Biological Journal of the Linnean Society, 2004, 82, 237–248. With 1 figure

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Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2004? 2004822237248Original Article

COLOUR POLYMORPHISM AND NICHE WIDTH IN BIRDSP. GALEOTTI and D. RUBOLINI

*Corresponding author. E-mail: galeozot@unipv.it

The niche variation hypothesis and the evolution of colour polymorphism in birds: a comparative study of owls, nightjars and raptors

PAOLO GALEOTTI* and DIEGO RUBOLINI

Laboratorio di Eco-Etologia, Dipartimento di Biologia Animale, Università di Pavia, P.zza Botta 9, 27100 Pavia, Italy

Received 1 September 2003; accepted for publication 22 December 2003

We studied the evolution of colour polymorphism in diurnal raptors, owls and nightjars, the avian taxa in which thistrait is most widespread, in relation to species ecological niche width and diet. Two main mechanisms have been putforward to explain the maintenance of polymorphism, namely apostatic selection and disruptive selection. The nichevariation hypothesis states that species with broader ecological niches should be more variable compared with thosewith narrow niches because of the action of disruptive selection; the apostatic selection hypothesis conversely sug-gests that intraspecific colour variation should be promoted in predators by prey forming an avoidance image for themore common colour morph. Our aim was to determine if colour polymorphism occurrence was associated with broadecological niches as predicted by the niche variation hypothesis, or with predation on intelligent and sharp-sightedprey as predicted by the avoidance image hypothesis. Pairwise comparisons were made between pairs of closelyrelated species differing in variables expected to influence the occurrence of polymorphism. We found that polymor-phic species of all three groups showed wider and more continuous distribution ranges, frequented many differenthabitats, both open and closed, and lived in seasonally alternating dry/wet climates. Polymorphic species were moremigratory compared with monomorphic ones, and they showed an activity pattern covering both day and night. Con-versely, colour polymorphism was not higher in species preying on birds and mammals. All these findings support thehypothesis that colour polymorphism evolved in bird species with wider niche breadth and not in species preying onintelligent prey. Therefore, we propose that disruptive selection may be the main mechanism maintaining colourpolymorphism in these bird groups by favouring different morphs in different environmental conditions. © 2004The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 237–248.

ADDITIONAL KEYWORDS: apostatic selection – comparative method – disruptive selection – morphs – nichewidth – plumage colour – speciation.

INTRODUCTION

Polymorphism in colour is a widespread phenomenonin many animal taxa, and is defined as the coexistenceof two or more distinct and genetically determinedcolour morphs in one interbreeding population (Hux-ley, 1955). Such intraspecific colour variation is inde-pendent of sex, age and season (Butcher & Rohwer,1989), and evidence for birds suggests a strong geneticcontrol of colour morphs (e.g. Van Camp & Henny,1975; Roulin, Richner & Ducrest, 1998; Krüger, Lind-strom & Amos, 2001; Roulin & Dijkstra, 2003). Follow-ing the seminal review by Huxley (1955), a number of

papers have treated this topic in single avian speciesor genera (see Galeotti et al., 2003 and referencestherein). A comprehensive review of this phenomenonin birds as a whole showed that colour polymorphismis relatively rare, involving only 3.5% of species (Gale-otti et al., 2003). However, 61% of the 23 bird ordersand 37% (53) of the 143 families contain polymorphicspecies, and the occurrence of polymorphic species isparticularly high in Strigiformes, i.e. owls and night-jars (33.5%), Cuculiformes (12%), Galliformes (9.5%)and Ciconiiformes (9%), particularly among diurnalraptors. Small families such as Podargidae andAegothelidae include more than 50% of polymorphicspecies, but also two large families, Strigidae andAccipitridae, show a great incidence of colour polymor-

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phism (38.5% and 22.1%, respectively, Galeotti et al.,2003).

Owls and nightjars form closely related orders, buttheir relationship with diurnal raptors is more dis-tant. Similarly, cuckoos and pheasants are not closelyrelated taxa (Sibley, Ahlquist & Monroe, 1988; Sibley& Ahlquist, 1990). Moreover, Galliformes belong to theEoaves, whereas all the others are Neoaves; this sug-gests that the potential to develop colour polymor-phism is common to both ancestral and modern birdtaxa, and it appears to have evolved independentlymany times in birds. Indeed, colour polymorphismmight reflect similar selective pressures under whichavian species are evolving.

Two main hypotheses have been proposed to explainthe maintenance of colour polymorphism: apostaticselection, and disruptive selection (Ford, 1945; Huxley,1955; Butcher & Rohwer, 1989; Lank, 2002). Thesetwo hypotheses have received most attention, while athird mechanism, namely sexual selection (Butcher &Rohwer, 1989) is apparently hardly applicable to poly-morphic species, because individuals of each morphare generally quite uniform and the occurrence of sex-ual dichromatism is not higher in polymorphic species,as could be expected if sexual selection was involved inthe evolution of this trait (Galeotti et al., 2003; but seeFowlie & Krüger, 2003).

