R Soc Lond B 268:1337–1344

    Article  CAS  Google Scholar 

  • Burley N (1983) The meaning of assortative mating. Ethol Sociobiol 4:191–203

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information theoretic approach. Springer, New York

    Google Scholar 

  • Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595

    Article  PubMed  Google Scholar 

  • Cézilly F (2004) Assortative mating. In Encyclopedia of Animal Behavior 876–881 (M. Bekoff, Editor). Greenwood, Westport

  • Chew BP, Park JS (2004) Carotenoid action on the immune response. J Nutr 134:257S–261S

    CAS  PubMed  Google Scholar 

  • Childress RB, Bennun LA (2002) Sexual character intensity and its relationship to breeding timing, fecundity and mate choice in the great cormorant Phalacrocorax carbo lucidus. J Avian Biol 33:23–30

    Article  Google Scholar 

  • Clutton-Brock T (2009) Sexual selection in females. Anim Behav 77:3–11

    Article  Google Scholar 

  • Cuervo JJ, Palacios MJ, Barbosa A (2009) Beak coloration as a possible sexual ornament in gentoo penguins: sexual dichromatism and relationship to body condition. Polar Biol 32:1305–1314

    Article  Google Scholar 

  • D’Alba L, Van Hemert C, Spencer KA, Heidinger BJ, Gill L, Evans NP, Monaghan P, Handel CM, Shawkey MD (2014) Condition dependence of melanin-based plumage color through feather microstructure. Integr Comp Biol 54:633–644

  • Darwin C (1871) The descent of man, and selection in relation to sex. John Murray, London

  • Dey CJ, Valcu M, Kempenaers B, Dale J (2015) Carotenoid-based bill coloration functions as a social, not sexual, signal in songbirds (Aves: Passeriformes). J Evol Biol 28:250–258

    Article  CAS  PubMed  Google Scholar 

  • Doutrelant C, Grégoire A, Gomez D, Staszewski V, Arnoux E, Tveraa T, Faivre B, Boulinier T (2013) Coloration in Atlantic puffins and blacklegged kittiwakes: monochromatism and links to body condition in both sexes. J Avian Biol 44:451–460

    Google Scholar 

  • Duckworth RE, Medonça MT, Hill GE (2001) A condition dependent link between testosterone and disease resistance in the house finch. Proc R Soc Lond B 268:2467–2472

    Article  CAS  Google Scholar 

  • Ducrest AL, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioral syndromes. Trends Ecol Evol 23:502–510

    Article  PubMed  Google Scholar 

  • Evans SR, Sheldon BC (2012) Quantitative genetics of a carotenoid-based color: heritability and persistent natal environmental effects in the great tit. Am Nat 179:79–94

    Article  PubMed  Google Scholar 

  • Evans MR, Goldsmith AR, Norris SRA (2000) The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behav Ecol Sociobiol 47:156–163

    Article  Google Scholar 

  • Faivre B, Grégoire A, Préault M, Cézilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103

    Article  CAS  PubMed  Google Scholar 

  • Fargallo JA, Martínez-Padilla J, Toledano-Díaz A, Santiago-Moreno J, Dávila JA (2007) Sex and testosterone effects on growth, immunity and melanin coloration of nestling Eurasian kestrels. J Anim Ecol 76:201–209

    Article  PubMed  Google Scholar 

  • Fargallo JA, Velando A, López-Rull I, Gañán N, Lifshitz N, Wakamatsu K, Torres R (2014) Sex-specific phenotypic integration: endocrine profile, coloration and behavior in fledgling boobies. Behav Ecol 25:76–87

    Article  Google Scholar 

  • Fisher RA (1930) The Genetical Theory of Natural Selection. Oxford University Press, Oxford

  • Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

    Article  Google Scholar 

  • Gladbach A, Gladbach DJ, Kempenaers B, Quillfeldt P (2010) Female-specific colouration, carotenoids and reproductive investment in a dichromatic species, the upland goose Chloephaga picta leucoptera. Behav Ecol Sociobiol 64:1779–1789

