Absolute and relative signals: a comparison between melanin- and carotenoid-based patches
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1 Absolute and relative signals: a comparison between melanin- and carotenoid-based patches J.C. Senar 1) & J. Quesada (Behavioural and Evolutionary Ecology Associate Research Unit (CSIC), Museu de Ciències Naturals, Barcelona, Spain) (Accepted: 6 February 2006) Summary Some signalling traits may be highly influenced by environmental factors, thereby decreasing between-year trait repeatability what could compromise the honesty of signal. However, although the repeatability of environmentally-influenced traits of individuals between years may be low, their relative position within the population can be maintained (i.e. significant correlation between years). In the great tit Parus major, individual hue of the yellow breast coloration, an environmentally influenced trait, showed a significant correlation between years in spite of repeatability between years being very low. However, the size of the black breast band, a heritable trait, showed both a high correlation and inter-year repeatability. Results emphasise the distinction between absolute and relative signals and also suggest that for environmentally-influenced ornaments, individuals maintain their relative position on a continuum. Keywords: signalling, plumage colour, sexual selection, melanin, carotenes, Parus major. Introduction Models of sexual selection have traditionally considered that the expression of signals should be constant over time as a consequence of gene expression (Andersson, 1994; Jennions et al., 1995). However, it has recently been 1) Corresponding author s address: Unidad Asociada de Ecología Evolutiva y de la Conducta, CSIC, Museu de Ciències Naturals, Passeig Picasso s/n, Barcelona, Spain; address: jcsenar@mail.bcn.es Koninklijke Brill NV, Leiden, 2006 Behaviour 143, Also available online -
2 590 Senar & Quesada shown that environmental conditions influence the expression of sexual selected traits (Jia et al., 2000; Greenfield & Rodriguez, 2004). In birds, for instance, the absolute value of some sexual traits may change from one year to the next (Pärt & Qvarnström, 1997; Hill, 2002). This should potentially confound the receiver about the honesty of the emitter s advertisement. Nevertheless, traits may still be reliable in such circumstances provided they either reflect the current status or changes in status over time (e.g., parasite load, physical condition: Qvarnström, 2001; Greenfield & Rodriguez, 2004), or maintain the relative value among the different individuals over time. Thus, the most ornamented individuals in the population in one year would continue to be the most ornamented over the following years, even though environmental conditions may change the medium value of the population trait (Senar et al., 2002). Such data are scarce for birds. In this paper we use the great tit Parus major to test whether environmentally-influenced ornaments in birds (e.g., carotenoid-based hue of the yellow on the breast: Slagsvold & Lifjeld, 1985) can maintain their relative value over time, thereby sustaining the honesty of the signal in spite of the changes in their absolute values. We compare this kind of ornament with that of a highly genetically-influenced trait (the melanin-based black breast stripe: Norris, 1993). We hypothesize that the black stripe operates as an absolute signal, and predict a high repeatability and correlation between consecutive years in its size, meanwhile the hue of the yellow on the breast functions as a relative signal, and predict a low inter-year repeatability but a significant correlation in the value of this trait between subsequent years. Material and methods The study was carried out from 1998 to 2001 in a population of great tits in Northeast Spain. Birds were captured in special funnel traps. Two measures of each trait were taken from the same individual in consecutive years (1 year ± 4 months). We used only adult male birds in the analyses (Euring ages 7 and 9) because: (1) sexual traits and sexual selection are stronger in males than in females (Andersson, 1994), (2) moult is complete in adult birds but only partial in juveniles, (3) both the size of the black breast stripe and the hue of the yellow breast differ between yearling and adult birds (Senar et al., 2003), and (4) senescence could affect plumage coloration of older individuals (Potti & Montalvo, 1991; Møller & De Lope, 1999),