Apostatic selection in the form of the avoidanceimage hypothesis has been invoked repeatedly toexplain polymorphism in birds of prey (Paulson, 1973;Rohwer, 1983; Rohwer & Paulson, 1987). The logicbehind this hypothesis is fascinating: it may be advan-tageous for a morph of an avian predator to be differ-ent from other conspecifics in the area as it will be lessfamiliar to potential prey. In short, prey do not form an‘avoidance image’ for the rare morph in the predatorpopulation and therefore do not react quickly to it; theslight advantage in prey capture thus accrued wouldpresumably lead to a balanced polymorphism in pred-ator species. Under this hypothesis, prey are consid-ered the apostatic selective agents.

The avoidance image hypothesis has been pro-posed to explain colour polymorphism in avian pred-ators such as hawks (Accipitridae and Falconidae)and skuas (Laridae) that prey on intelligent andsharp-sighted prey (birds, medium-sized mammalsand some lizards). However, Preston (1980) arguedeffectively against such a selection mechanism, andrecent comparative studies controlling for phylogenyfailed to find support for this hypothesis as a gen-eral rule to explain the maintenance of colour poly-morphism in birds (Galeotti et al., 2003; Fowlie &Krüger, 2003).

Conversely, a balanced colour polymorphism may bedue to disruptive selection that favours extreme indi-viduals but disadvantages intermediate individuals of

a normally distributed population. Clearly, for anequilibrium between the morphs to be established,selective pressures must favour alternately one of thetwo (or more) phenotypes. As Fisher (1930) first sug-gested, heterogeneity in space and time is an evolu-tionary prerequisite, since habitat and climatedifferences in selective pressures may be responsiblefor producing a balanced colour polymorphism in spe-cies with broad ecological niches. Moreover, a largepopulation size and hence a large gene pool mayfavour the evolution of plumage variability (Fowlie &Krüger, 2003). Van Valen & Grant (1970) pointed outthat a species may occupy a wide range of environ-ments either because individuals are generalist intheir habitat use, or because the species is made up ofa number of divergent individuals, each specialized inits habitat use. Van Valen (1965) suggested that if dif-ferent sections of a species are each adapted to theirspecialized habitat then polymorphism would be pro-moted in species with broad habitat use. This idea hasbecome known as the ‘niche variation hypothesis’,which states that species with broader ecologicalniches should be more variable compared with thosewith narrow niches because of the action of disruptiveselection. Following this hypothesis, colour polymor-phism could enhance foraging efficiency or defensivecamouflage of members of a species, depending ontheir habitat use, thus providing additional survivaladvantages to different morphs of a polymorphic spe-cies colonizing environments highly heterogeneous inspace, time and light conditions. Colour polymorphismmay therefore function in helping a bird to avoiddetection by its predators (Baker & Parker, 1979),reducing the chances of it being seen by its prey (Göt-mark, 1987), and limiting inter- and intraspecific com-petition (Spear & Ainley, 1993), allowing differentmorphs to realize different ecological niches. If morphsshow selective habitat preference, polymorphismcould be maintained even in the presence of high geneflow between the different habitats, and might lead tospecies divergence. Some studies support this conten-tion (Rothstein, 1973; Grant et al., 1976; Grant, 1985;Hedrick, 1986) while others apparently do not (Wil-son, 1969; Soulé & Stewart, 1970). According to thedisruptive selection hypothesis, colour polymorphismis greatest in avian species living in both open andclosed habitats and particularly in species which areactive during both day and night (Galeotti et al.,2003). These patterns suggest that varying light con-ditions may be the most important selective mecha-nism maintaining colour polymorphism in birds, andcrypsis, i.e. matching habitat background, may repre-sent the major function.

Here we present a further comparative analysis ofcolour polymorphism, within bird groups showing thehighest occurrence of this phenomenon, namely rap-

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tors, owls and nightjars. Owls and nightjars are genet-ically very close, and raptors share with owls anumber of morphological and ecological traits due totheir predatory habit. In particular, we focused on apo-static selection and disruptive selection as the mainpotential mechanisms of polymorphism maintenancein predatory birds.

The avoidance image hypothesis makes two predic-tions referring mainly to diurnal raptors: first, poly-morphism should be higher in species hunting birds ormammals with good vision and learning/memorycapabilities; second, polymorphism should be higherin migratory species than it is in resident species. Thisfollows from the assumption that resident predatorshave non-overlapping hunting ranges throughout theyear, while migrant predators are likely to have over-lapping hunting ranges in winter. Therefore, duringwinter prey have more chances to meet many differentindividuals of a migrant predator species, so that arare predator morph may invade a monomorphic pop-ulation more easily. This last prediction is, however,weak, since (a) it is based on several untested assump-tions (Rohwer & Paulson, 1987), and (b) the develop-ment of an avoidance image must require, by analogywith search image formation, a certain amount of timeand repeated encounters between the prey and a spe-cific predator, i.e. the formation of a specific prey–predator system. However, it is highly unlikely thatprey faces only one predator species during winterwhen many different predator species share huntingranges, and this may strongly interfere with the for-mation of a specific avoidance image (see Pietrewicz &Kamil, 1979, 1981 for problems related to searchimage formation).