    Article  PubMed  PubMed Central  Google Scholar 

  • Griffith SC, Parker TH, Olson VA (2006) Melanin- versus carotenoid-based sexual signals: is the difference really so black and red? Anim Behav 71:749–763

    Article  Google Scholar 

  • Griggio M, Valera F, Casas A, Pilastro A (2005) Males prefer ornamented females: a field experiment of male choice in the rock sparrow. Anim Behav 69:1243–1250

    Article  Google Scholar 

  • Håstad O, Ernstdotter E, Ödeen A (2005) Ultraviolet vision and foraging in dip and plunge diving birds. Biol Lett 1:306–309

  • Hill GE (2006) Female mate choice for ornamental coloration. In: Hill G, McGraw K (eds.) Bird coloration. Harvard University Press, Cambridge, pp 137–200

  • Hill GE (2011) Condition-dependent traits as signals of the functionality of vital cellular processes. Ecol Lett 14:625–634

    Article  PubMed  Google Scholar 

  • Hill GE, Montgomerie R (1994) Plumage color signals nutritional condition in the house finch. Proc R Soc Lond B 258:47–52

    Article  Google Scholar 

  • Ismar SM, Baird K, Patel S, Millar CD, Hauber ME (2010) Morphology of the recently re-classified Tasman masked booby (Sula dactylatra tasmani) breeding on the Kermadec Islands. Mar Ornithol 38:105–109

    Google Scholar 

  • Ismar SM, Daniel C, Igic B, Morrison-Whittle PK, Ballard G, Millar CD et al (2014) Sexual plumage dichromatism in a size monomorphic seabird. Wilson J Ornithol 126:417–428

    Article  Google Scholar 

  • Jawor JM, Breitwisch R (2003) Melanin ornaments, honesty, and sexual selection. Auk 120:249–265

    Article  Google Scholar 

  • Jiang Y, Bolnick DI, Kirkpatrick M (2013) Assortative Mating in Animals. Am Nat 181:E125–E138

    Article  PubMed  Google Scholar 

  • Johnsen TS, Hengeveld JD, Blank JL, Yasukawa K, Nolan V Jr (1996) Epaulet brightness and condition in female red-winged blackbirds. Auk 113:356–362

    Article  Google Scholar 

  • Johnstone RA, Reynolds JD, Deutsch JC (1996) Mutual mate choice and sex differences in choosiness. Evolution 50:1382–1391

    Article  Google Scholar 

  • Jones IL, Hunter FM (1993) Mutual sexual selection in a monogamous seabird. Nature 362:238–239

    Article  Google Scholar 

  • Jones IL, Hunter FM (1999) Experimental evidence for mutual inter and intrasexual selection favouring a crested auklet ornament. Anim Behav 57:521–528

    Article  PubMed  Google Scholar 

  • Jones IL, Montgomerie R (1992) Least auklet ornaments: do they function as quality indicators? Behav Ecol Sociobiol 30:43–52

    Article  Google Scholar 

  • Kimball R (2006) Hormonal control of coloration. In: Hill G, McGraw K (eds.) Bird coloration. Harvard University Press, Cambridge, pp 431–468

  • Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38

    Article  Google Scholar 

  • Kraaijeveld K, Gregurke J, Hall C, Komdeur J, Mulder RA (2004) Mutual ornamentation, sexual selection, and social dominance in the Black Swan. Behav Ecol 5:380–389

    Article  Google Scholar 

  • Kraaijeveld K, Kraaijeveld-Smit FJL, Komdeur J (2007) The evolution of mutual ornamentation. Anim Behav 74:657–677

    Article  Google Scholar 

  • Kristiansen KO, Bustnes JO, Folstad I, Helberg M (2006) Carotenoid coloration in great black-backed gull Larus marinus reflects individual quality. J Avian Biol 37:6–12

    Article  Google Scholar 

  • Lande R (1980) Sexual dimorphism sexual selection and adaptation in polygenic characters. Evolution 34:292–305

    Article  Google Scholar 

  • Lande R, Arnold SJ (1985) Evolution of mating preference and sexual dimorphism. J Theor Biol 117:651–664