3 Plumage colour as absolute and relative signals 591 The area of the black breast stripe (N = 14) was measured from digital pictures using ImageTool 1.28 (Texas, USA) (Figuerola & Senar, 2000). Mean of the yellow hue coloration of the breast and abdomen was assessed by a portable colorimeter Minolta CR200 (Minolta Corporation 1994 ) (Figuerola et al., 1999) (N = 35). The great tit presents a peak of UV in the yellow breast plumage but a high correlation between the reflectance of the peak of UV ( nm) and the peak of the yellow-red spectrum ( nm) is present (Spearman rank order correlation, r s = 0.83, p<0.001; N = 29, birds measured with Ocean Optics spectrophotometer). Inter-year repeatability in character expression was measured with oneway ANOVA, according to Lessells & Boag (1987). Inter-year correlation in the expression of the different colour traits was computed with an independent one way-ancova for each trait (melanin and carotenoid hue). 1 st year ( ) was the independent factor which allowed to standardise for yearly variations in ornament expression, ornament value 1 st year was the dependent variable and ornament value 2 nd year was the covariant. Results The hue of the yellow breast colour showed very low inter-year repeatability (r i = 0.01, p = 0.52, N = 35), but the values of an individual in the population from one year to the next were significantly correlated (ANCOVA, F (1,34) = 30.77; p<0.001; covariant interaction: r = 0.58, p<0.001, N = 35). The greenest male one year thus tended to be the greenest male the following year, thereby maintaining the relative value of each individual in relation to the others in the population (Figure 1). The size of the great tit black breast stripe showed both a high repeatability in consecutive years (r i = 0.76, p<0.001, N = 14), and a high correlation from one year to the next (ANCOVA, F (1,10) = 2.6; p = 0.12; covariant interaction: r = 0.91, p < 0.001, N = 14). Discussion Phenotypic plasticity is increasingly recognised to shape character evolution (DeWitt et al., 1998; Payne & Krakauer, 2000; Agrawal, 2001; Price et al.,
4 592 Senar & Quesada Figure 1. Correlation in the great tit, between subsequent years, in the values of (a) hue of the carotenoid-based breast patch (in ) and, (b) the size of the melanin based breast patch, (in mm 2 ). Data were standardised by year as we used data from 1998 to 2001 (both included). 2003). For instance, both context-dependent sexual advertisement (Qvarnström, 2001; Badyaev & Qvarnström, 2002; Badyaev & Duckworth, 2003; Badyaev & Young, 2004) and life-history (Griffith, 2000; Qvarnström, 2001) affect ornament expression in birds. However, not all plasticity is adaptive. Passive plasticity, in which variation in character expression is just the result of a response to environmental variation (Scheiner, 1999), may also modulate ornaments. This random variation in character expression could evidently compromise the use of these characters in inter-sexual signalling. Nevertheless, these highly environmental-influenced ornaments may still transmit important information on the qualities of the bearer as long as the relative value of the character of each individual within the population is maintained (Senar et al., 2002). Here we suggest that this is the case for the hue of carotenoidpigmented great tit plumage coloration. Repeatability of this character from year to year was very low, but the most ornamented individuals one year continued to be the most ornamented in the following years (Senar et al., 2002). This is why we propose calling such characters relative signals. This would counterpoise to absolute signals which to a larger extent would be genet-
5 Plumage colour as absolute and relative signals 593 ically determined and show a high repeatability in the expression of their absolute values from year to year (e.g., the black breast stripe). The relative nature of carotenoid-based ornaments could explain why females from populations with a depressed expression of this character continue to choose very highly ornamented males (Hill, 1994, 2002). Since the expression of carotenoid-based colours can vary both temporally and geographically, the best evolutionary response for females is to be constantly sensitive to the most ornamented males. What we present as relative and absolute signals are the extremes of a continuum as a very heritable signal may show fluctuations in its absolute value from year to year (Potti, 1993; Griffith & Sheldon, 2001; Qvarnström, 2001; Fitze & Richner, 2002) and a genetic predisposition could also determine a limitation of carotenoid based-colour expression (Tschirren et al., 2003). However, we would like to stress that the concept of the relative value of signals may provide an alternative view to interpret evolutionary