On the other hand, if colour polymorphism is an evo-lutionary adaptation to alternating extremes of condi-tion, or to a wider range of habitats or niches, we maypredict that polymorphic species will share a widerdistribution range, exploit more habitats, live in sea-sonally alternating climates, and frequent both openand closed habitats. Furthermore, we would expectpolymorphism to occur preferentially in species expe-riencing more variable light conditions, i.e. those thatare active during both day and night (Galeotti et al.,2003), and being characterized by larger dispersalmovements, because migrants realize wider nichesthan do residents (Greenberg, 1985; Leisler, 1990).Following this line of reasoning, we might theoreti-cally expect polymorphic species to have wider trophicniches, but in fact we did not have a specific predictionregarding trophic niche width of polymorphic species,since colour morphs of a species do not differ in mor-phological traits related to feeding, such as involvingthe bill or claws, which may influence exploitation offood supplies. Therefore, we did not consider trophicniche width in these analyses.

In this study, we examined the role of the twoproposed selective mechanisms in the evolutionarytransition between monomorphic and polymorphicplumage, by contrasting several ecological features ina dataset including a large number of closely relatedpairs of species differing in plumage colour pattern.Pairwise comparisons provided a control for phylogenyand other confounding factors, since closely relatedspecies usually show similar morphological and eco-logical traits due to their common ancestry (Møller &Birkhead, 1992; Maddison, 2000).

METHODS

DATA COLLECTION

We collected data on plumage coloration pattern andseveral behavioural and ecological traits for all speciesbelonging to the orders Ciconiiformes (diurnal raptors:families Accipitridae and Falconidae), Strigiformes(owls: families Tytonidae, Strigidae; nightjars: fami-lies Nyctibidae, Caprimulgidae, Podargidae, Batra-chostomidae, Aegothelidae) by consulting the existingspecialist literature on these bird groups (King &Dickinson, 1975; Howard & Moore, 1980; Brown,Urban & Newman, 1992; Meyer De Schauensee, 1992;Pizzey & Knight, 1997; Cleere & Nurney, 1998;Cramp, 1998; Grimmet, Inskipp & Inskipp, 1998; Wes-toll, 1998; del Hoyo, Elliott & Sargatal, 1999; König,Weick & Becking, 1999; Scott, 1999; Ferguson-Lees &Christie, 2001). Species were classified as monomor-phic (all individuals of a given sex show the sameplumage colour) or polymorphic (individuals of bothsexes may occur in two or more colour morphs). Weconsidered only species in which colour polymorphismoccurred in adults of both sexes. A degree of colourpolymorphism in a species could be attributed also tosexual dichromatism; to reduce a possible confoundingeffect of sexual dichromatism in our analyses, weselected pairs of species in which the monomorphicmember was also sexually monochromatic or pairsof species in which both members were sexuallydichromatic.

For each species we recorded the following ecologicaland behavioural variables:

distribution range: extent of distribution rangescored as follows: 1, isolated; 2, small (<30% of thebiogeographical region) and fragmented; 3, small andcontinuous; 4, wide (>30% of the biogeographicalregion) and fragmented; 5, wide and continuous;

main food: main food categories indicated with val-ues ranging from 0 for species preying mainly oninvertebrates, fishes, amphibians and reptiles, to 1 forspecies preying mainly on birds and mammals; thisvariable was collected only for raptors and owlsbecause all nightjars are insectivorous;

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number of habitats: number of main habitats usedby the species;

vegetation cover: vegetation cover of frequentedhabitats: 1, species frequenting only a single habitattype in terms of vegetation cover being open (canopycover absent or very scarce) or closed (dense canopycover); 2, species frequenting a mixture of open andclosed habitats; closed habitats included forestedareas, while open habitats included areas mostlydevoid of tree cover, such as savannahs, grasslands,deserts, tundra, lakes or coastal shores;

climate: 1, species living in a single climate type,wet (absence of dry seasons) or dry (absence of rainyseasons throughout the year); 2, species living in dry/wet climates (alternating dry and wet seasons);

activity rhythm: 1, species active only during day-time, only during night time, or only during twilight;2, species active during twilight/day or twilight/night;3, species active throughout the day (daytime, nighttime and twilight);

phenology: 1, resident (species living all year in thesame location); 2, nomadic (species showing dispersiveand erratic movements within and outside breedingareas); 3, partial migrant (species with both migrantand resident populations); 4, migrant (species showingregular migratory movements).

PHYLOGENETIC ANALYSIS AND STATISTICS

Data for different species cannot be considered asindependent points in comparative studies becauseclosely related species are more likely to share similarecological features due to a common ancestor (Felsen-stein, 1985; Harvey & Pagel, 1991). Therefore, we usedthe pairwise comparative method to control for possi-ble similarities among closely related species due tophylogeny (Møller & Birkhead, 1992; Maddison,2000).

