a continuous, or nearly so, band of distinctively coloured feathers (i.e. not black) .... sociation between adult collar scores of parents and off- spring. DISCUSSION.
I B I S 1 3 7 : 405-409
Some male Pied Flycatchers Ficedula hypoleuca in Iberia become collared with age JAIME POTTI & SANTIAGO MERINO Departamento de Biologia Animal, Universidad de Alcald de Henares, E-28871 Madrid, Spain
The development of a collar in Pied Flycatchers Ficedula hypoleuca in Spain is described and its ontogeneticand genetic variation and phenotypical correlates are analysed. Collared males were older than males having traces of collar or lacking one. Also, males showing a collar or trace of a collar had larger white forehead patches than those lacking a collar. Intrapopulation variation in both collar expression and white patch size, which might be genetically determined but phenotypically decoupled in temporal expression, resembles between-species variation among the black and white European flycatchers. were captured in their nestboxes while they fed nestlings, measured, ringed, aged and released. The age (1year old or older) was determined using criteria given in Karlsson et al. (1986) and Potti and Montalvo (1991a). Male colour variation was assessedby estimatingthe percentageof non-black feathers (“brownness scores” hereafter) on the head and mantle (Alatalo et al. 1984, Potti & Montalvo 1991b). Such feathers may be white, grey or brown in colour. In seven years experience of examining males in the hand, one of us (J.P.)has found three males with nearly complete or complete collars whose collar feathers changed colour with age. In the first case, the collar colour changed from brown to white, in the other two males, from white to grey. In addition, the collar may disappear in some males (see Results). Hence. the term “collar”. as defined in this paper, refers to a continuous, or nearly so, band of distinctively coloured feathers (i.e. not black) on the sides and rear of the neck. This is not. in a strict sense, a collar as shown by the Collared Flycatcher, where all collar feathers are white (31% white in all males with collar or trace of it in our population, n = 225). but it is a convenient way of categorization for our purposes, given the hitherto unexplained change in collar feather colour (and in male colour variation in general; see Lundberg & Alatalo 1992). We defined three categories of collar variation, irrespective of its colour: no collar present (NC). slight collar (SC) and complete collar (CC) (Fig. 1). Males with SC had collars incomplete around the back of the neck or. in a few cases, forming a very narrow continuous line so that, unlike in CC males, it is not distinguishable with binoculars and may be appreciated only when the bird is in the hand. In addition, we measured the length and width (to the nearest 0.05 mm) of the white patch on the male’s forehead, and its size was calculated as described in Potti and Montalvo (1991a).
Among the European small passerines, the black and white flycatchers (Ficedula spp.) offer much promise for the elucidation of patterns of speciation and hybridization and the role of sexual selection in both processes (von Haartman 1949, Alerstam et al. 1978. Rsskaft et al. 1986, Krfd et al. 1988. Gelter 1989, Alatalo et al. 1990. Tegelstrom & Gelter 1990.Lundberg & Alatalo 1992,Rsskaft & J&vi 1992).There seems to be general agreementon the existence of two “good” species which partially replace geographicallythe Collared FlycatcherFicedula albicollis and the Pied FlycatcherFicedula hypoleuca, although hybrids with partial sterility are known in syrnpatry (Alataloet al. 1990,Gelteret al. 1992).However, the taxonomic relationships among the several proposed subspeciesof Pied Flycatchers (nominatehypoleuca in Britain and central-northern Europe, which may include the subspeciesiberiae in Spain and Portugal,tomensis from the Urals eastwards and speculigera in northern Africa: see Howard & Moore 1991, Lundberg & Alatalo 1992)are uncertain. This is also the case for the taxonomic status of Semicollared Flycatchers, which are variously considered as a good species (Ficedula semitorquata) or as a subspecies of Ficedula albicollis (see Cramp & Perrins 1993).The presence of a collar of white feathers on the neck of males (or trace of it) is considered a key character in the evolution of plumage differences among the European flycatchers (Svensson & Mild 1992). Here we report on the frequency and ontogenetic expression of a collar in males of a population of Spanish Pied Flycatchers and point out the implications of our findings for the understanding of their evolutionary relationships. However, we will not address here the controversy about the subspecificstatus of Iberian Pied Flycatchers, which warrants further studies of additional plumage and behavioural features.