    Article  CAS  PubMed  Google Scholar 

  • LeBas NR (2006) Female finery is not for males. Trends Ecol Evol 21:170–173

    Article  Google Scholar 

  • Leclaire S, White J, Arnoux E, Faivre B, Vetter N, Hatch SA, Danchin E (2011) Integument coloration signals reproductive success, heterozygosity, and antioxidant levels in chick-rearing black-legged kittiwakes. Naturwissenschaften 98:773–782

    Article  CAS  PubMed  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

  • Linville SU, Breitwisch R (1997) Carotenoid availability and plumage coloration in wild populations of northern cardinals. Auk 114:796–800

    Article  Google Scholar 

  • Linville SU, Breitwisch R, Schilling AJ (1998) Plumage brightness as an indicator of parental care in northern cardinals. Anim Behav 55:119–127

    Article  PubMed  Google Scholar 

  • Lozano GA (1994) Carotenoids, parasites and sexual selection. Oikos 70:309–311

  • Lozano GA (2009) Multiple cues in mate selection: the sexual interference hypothesis. Biosci Hypotheses 2:37–42

    Article  Google Scholar 

  • Machovsky Capuska GE, Huynen L, Lambert D, Raubenheimer D (2011) UVS is rare in seabirds. Vision Res 51:1333–1337

  • Martínez-Padilla J, Mougeot F, Pérez-Rodríguez L, Bortolotti GR (2007) Nematode parasites reduce carotenoid-based signalling in male red grouse. Biol Lett 3:161–164

    Article  PubMed  PubMed Central  Google Scholar 

  • Massaro M, Davis LS, Darby JT (2003) Carotenoid derived ornaments reflect parental quality in male and female yellow-eyed penguins (Megadyptes antipodes). Behav Ecol Sociobiol 55:169–175

    Article  Google Scholar 

  • Maynard Smith J, Harper D (2003) Animal Signals. Oxford University Press, Oxford

  • McGraw KJ, Hill GE (2000) Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc R Soc Lond B 267:1525–1531

    Article  CAS  Google Scholar 

  • Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments? Behav Ecol Sociobiol 32:167–176

    Google Scholar 

  • Møller AP, Garamszegi LZ, Gil D, Hurtrez-Bousses S, Eens M (2005) Correlated evolution of male and female testosterone profiles in birds and its consequences. Behav Ecol Sociobiol 58:534–544

    Article  Google Scholar 

  • Montgomerie R (2006) Analyzing colors. In: Hill G, McGraw K (eds) Bird coloration. Harvard University Press, Cambridge, pp 90–147

  • Monticelli D, Ramos J (2012) Laying date, body mass and tick infestation of nestling tropical Roseate Terns Sterna dougallii predict fledging success, first-year survival and age at first return to the natal colony. Ibis 154:825–837

    Article  Google Scholar 

  • Montoya B, Torres R (2015) Male skin color signals direct and indirect benefits in a species with biparental care. Behav Ecol 26:425–434. doi:10.1093/beheco/aru204

    Article  Google Scholar 

  • Mundy NI (2006) Genetic basis of color variation in wild birds. In: Hill G, McGraw K (eds.) Bird coloration. Harvard University Press, Cambridge, pp 469–506

  • Negro JJ, Bortolotti GR, Tella JL, Fernier KJ, Bird DM (1998) Regulation of intergumentary colour and plasma carotenoids in American Kestrels consistent with sexual selection theory. Funct Ecol 12:307–312

    Article  Google Scholar 

  • Nelson JB (1978) The Sulidae: gannets and boobies. Oxford University Press, Oxford

  • Nelson JB (2005) Pelicans, cormorants, and their relatives: the Pelecaniformes. Oxford University Press, Oxford

  • Nolan PM, Dobson FS, Nicolaus M, Karels TJ, Mcgraw KJ, Jouventin P (2010) Mutual mate choice for colorful traits in king penguins. Ethology 116:635–644