We used recent phylogenetic information based onmolecular or morphological traits to form closelyrelated pairs of species with contrasting plumagecolour patterns (Cleere & Nurney, 1998; Griffith, 1999;Wink & Heidrich, 1999; Ferguson-Lees & Christie,2001). A lack of variance in plumage pattern withinclades often limited the number of species pairs thatcould be used for comparisons. Pairs were chosen to bephylogenetically separate, i.e. the path between mem-bers of a pair, along the branch of the tree, did nottouch the path of any other pair (Maddison, 2000).One phylogenetic tree could yield several pairs as longas pairs failed to share common branches. When sev-eral species were available as sister taxa, we selected,if possible, species that occurred in the same geo-graphical area. When phylogenetic information wasnot available, we formed pairs by selecting two speciesfrom the same genera, with a preference for species

occurring in the same geographical area. In the fewcases (10 of 91 pairs) for which a proper congener spe-cies was not available, we chose a species belonging toa sister genera occurring in the same geographicalarea (e.g. Morphnus guaianensis and Harpia harpyja).We selected pairs from as many families as possible toreduce the problem of sampling repeatedly in thesame clades (Beauchamp & Heeb, 2001).

The Wilcoxon signed-rank test was used to test thehypothesis of consistent changes across the set of spe-cies pairs in the states of ecological and behaviouralvariables associated with the two plumage patterns.Tests were performed for all pairs of all bird groupstogether and for each bird group separately. Samplesizes varied slightly among different tests because ofmissing data for some species (see Results). We usedthe sequential Bonferroni test procedure to adjust theobserved significance level to the number of testsmade with the same data set (Rice, 1989). We presentthe P-values of the tests before performing the Bon-ferroni test and describe whether the correction mod-ified their significance. For clarity, means and SEs arepresented for analysed variables instead of mediansand quartiles.

RESULTS

The search in the published literature provided a totalof 91 pairs of species with contrasting plumage colourpattern, of which 41 were raptors, 31 owls, and 19nightjars (see Appendix).

Polymorphic species of owls, nightjars and raptorsshared similar ecological features that differed signif-icantly from those of their monomorphic counterparts(Table 1). Overall, polymorphic species showed widerand more continuous distribution ranges, frequentedmany different habitats, both open and closed, andlived in seasonally alternating dry/wet climates. Poly-morphic species also showed a stronger migratorytendency compared with their monomorphic counter-parts. Finally, they exhibited an extended day/nightactivity pattern. In contrast, polymorphic species ofraptors and owls were not more specialized on intelli-gent prey than were their monomorphic counterparts(Table 1).

Considering bird groups separately (Fig. 1), wefound that polymorphic species of raptors showed awider distribution range compared with their mono-morphic counterparts (Z = -4.2, P < 0.0001, N = 41pairs); they also frequented more habitats (Z = -3.03,P = 0.002, N = 41 pairs), and showed a stronger migra-tory habit (Z = -2.7, P = 0.007, N = 41 pairs). AfterBonferroni correction no other traits were found to beassociated with colour polymorphism in raptor species(climate: Z = -2.1, P = 0.039, N = 41 pairs; activitypattern: Z = -1.6, P = 0.10, N = 41 pairs; main food:

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Z = -1.3, P = 0.18, N = 37; vegetation cover: Z = -1.15,P = 0.25, N = 41).

In owls, the number of habitats frequented was sig-nificantly higher in polymorphic species than it was inmonomorphic ones (Z = -2.95, P = 0.002, N = 31 pairs),and polymorphic species used more varied habitats interms of vegetation cover (Z = -2.7, P = 0.007, N = 31pairs). The distribution range of polymorphic owls waswider than that of monomorphic ones (Z = -2.5,P = 0.01, N = 31 pairs), and polymorphic speciestended to be active during both day and night(Z = -2.1, P = 0.035, N = 28 pairs), but these differ-ences were no longer significant after Bonferroni cor-rection. Other variables did not differ betweenpolymorphic and monomorphic owls (all P > 0.05).

In nightjars only the extent of distribution rangewas significantly associated with colour polymorphism(Z = -2.7, P = 0.008, N = 19 pairs), and no other traitswere found to differ between monomorphic and poly-morphic species after Bonferroni correction (e.g. num-ber of habitats: Z = -2.3, P = 0.019, N = 19 pairs;phenology: Z = -2.3, P = 0.021, N = 19 pairs, climate:Z = -2.0, P = 0.046, N = 19 pairs).

The observed differences between bird groups in theecological and behavioural features associated withcolour polymorphism may be due to different samplesizes or to some differences in the general biology ofgroups, for example, nightjars are mostly crepuscularand most owls show strong residency and nocturnalhabits. However, the trends were remarkably similaramong the three groups for most variables (Fig. 1).