METHODS
RESULTS
From 1991 to 1993 we scored male Pied Flycatchers for collar variation in an intensively studied population in central Spain (Potti & Montalvo 1991a,b,c, 1993). The males
We scored males for collar variation 225 times (151different individuals) in the three study years. All CC males were 405
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Table 1. Brownness scores and size of the white patch in relation to variation in collar expression of male Pied Flycatchers
IBIS
Table 3. Within-male variation in collar type in successive years for Pied Flycatcher in Spain. Abbreviations as in Table 1
Size of white patch Brownness score s.e.
n
Mean
s.e.
n
34.7 26.6 21.4
5.16 3.43 1.78
20 36 165
45.96 46.51 41.62
1.84 1.55 0.71
20 36 164
CC. complete collar: SC. slight collar;NC. no collar present.
independently aged as being over 1year old, hence presence of a complete collar adds to previous criteria of age determination as a reliable trait, as least in Pied Flycatchers in Spain. Not unexpectedly, brownness scores decreased through the gradient CC-SC-NC (Kruskal-WallisANOVA. H = 11.6. P < 0.001; Table l),although, among young males, SC and NC males did not differ in brownness (medians 30% [ n = 81 and 20% [ n = 311, respectively; Mann-Whitney test, Z = 0.35, n.s.). To avoid the inclusion of the same male more than once in the estimation of collar type frequencieswhile at the same time taking into account the age effect in collar expression, we proceeded as follows with the restricted sample of 151 different males (Table 2). Except for 13 males that were scored both when they were 1year old and when they were older, when the same male was scored in two or three different years and scores differed (e.g. NC in one year, CC the following year), we selected the least conservative score (CC in the example). About 30% of male Pied Flycatchers had a collar, or traces of it, at any one time, most frequently at an older age (Table 2). Fifty-six males were examined for collar variation in two or three successive years (Table 3). Slight or complete collars developed in 29 males (52%). Within this group, we counted the numbers of males developing, maintaining or losing a collar or trace of collar from one year to the next. Overall,
Table 2. Frequencies of collar types in male Pied Flycatchers in Spain in relation to age. Thirteen males that were scored both as yearlings and at older ages appear in both age groups, hence sample size is 164 scores oj 15 1 different individuals. Abbreviations as in Table 1 Male age Collar type
cc sc NC
First year 0 8 (21%)
30 (79%)
Collar type
( m 2 )
Collar type” Mean CC SC NC
137
Older 18 (14%) 24 (19%) 84 (67%)
First year
Second year
Number of males
NC NC NC
NC
sc sc sc cc cc cc
NC
27 8 7 5 3 3 2 1 0
sc cc
sc cc NC
cc sc
there were 22 increases in collar and seven losses of CC or SC with advancing age. Clearly, the “collared trait” is more characteristic of advancing age than the opposite. However, two CC males scored NC in the following year, and five SC males also lost their trace of collar with advancing age, which suggests that the presence of collar is also related to other factors unrelated to age. We have examined covariation of collar scores with many morphological and reproductivetraits and with some components of the ectoparasite (lice) loads. However, the only significant correlation with the different types of collar variation was the size of the white patch on the forehead of the male: males with SC and CC cores were more likely to have larger white patches than were NC males (one-way ANOVA, F , , , , = 5.60, P < 0.005: Table 1).This relationship holds for the total as well as the sample of older males, although it is not statistically significant in the group of 1-year-old males, where the comparison is reduced in both range and sample size. To examine the possibility of genetic transmission of the collared trait, we constructeda contingencytable comparing presence/absence of collar, i.e. NC v SC/CC scores, between fathers and sons. A constraint of the analysis is that, due to the age variation just described, we had to restrict it to those males examined at least once when aged over 1 year old (Table 4). Nevertheless, the analysis indicates a lack of association between adult collar scores of parents and offspring.
DISCUSSION Some male Pied Flycatchers in Spain developed a collar with advancing age, resemblingthe allopatric F. semitorguata males and male hybrids between Collared and Pied Flycatchers in northern Europe (see Lundberg & Alatalo 1992. Cramp & Perrins 1993). Covariation of collar and brownness scores in our population indicates that a substantial part of the neck plumage becomes lighter in some males with advancing age (Potti & Montalvo 1991b); this may be attributable to
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Figure 1. Male Pied Flycatchers Ficedula hypoleuca (upper) with a complete collar: (lower left) Slight collar; Oower right) No collar.