    Google Scholar 

  • Nordeide JT, Kekäläinen J, Janhuhen M, Kortet R (2013) Female ornaments revisited – are they correlated with offspring quality? J Anim Ecol 82:26–38

    Article  PubMed  Google Scholar 

  • Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891

    Article  Google Scholar 

  • Peig J, Green AJ (2010) The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct Ecol 24:1323–1332

    Article  Google Scholar 

  • Pérez-Rodríguez L (2008) Carotenoid-based ornamentation as a dynamic but consistent individual trait. Behav Ecol Sociobiol 62:995–1005

    Article  Google Scholar 

  • Pérez-Rodríguez L, Viñuela J (2008) Carotenoid-based bill and eye ring coloration as honest signals of condition: an experimental test in the red-legged partridge (Alectoris rufa). Naturwissenschaften 95:821–830

    Article  PubMed  Google Scholar 

  • Pérez-Rodríguez L, Blas J, Viñuela J, Marchant TA, Bortolotti GR (2006) Condition and androgen levels: are condition-dependent and testosterone-mediated traits two sides of the same coin? Anim Behav 72:97–103

    Article  Google Scholar 

  • Pham TT, Queller PS, Tarvin KA, Murphy TG (2014) Honesty of a dynamic female aggressive status signal: baseline testosterone relates to bill color in female American goldfi nches. J Avian Biol 45:22–28

    Article  Google Scholar 

  • Piault R, Gasparini J, Bize P, Paulet M, McGraw KJ, Roulin A (2008) Experimental support for the makeup hypothesis in nestling tawny owls (Strix aluco). Behav Ecol 19:703–709

    Article  Google Scholar 

  • Potti J, Merino S (1996) Decreased levels of blood trypanosome infection correlate with female expression of male secondary sexual trait: implications for sexual selection. Proc R Soc Lond B 263:1199–1204

    Article  Google Scholar 

  • Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239

    Article  Google Scholar 

  • Romero-Pujante M, Hoi H, Blomqvist D, Valera F (2002) Tail length and mutual mate choice in Bearded Tits (Panurus biarmicus). Ethology 108:885–895

    Article  Google Scholar 

  • Roulin A (2015) Condition-dependence, pleiotropy and the handicap principle of sexual selection in melanin‐based colouration. Biol Rev 91(2):328–348

    Article  PubMed  Google Scholar 

  • Schroeder J, Lourenç PM, Hooijmeijer JC, Both C, Piersma T (2009) A possible case of contemporary selection leading to a decrease in sexual plumage dimorphism in a grassland-breeding shorebird. Behav Ecol 20:797–807

    Article  Google Scholar 

  • Schulte-Hostedde AI, Zinner B, Millar JS, Graham JH (2005) Restitution of mass–size residuals: validating body condition indices. Ecology 86:155–163

    Article  Google Scholar 

  • Simons MJP, Cohen AA, Verhulst S (2012) What does carotenoid dependent coloration tell? Plasma carotenoid level signals immunocompetence and oxidative stress state in birds—a meta-analysis. PLoS ONE 7:e43088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tobias JA, Gamarra-Toledo V, García-Olaechea D, Pulgarin PC, Seddon N (2011) Year-round resource defence and the evolution of male and female song in suboscine birds: social armaments are mutual ornaments. J Evol Biol 24:2118–2138

    Article  CAS  PubMed  Google Scholar 

  • Tobias JA, Montgomerie R, Lyon BE (2012) The evolution of female ornaments and weaponry: social selection sexual selection and ecological competition. Philos Trans R Soc Lond B 367:2274–2293

    Article  Google Scholar 

  • Torres R, Velando A (2003) A dynamic trait affects continuous pair assessment in the blue-footed booby Sula nebouxii. Behav Ecol Sociobiol 55:65–72

    Article  Google Scholar 

  • Torres R, Velando A (2005) Male preference for female foot color in the socially monogamous blue-footed booby, Sula nebouxii. Anim Behav 69:59–65