DISCUSSION

The results of this study indicate that, across a widerange of bird species, the evolutionary transitionfrom monomorphic to polymorphic plumage is associ-ated with a broad ecological niche, thus supportingthe niche variation hypothesis (Van Valen, 1965) forthe maintenance of colour polymorphism in predatorybirds. Most polymorphic species of raptors, owls and

nightjars were widely distributed and adapted to abroader range of environmental conditions comparedwith their monomorphic counterparts. This may bethe result of different individuals within a speciesoccupying different parts of a broad niche. The evolu-tion of polymorphism is therefore favoured if individ-uals have a better than random chance of colonizingthe kind of microhabitat to which their genotype bestsuits them, and this occurs if animals can accomplishthe correlation between genotype and environmentby habitat selection. Thus, adaptation to differentaspects of the environment appears to be a majorcause of intraspecific variation in plumage colouramong these bird groups. In this sense morphs mayactually be ecotypes of a species. Indeed, our resultsmet most predictions stemming from the disruptiveselection mechanism of polymorphism maintenance.Conversely, the alternative hypothesis for the main-tenance of colour polymorphism, i.e. apostaticselection in the form of avoidance image develop-ment (Paulson, 1973; Rohwer, 1983; Rohwer & Paul-son, 1987) did not find support in this study. Weshowed that polymorphic raptors did not differ in themain food categories consumed compared with mono-morphic species, i.e. polymorphic raptors were notmore likely to catch birds and mammals (intelligentprey) than were monomorphic ones. The second pre-diction of the avoidance image hypothesis, namelythat migratory species should be more polymorphiccompared with resident species, was met in thisstudy. However, this result is equally compatible withthe niche variation hypothesis, because generallymigratory and/or nomadic species occur in a widerrange of habitats and exploit environments morevariable in terms of climate, type, and vegetationcover than do residents (e.g. Greenberg, 1985; Leisler,1990). In addition, explaining the associationbetween plumage polymorphism and migratory habitunder the niche variation hypothesis is more parsi-monious, because it does not require any underlyingassumption, as conversely required under the apos-

Table 1. Mean (SE) of variables measured for monomorphic and polymorphic pairs of species of raptors, owls and nightjars

Variable Monomorphic species Polymorphic species N pairs Z P

Distribution range 2.59 (0.13) 3.70 (0.14) 91 -5.57 0.000*No. of habitats 1.91 (0.12) 2.79 (0.15) 91 -4.88 0.000*Main fooda 0.58 (0.06) 0.59 (0.06) 66 -0.33 0.74Vegetation cover 0.29 (0.04) 0.54 (0.05) 91 -3.29 0.001*Climate 0.22 (0.04) 0.45 (0.05) 89 -3.33 0.001*Activity 1.36 (0.06) 1.50 (0.07) 88 -2.60 0.011*Phenology 1.37 (0.08) 1.74 (0.11) 91 -3.20 0.001*

Wilcoxon signed-rank test; asterisks indicate significant P-values after sequential Bonferroni correction. arecorded onlyfor raptors and owls.

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Figure 1. Mean (+ SE) of ecological and behavioural traits for monomorphic (open bars) and polymorphic (black bars)species of raptors, owls and nightjars.

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tatic selection hypothesis (see Introduction andRohwer & Paulson, 1987).

In fact, the avoidance image hypothesis has severalweaknesses (see also Preston, 1980): (a) no evidenceexists to show that prey develop an ‘avoidance image’of common avian predator morphs; assuming they doby analogy with search image formation by predatorsmay seem appealing at first glance, but it certainlydoes not represent a solid basis for further specula-tion; (b) it would be maladaptive for prey to focus onplumage pattern while ignoring other cues indicativeof a predator, such as silhouette, vocalizations, noises,movements (e.g. Hendrie, Weiss & Eilam, 1998); (c)intelligent prey must constitute an unknown butclearly substantial fraction of a predator diet to effec-tively exert a selection pressure on the predator itself(see Paulson, 1973); however, to the best of our knowl-edge, very few polymorphic raptor species can be con-sidered to be so specialized on this kind of prey (e.g.some large falcons); (d) prey must repeatedly encoun-ter a single predator morph in order to effectivelydevelop a specific avoidance image (by analogy withsearch image formation, see Pietrewicz & Kamil,1979, 1981); this contrasts with the common notionthat many predator pairs are mixed-coloured, andwith the fact that prey may encounter many predatortypes and should learn to avoid them regardless oftheir plumage pattern (Arnason, 1978).

Moreover, recent comparative studies failed to sup-port the apostatic selection mechanism for colour poly-morphism maintenance in birds: first, among allpolymorphic species, colour polymorphism was notexpressed more in diurnal predator species as postu-lated by the hypothesis, but in fact was more wide-spread in vegetarian taxa and in those active duringboth day and night (Galeotti et al., 2003); second,among raptors and owls, plumage polymorphism wasnot more common in taxa preying on avian or mam-malian prey, but was consistently related to popula-tion and range size of species (Fowlie & Kruger, 2003),which is in accordance with predictions based on theniche variation hypothesis. Although a large popula-tion size may be a precursor to the occurrence of plum-age polymorphism, as advocated by Fowlie & Kruger(2003), it may also be a consequence of intraspecificvariation in niche occupancy, which permits a popula-tion size greater than would otherwise be possible(Van Valen, 1965). Therefore, the present evidencesuggests that apostatic selection is an unlikely mech-anism to explain colour polymorphism maintenance inbirds.