processes related to signalling. Acknowledgements We are most grateful to Alex Badyaev for comments on the paper and L. Arroyo, D. Boné, J. Broggi, J. Domènech, J. Figuerola and I. Ruiz for their help in fieldwork. Carolyn Newey improved the English. BOS project to JCS and FPI grant FP to JQ, both from Ministerio de Ciencia y Tecnología, funded this work. References Agrawal, A.A. (2001). Phenotypic plasticity in the interactions and evolution of species. Science 294: Andersson, M. (1994). Sexual selection. Princeton University Press, Princeton, NJ. Badyaev, A.V. & Duckworth, R.A. (2003). Context-dependent sexual advertisement: plasticity in development of sexual ornamentation throughout the lifetime of a passerine bird. J. Evol. Biol. 16: Badyaev, A.V. & Qvarnström, A. (2002). Putting sexual traits into the context of an organism: a life-history perspective in studies of sexual selection. Auk 119: Badyaev, A.V. & Young, R.L. (2004). Complexity and integration in sexual ornamentation: an example with carotenoid and melanin plumage pigmentation. J. Evol. Biol. 17:
6 594 Senar & Quesada DeWitt, T.J., Sih, A. & Wilson, D.S. (1998). Costs and limits of phenotypic plasticity. Trends Ecol. Evol. 13: Figuerola, J., Pascual, J. & Senar, J.C. (1999). The use of a colorimeter in field studies of blue tit Parus caeruleus coloration. Ardea 87: Figuerola, J. & Senar, J.C. (2000). Measurement of plumage badges: an evaluation of methods used in the great tit Parus major. Ibis 142: Fitze, P.S. & Richner, H. (2002). Differential effects of a parasite on ornamental structures based on melanins and carotenoids. Behav. Ecol. 13: Greenfield, M.D. & Rodriguez, R.L. (2004). Genotype-environment interaction and the reliability of mating signal. Anim. Behav. 68: Griffith, S.C. (2000). A trade-off between reproduction and a condition-dependent sexually selected ornament in the house sparrow Passer domesticus. Proc. R. Soc. Lond. B 267: Griffith, S.C. & Sheldon, B.C. (2001). Phenotypic plasticity in the expression of sexually selected traits: neglected components of variation. Anim. Behav. 61: Hill, G.E. (1994). Geographic variation in male ornamentation and female mate preference in the house finch: a comparative test of models of sexual selection. Behav. Ecol. 5: Hill, G.E. (2002). A red bird in a brown bag. Oxford University Press, Oxford. Jennions, M.D., Backwell, P.R.Y. & Passmore, N.I. (1995). Repeatability of mate choice: the effect of size in the African painted reed frog, Hyperolius marmoratus. Anim. Behav. 49: Jia, F.Y., Greenfield, M.D. & Collins, R.D. (2000). Genetic variance of sexually selected traids in waxmoths: maintenance by genotype environment interaction. Evolution 54: Lessells, C.M. & Boag, P.T. (1987). Unrepeatable repeatabilities: a common mistake. Auk 104: Møller, A.P. & De Lope, F. (1999). Senescence in a short-lived migratory bird: age-dependent morphology, migration, reproduction and parasitism. J. Anim. Ecol. 68: Norris, K.J. (1993). Heritable variation in a plumage indicator of viability in male great tits Parus major. Nature 362: Payne, R.J.H. & Krakauer, D.C. (2000). Disruptive sexual selection. Trends Ecol. Evol. 15: Pärt, T. & Qvarnström, A. (1997). Badge size in collared flycatchers predicts outcome of male competition over territories. Anim. Behav. 54: Potti, J. (1993). A male trait expressed in female pied flycatchers, Ficedula hypoleuca: the white forehead patch. Anim. Behav. 45: Potti, J. & Montalvo, S. (1991). Male colour variation in Spanish pied flycatchers Ficedula hypoleuca. Ibis 133: Price, T.P., Qvarnström, A. & Irwin, D.E. (2003). The role of phenotypic plasticity in driving genetic evolution. Proc. R. Soc. Lond. B 270: Qvarnström, A. (2001). Context-dependent genetic benefits from mate choice. Trends Ecol. Evol. 16: 5-7. Scheiner, S.M. (1999). Towards a more synthetic view of evolution (book review). Am. J. Botany 86: Senar, J.C., Figuerola, J. & Domènech, J. (2003). Plumage coloration and nutritional condition in the great tit Parus major: the roles of carotenoids and melanins differ. Naturwissenschaften 90:
7 Plumage colour as absolute and relative signals 595 Senar, J.C., Figuerola, J. & Pascual, J. (2002). Brighter yellow blue tits make better parents. Proc. R. Soc. Lond. B 269: Slagsvold, T. & Lifjeld, J.T. (1985). Variation in plumage colour of the great tit Parus major in relation to habitat, season and food. J. Zool., Lond. 206: Tschirren, B., Fitze, P.S. & Richner, H. (2003). Proximate mechanisms of variation in the carotenoid-based plumage coloration of nesting great tits (Parus major L.). J. Evol. Biol. 16:
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