    Article  Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179

  • Velando A, Lessells CM, Márquez JC (2001) The function of female and male ornaments in the Inca tern: evidence for links between ornament expression and both adult condition and reproductive performance. J Avian Biol 32:311–318

    Article  Google Scholar 

  • Velando A, Beamonte-Barrientos R, Torres R (2006) Pigment based skin color in the blue-footed booby: an honest signal of current condition used by females to adjust reproductive investment. Oecologia 149:535–542

    Article  PubMed  Google Scholar 

  • Velando A, Beamonte-Barrientos R, Torres R (2014) Enhanced male coloration after immune challenge increases reproductive potential. J Evol Biol 27:1582–1589

    Article  CAS  PubMed  Google Scholar 

  • Vergara P, Fargallo JA (2011) Multiple colored ornaments in male common kestrels: different mechanisms to convey quality. Naturwissenschaften 98:289–298

    Article  CAS  PubMed  Google Scholar 

  • Vergara P, Fargallo JA, Martínez-Padilla J (2015) Genetic basis and fitness correlates of dynamic carotenoid-based ornamental coloration in male and female common kestrels Falco tinnunculus. J Evol Biol 28:146–152

    Article  CAS  PubMed  Google Scholar 

  • Wikelski M, Lynn S, Breuner C, Wingfield JC, Kenagy GJ (1999) Energy metabolism, testosterone and corticosterone in white-crowned sparrows. J Comp Physiol A 185:463–470

    Article  CAS  Google Scholar 

  • Wingfield JC (1987) Changes in reproductive function in free-living birds in response to environmental perturbations. In: Stetson M (ed.) Processing of environmental information in vertebrates. Springer, New York, pp 121–148

  • Wingfield JC, Hegner RE, Dufty AM, Ball GF (1990) The ‘challenge hypothesis’: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846

    Article  Google Scholar 

  • Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 67:205–214

    Article  Google Scholar 

Download references

Acknowledgments

We thank J.A. Fargallo for his valuable comments on the manuscript, L.M. Bautista and O. Gordo for statistical advice and L. García and E. Ávila for their kind help in the laboratory and logistics. Research was founded by Consejo Nacional de Ciencia y Tecnología (CONACYT 129774), Universidad Nacional Autónoma de México (UNAM, PAPIIT-IN206713) and Posgrado en Ciencias Biológicas, Universidad Autónoma de Tlaxcala (UATx). I.L.R was supported by a postdoctoral fellowship from UNAM (DGAPA), and a postdoctoral fellowship from CONACYT at the UATx. Permissions to carry out the research were granted by Secretaría del Medio Ambiente y Recursos Naturales (SEMARNAT). Logistical facilities were provided by the Armada de México and the staff of Parque Nacional Arrecife Alacranes. The work was carried out in accordance with the legal and ethical standards of México.

Author information

Authors and Affiliations

  1. Centro Tlaxcala de Biología de la Conducta, Universidad Autónoma de Tlaxcala, Tlaxcala, Mexico

    Isabel López Rull, Leticia Nicolás & Margarita Martínez

  2. Instituto de Ecología, Departamento de Ecología Evolutiva, Universidad Nacional Autónoma de México, México, DF, 4510, Mexico

    Isabel López Rull, Nadia Neri-Vera, Víctor Argáez & Roxana Torres

  3. Instituto de Investigaciones Biomédicas, Departamento de Biología Celular y Fisiología, Universidad Nacional Autónoma de México, México, DF, 4510, Mexico

    Margarita Martínez

  4. Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, C/José Gutiérrez Abascal, 2, Madrid, 28006, Spain

    Isabel López Rull

Authors
  1. Isabel López Rull
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leticia Nicolás
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nadia Neri-Vera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Víctor Argáez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Margarita Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Roxana Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isabel López Rull.

Additional information

Communicated by C. Barbraud.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rull, I.L., Nicolás, L., Neri-Vera, N. et al. Assortative mating by multiple skin color traits in a seabird with cryptic sexual dichromatism. J Ornithol 157, 1049–1062 (2016). https://doi.org/10.1007/s10336-016-1352-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-016-1352-4

Keywords

Search

Navigation