In conclusion, broad-niche species have a higherpotential to develop different colour patterns that maybe adaptive in different environmental conditions byproviding efficient crypsis to bearers. Different mor-phs may vary in success in different habitats or in the

same habitat under different conditions, because ofvariation in foraging efficiency or survival due tohunting or defensive camouflage. If fitness of differentmorphs differs between habitats, then polymorphismcan be established with different equilibrium gene fre-quencies in the different habitats or in the same hab-itat under different conditions. The high frequency ofmorph ratio-clines according to several environmentalfactors further supports this prediction based on dis-ruptive selection (Galeotti et al., 2003). A commonenvironmental feature of these morph ratio-clines isvariation in light conditions (Galeotti et al., 2003). It isnow well documented that the conspicuousness orcrypsis of colour patterns of an animal stronglydepend on the interaction between light levels, spec-tral composition of ambient light and the reflectancespectra of colour pattern elements (Endler, 1978, 1986,1990, 1991; Endler & Théry, 1996). Thus, the balancebetween different plumage coloration in a bird speciesmay be determined by the relative benefits of conspic-uousness or crypsis to predators, prey, conspecifics andguild members, in a variety of different habitats orhabitat conditions, and light levels appear to play amajor role (Galeotti et al., 2003).

Based on our results, we conclude that colour poly-morphism may be maintained by disruptive selectionacting on species with broader ecological niches, andmight be a first step towards species divergence (Mar-chetti, 1993). A further empirical and intraspecific testof the niche variation hypothesis may be provided bycomparison between members of the same populationin order to demonstrate that different morphs differ inhabitat use. Alternatively, one may compare the levelof polymorphism among different populations of thesame species, in order to demonstrate that habitat useis wider in some populations, and then to show thatplumage colour is more variable in populations inwhich the habitat use is broader.

ACKNOWLEDGEMENT

We thank Dr A. Roulin for his useful criticisms andsuggestions on an early draft of the paper.

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APPENDIX

List of closely related pairs of monomorphic and polymorphic species of raptor (families Accipitridae and Falconidae), owlsand nightjars (order Strigiformes) and associated scores for ecological and behavioural traits (see Methods for explanationof scores). The variable ‘Polymorphism’ indicated whether a species was monomorphic (score 0) or polymorphic (score 1).

Species PolymorphismDistributionrange

No. of habitats

Mainfood

Vegetationcover Climate Activity Phenology

Raptors (N = 41 pairs)Rostrhamus sociabilis 0 4 1 0 0 0 1 2Chondrohierax uncinatus 1 5 5 0 1 1 1 1Pernis celebensis 0 2 1 0 0 0 1 1Pernis apivorus 1 5 2 0 1 1 1 4Circaetus fasciolatus 0 3 1 1 0 0 1 2Terathopius ecaudatus 1 5 2 1 1 0 1 2Circus ranivorus 0 2 3 1 0 1 1 2Circus aeruginosus 1 4 3 1 0 1 1 3Circus cinereus 0 5 3 1 0 0 1 3Circus buffoni 1 5 3 1 0 0 1 3Circus macrourus 0 3 3 1 0 0 1 4Circus pygargus 1 4 5 1 0 1 1 4Accipiter castanilius 0 3 1 1 0 0 1 1Micronisus (Melierax) gabar 1 5 3 1 0 0 1 1Accipiter toussenelii 0 3 1 1 0 0 1 1Accipiter tachiro 1 5 2 1 0 1 1 1Accipiter fasciatus 0 4 4 1 1 1 1 1Accipiter novaehollandiae 1 2 2 1 0 0 1 1Accipiter melanochlamys 0 2 2 1 0 0 1 1Accipiter albogularis 1 1 3 1 0 0 1 1Accipiter luteoschistaceus 0 1 2 – 1 0 1 1Accipiter imitator 1 1 1 – 0 0 1 1Accipiter princeps 0 1 1 – 0 0 1 1Accipiter poliocephalus 1 3 2 1 1 0 1 1Accipiter rufiventris 0 2 4 1 1 1 1 1Accipiter ovampensis 1 4 3 1 1 0 1 2Accipiter chionogaster 0 1 1 1 0 0 1 1