the concentration of non-black feather tracts to the rear of the neck. An interestingand unexpected correlate of collar variation in Spanish Pied Flycatchers was the size of their white forehead patch, which seems to be a sexually selected trait in our population and is known to be heritable (Potti & Montalvo 1991a, Potti 1993).Males with large forehead patches were more likely to develop a collar than were males with smaller patches, although the collar per se was not related
to higher mating or reproductive success and no evidence was found for genetic transmission of the collar, unlike the case for the white forehead patch size. Our results on fatherson resemblance in collar expression may be considered as highly conservative due to constraints on father-offspring comparisons we were able to make. The white forehead patch size is consistent within males in successive years (Potti 1993, J. Potti & S. Merino, unpubl.) so the variation in both collar expression and white patch size seems to be
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POTTI & S . M E R I N O
Table 4. Frequencies of collar expression in parent and offspring male Pied Flycatchers (xzl = 0.02, Yates’ correction; n.s.)
Fathers Collar expression Sons Present Absent
Present
7 11
Absent
9 13
temporally decoupled across the individual ontogeny. A possible proximate explanation of this fact may be based on the multiple, pleiotropic effects of genes coding for non-black feather tracts and expressing their effects at a different time. Although this explanation will remain speculativeuntil more evidence is gathered, substantial evidence exists for the heritability of plumage sexual traits in this species (see Lundberg & Alatalo 1992, Potti 1993). Our demonstration that a collar may develop with advancing age in Pied Flycatchers in Spain casts doubt on several other observations which are relevant to the confused, controversial taxonomy of the Eurowan Ficedula species (von Haartman 1949. Curio 1960, Vaurie 1965, Howard & Moore 1991, M o d et al. 1991, Svensson & Mild 1992, Cramp 81 Perrins 1993). Collared males reportedly have been identified as F. semitorquatu in an Algerian population of F. hypoleuca speculigera (a subspecies which is believed to be most closely related to the “subspecies” iberiae) on the basis of its large white forehead patch and several other plumage traits (Curio 1960, Lundberg & Alatalo 1992, Svensson 81 Mild 1992. but see Howard & Moore 1991). Judging from the photographspresented in Moali et d,(1991), some of our collared males do not differ from theirs nor from sketches and photographs of hypoleuca x albicollis hybrid males (e.g. Lundberg& Alatalo 1992, E. m k a f t , prs. corn.). although we lack direct field experience with confirmed hybrid males. It is possible that some F. h. speculigera males also develop a collar with age. If this is true, the alleged presence of F. semitorquata males in northern Africa might be based on a confusion between ontogeneticand subspecific variation that deserves further investigation,although other explanationscould be offered (see also Svensson & Mild 1992). The within-population relationship in our study between presence of collar and white patch size is somewhat reminiscent of the between-species variation in both characters in “pure” Collared Flycatchers and nominate Pied Flycatchers. the former having larger patches than the latter (Svensson & Mild 1992).This relationship is interesting because it may shed light on the proposed pattern of speciation within these closely related species, which are known to hybridize in Gotland and other contact areas (Alataloet al. 1990).One possible interpretation is that the expression of collar in old male Pied Flycatchers might be a case of paedogenesis (heterochrony by retardation of somatic features present in the
IBIS
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juvenile stages of the ancestor species [Gould 1977, Ridley 19931). We therefore suggest that the ancestor flycatcher should have shown a collar, which was subsequently lost by northern races (F. h. hypoleuca) or maintained in the southern species and subspecies (F. h. iberiae, F. h. speculi-
gera, F. semitorquatu, F. albicollis). We thank Eivin RBskaft for his key comment on a photograph of a Spanish pied-collared male flycatcher and for valuable comments on a first draft. Our work was funded by the Spanish DGICYT (projects PB86-OOO6-CO2-02 and PB91-0084-CO3-03).
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Zang. H. 1986. Geographic variation in secondary sexual plumage colour characteristics of the male Red Flycatchers. Omis Scand. 17: 293-298. Svensson. L. 81 Mild. K. 1992. A comment to the note about the first possible breeding record of the Semi-collared Flycatcher Ficeduta semitorquota in Algeria. Alauda 60: 117-118. Tegelstrom. H. & Gelter. H.P. 1990. Haldane’s rule and sex biassed gene flow between two hybridizing flycatcher species (Ficedula albicollisand F. hypoleuca,Aves: Muscicapidae).Evolution 44.20122021. Vaurie. C. 1965. The Birds of the Palearctic fauna. Passeriformes. London: Witherby. Submitted 1 January 1994; revision accepted 1 October 1994