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Accipiter ventralis 1 2 1 1 1 1 1 1Accipiter gundlachi 0 1 3 1 1 1 1 1Accipiter bicolor 1 5 3 1 1 1 1 1Accipiter henstii 0 1 1 1 0 1 1 1Accipiter melanoleucos 1 4 2 1 1 1 1 3Erythrotriorchis radiatus 0 5 1 1 1 1 1 1Erythrotriorchis buergensi 1 3 1 1 0 0 1 1Megatriorchis doriae 0 3 1 1 0 0 1 1Urotriorchis macrourus 1 4 1 1 0 0 1 1Buteo magnirostris 0 5 4 0 1 1 1 1Buteo platypterus 1 4 2 1 1 1 1 4Buteo albigula 0 3 1 1 0 0 1 1Buteo brachyurus 1 5 4 1 1 1 1 3Buteo albonotatus 0 4 4 1 1 1 1 3Buteo swainsoni 1 4 3 1 1 0 1 4Buteo galapagoensis 0 1 2 1 1 0 1 1Buteo polyosoma 1 5 4 1 0 0 1 3Buteogallus anthracinus 0 2 3 1 1 1 1 3Buteo jamaicensis 1 5 4 1 1 1 1 3Buteo oreophilus 0 2 2 1 1 0 1 3Buteo buteo 1 5 4 1 1 1 1 3Buteo auguralis 0 2 3 0 1 1 1 3Buteo rufinus 1 4 3 1 0 0 1 3Parabuteo unicinctus 0 4 2 1 0 0 1 1Buteo regalis 1 3 2 1 0 0 1 3Buteo archeri 0 1 1 – 0 0 1 1Buteo augur 1 4 3 1 1 1 1 1Harpia harpyja 0 5 1 1 0 0 1 1Morphnus guaianensis 1 5 1 1 0 0 1 1Aquila nipalensis 0 4 1 1 0 0 1 4Aquila pomarina 1 2 2 1 1 1 1 3Aquila verreauxii 0 2 1 1 0 0 1 1Aquila wahlbergi 1 5 2 1 1 1 1 4Hieraaetus fasciatus 0 2 1 1 0 0 1 1Hieraaetus pennatus 1 4 1 1 1 0 1 3Hieraaetus kienerii 0 2 1 1 0 0 1 1Hieraaetus morphnoides 1 5 3 1 1 1 1 1Spizaetus alboniger 0 2 1 1 1 0 1 1Spizaetus cirrathus 1 4 3 1 1 1 1 1Micrastur gilvicollis 0 3 1 0 0 0 1 1Micrastur ruficollis 1 5 1 1 0 0 1 1Micrastur buckleyi 0 3 1 – 0 0 1 1Micrastur semitorquatus 1 5 2 1 0 0 1 1Falco tinnunculus 0 5 4 0 1 1 1 3Falco sparverius 1 5 4 0 1 1 1 3Falco araea 0 1 2 1 1 0 1 1Falco newtonii 1 3 4 0 0 0 2 1Falco concolor 0 2 3 0 0 1 1 4Falco eleonorae 1 2 3 0 0 1 3 4Falco novaeseelandiae 0 1 2 1 0 0 1 1Falco berigora 1 5 5 1 0 1 1 1Falco mexicanus 0 3 3 1 0 0 1 2Falco rusticolus 1 5 2 1 0 1 2 2

Species PolymorphismDistributionrange

No. of habitats

Mainfood

Vegetationcover Climate Activity Phenology

APPENDIX Continued

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Falco subbuteo 0 3 4 0 1 1 1 4Falco peregrinus 1 4 5 1 0 1 1 3

Owls (N = 31 pairs)Tyto tenebricosa 0 2 1 1 0 0 1 1Tyto novaehollandiae 1 5 3 1 1 0 2 1Otus icterorhynchus 0 2 2 0 0 0 1 1Otus ireneae 1 1 1 0 0 0 1 1Otus angelinae 0 1 1 0 0 0 1 1Otus balli 1 1 2 0 0 0 1 1Otus semitorques 0 3 1 0 0 – 1 3Otus bakkamoena 1 5 3 0 1 0 1 1Otus elegans 0 1 1 0 0 0 1 1Otus sunia 1 5 5 0 1 0 1 3Otus umbra 0 1 1 0 1 0 1 1Otus beccarii 1 1 1 0 1 0 1 1Otus longicornis 0 1 1 0 0 0 1 1Otus rutilus 1 3 4 0 1 1 1 1Otus insularis 0 1 1 0 0 – 1 1Otus pembaensis 1 1 1 0 0 0 1 1Otus cooperi 0 3 5 0 1 0 – 1Otus asio 1 5 5 0 1 1 3 1Otus sagittatus 0 3 1 – 0 0 – 1Otus trichopsis 1 3 1 0 0 0 1 1Otus mindorensis 0 1 1 0 0 0 1 1Otus choliba 1 5 7 0 1 0 1 1Otus koepckeae 0 2 1 0 0 0 1 1Otus roboratus 1 3 2 0 1 0 1 1Otus clarkii 0 3 1 0 0 0 2 1Otus barbarus 1 3 1 0 0 0 1 1Otus petersoni 0 3 1 0 0 0 1 1Otus ingens 1 4 2 0 1 0 2 1Otus albogularis 0 3 3 0 1 0 1 1Otus guatemalae 1 2 3 0 0 1 1 1Bubo magellanicus 0 3 3 1 0 0 2 1Bubo virginianus 1 4 5 1 1 1 3 1Bubo ascalaphus 0 4 2 1 0 0 2 1Bubo bubo 1 5 4 1 1 1 3 1Bubo capensis 0 2 3 1 1 0 2 1Bubo africanus 1 4 3 0 0 0 3 1Strix uralensis 0 4 1 1 0 1 2 1Strix aluco 1 4 4 1 1 1 2 1Strix occidentalis 0 2 1 1 0 1 1 1Strix woodfordii 1 4 2 0 0 1 1 1Strix hylophila 0 3 1 1 0 1 1 1Strix rufipes 1 3 1 1 0 0 2 1Strix albitarsis 0 3 2 – 0 0 1 1Strix virgata 1 5 4 1 1 1 2 1Pulsatrix perspicillata 0 5 4 1 1 1 1 1Lophostrix cristata 1 4 1 0 0 0 1 1Glaucidium passerinum 0 4 1 1 0 1 2 1Glaucidium brodiei 1 4 2 1 1 0 3 1Glaucidium perlatum 0 4 3 0 1 0 3 1Glaucidium gnoma 1 3 1 0 0 0 2 1

Species PolymorphismDistributionrange

No. of habitats

Mainfood

Vegetationcover Climate Activity Phenology

APPENDIX Continued

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Glaucidium nubicola 0 3 1 0 0 0 – 1Glaucidium costaricanum 1 3 2 0 1 0 3 1Glaucidium minutissimum 0 3 1 0 0 0 3 1Glaucidium jardinii 1 3 3 1 1 1 3 1Glaucidium peruanum 0 3 3 0 1 0 3 1Glaucidium brasilianum 1 5 6 0 1 1 3 1Glaucidium tephronotum 0 2 2 0 0 0 3 1Glaucidium siju 1 1 3 0 1 1 3 1Athene brama 0 5 5 0 0 0 2 1Athene noctua 1 5 5 0 0 0 3 1Ninox scutulata 0 4 4 0 0 0 2 3Ninox superciliaris 1 2 5 0 1 1 2 1

Nightjars (N = 19 pairs)Aegotheles tatei 0 1 1 – 0 0 2 1Aegotheles crinifrons 1 1 2 – 0 0 1 1Aegotheles wallacii 0 1 1 – 0 0 2 1Aegotheles albertisi 1 2 3 – 1 0 2 1Aegotheles bennettii 0 2 1 – 0 0 2 1Aegotheles cristatus 1 5 4 – 1 1 2 1Batrachostomus auritus 0 2 1 – 0 0 1 1Podargus ocellatus 1 2 1 – 0 0 2 1Batrachostomus moniliger 0 2 1 – 0 0 2 1Batrachostomus septimus 1 2 1 – 0 0 2 1Batrachostomus poliolophus 0 1 1 – 0 0 1 1Batrachostomus stellatus 1 2 1 – 0 0 1 1Nyctibius maculosus 0 3 1 – 0 0 1 1Nyctibius griseus 1 5 4 – 1 0 2 1Chordeiles pusillus 0 4 3 – 0 0 1 1Chordeiles gundlachii 1 2 2 – 1 0 2 4Podager nacunda 0 4 4 – 0 1 3 3Nyctidromus albicollis 1 5 4 – 1 1 2 1Nyctiphrynus rosenbergi 0 3 1 – 0 0 2 1Nyctiphrynus yucatanicus 1 3 4 – 1 0 2 1Siphonorhis brewsteri 0 1 2 – 1 0 2 1Nyctiphrynus ocellatus 1 4 1 – 0 0 2 1Caprimulgus rufus 0 4 4 – 1 1 2 1Caprimulgus carolinensis 1 3 3 – 1 1 2 4Caprimulgus cayennensis 0 3 2 – 0 0 2 1Caprimulgus longirostris 1 4 4 – 0 0 2 3Caprimulgus poliocephalus 0 2 2 – 1 0 2 1Caprimulgus pectoralis 1 5 3 – 1 1 2 3Caprimulgus

madagascariensis 0 3 3 – 0 0 2 1Caprimulgus asiaticus 1 5 2 – 1 1 2 3Caprimulgus tristigma 0 3 1 – 0 0 2 1Caprimulgus natalensis 1 3 2 – 0 0 2 1Caprimulgus batesi 0 2 2 – 1 0 2 1Caprimulgus inornatus 1 5 2 – 0 0 2 3Caprimulgus pulchellus 0 1 1 – 0 0 2 1Caprimulgus affinis 1 4 4 – 0 1 2 3Caprimulgus enarratus 0 2 1 – 0 0 2 1Caprimulgus climacurus 1 4 4 – 1 0 2 3

Species PolymorphismDistributionrange

No. of habitats

Mainfood

Vegetationcover Climate Activity Phenology

APPENDIX Continued