Plumage Polymorphism in a Newly Colonized Black Sparrowhawk Population: Classiﬁcation, Temporal Stability and Inheritance Patterns A

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Journal of Zoology. Print ISSN 0952-8369 Plumage polymorphism in a newly colonized black sparrowhawk population: classiﬁcation, temporal stability and inheritance patterns A. Amar, A. Koeslag & O. Curtis*

Percy FitzPatrick Institute of African Ornithology, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch, South Africa

Keywords Abstract polymorphism; raptors; inheritance; Mendelian; morphs; pedigree data. Persistent plumage polymorphism occurs in around 3.5% of bird species, although its occurrence is not distributed equally across bird families or genera. Correspondence Raptors show a disproportionately high frequency of polymorphism, and among Arjun Amar, Zoology, Percy FitzPatrick raptors it is particularly frequent among the Accipiter hawks. However, no sys- Institute for African Ornithology, University tematic study of polymorphism in this genus exists. Using a long-term study of of Cape Town, Private Bag X3, Rondebosch, the black sparrowhawk (Accipiter melanoleucus), a widespread polymorphic Cape Town 7701, South Africa. Tel: +021 African Accipiter, we ﬁrst demonstrate that the species shows discrete polymor- 650 3304 phism (cf. continuous polymorphism), occurring as either dark or light morph Email: [email protected] adults, and that morph type and plumage pattern are invariant with age. We then demonstrate that adult morph type follows a typical Mendelian inheritance *Current address: Overberg Lowlands pattern, suggesting a one-locus, two-allele system within which the allele coding Conservation Trust, 3 de Kock St., Napier for the light morph is dominant. This inheritance pattern provides further 7270. support for classifying polymorphism in this species as discrete. In most of the species’ range the dark morph is the rarer morph; however, in our study popu- Editor: Andrew Kitchener lation where the species is a recent colonist, over 75% of birds were dark and this remained fairly constant over the 10 years of our study. This reversal in morph Received 7 June 2012; revised 9 August ratio may represent an adaptive response to different environmental conditions 2012; accepted 14 August 2012 or could be a founder effect with colonizing individuals having been mostly dark morph birds simply by chance. The extreme differences in environment condi- doi:10.1111/j.1469-7998.2012.00963.x tions (seasonality of rainfall) that occur across the species’ range in South Africa provide support for an adaptive explanation, but further work is needed to test this hypothesis.

Introduction colour variant is under selective pressure. However, in many studies these factors often remain untested. Plumage polymorphism, in which different plumage morphs Polymorphism is particularly common in raptorial species occur within the same age and sex of a breeding population, (Fowlie & Krüger, 2003; Galeotti et al., 2003). Plumage occurs in around 3.5% of bird species (Roulin, 2004). Evolu- colour in polymorphic raptors can vary continuously or may tionary ecologists have long been fascinated by this phenom- show two or more discrete morphs, for example, the polymor- enon because the occurrence of two morphs in the same phic Swainson’s hawk (Buteo swainsoni) and common buzzard population runs counter to the notion that selective pressure (Buteo buteo) show continuous polymorphism, although they should favour the optimal form for an environment, and any are often classified as dark, light or intermediate for analyses lesser quality individuals should be quickly eliminated (Krüger & Lindström, 2001; Briggs, Collopy & Woodbridge, (Huxley, 1955). 2011). By contrast, discrete polymorphism exists in ferrugi- Various explanations have been postulated for the occur- nous hawk (Buteo regalis – Schmutz & Schmutz, 1981) and rence and maintenance of polymorphism in birds (Galeotti Eleonora’s falcon (Falco eleonorae – Gangoso et al., 2011) et al., 2003; Roulin, 2004), and some of the most established with either dark or light morph birds. hypotheses include: (1) apostatic selection (Fowlie & Krüger, The type of phenotypic plumage polymorphism is likely to 2003); (2) disruptive selection (Mather, 1955); (3) allopatric be influenced by the mode of genetic inheritance. Many evolution (Cooke, Rockwell & Lank, 1995); (4) sexual selec- studies have shown that polymorphic phenotypes are geneti- tion (O’Donald, 1983). Underpinning all these theories is the cally determined in birds and follow a Mendelian mode of notion that an individual’s phenotype is heritable, intransient, segregation (Roulin, 2004). To date, the use of pedigree data and not influenced by environmental variation, and that the to study the genetic pattern of inheritance of plumage morphs

Journal of Zoology •• (2012) ••–•• © 2012 The Authors. Journal of Zoology © 2012 The Zoological Society of London 1 Polymorphism in black sparrowhawks A. Amar, A. Koeslag and O. Curtis in raptors has been reported in the common buzzard (Krüger Cape Peninsula. The first breeding attempt on the Peninsula & Lindström, 2001), ferruginous hawk (Schmutz & Schmutz, was recorded in 1993 (Oettlé, 1994; Curtis, Hockey & 1981), Swainson’s hawk (Briggs, Woodbridge & Collopy, Koeslag, 2007) and the current population is estimated to be 2010a), Eleonora’s falcon (Gangoso et al., 2011) and gyrfal- at least 40 breeding pairs. con (Falco rusticolus – Chang, Lejeune & Cheng, 2010). In this paper, using a long-term study of the black sparrow- The first four studies suggest a simple one-locus, two-allele hawk on the Cape Peninsula, we undertake the first detailed autosomal inheritance pattern. For the ferruginous hawk and study of polymorphism in an Accipiter species. Using photo- Eleonora’s falcon that show discrete polymorphism, dark graphs to score plumage characteristics we: (1) describe the alleles are dominant and dark morph birds are thus either type of polymorphism present and establish whether polymor- homozygous (with the alleles designated DD, capital letters phism in this species is best quantified as discrete or continu- for dominant alleles) or heterozygous (Dl), and light birds are ous, and (2) determine whether an individual’s plumage homozygous for the recessive light allele (ll). For common pattern is invariant over time. Then, using pedigree data from buzzard and Swainson’s hawk, dark (d) and light (l) alleles wild, colour-ringed birds with known parental morphs, we show incomplete dominance and heterozygous (dl) individuals explore plumage inheritance patterns to test for a genetic basis therefore display intermediate plumage between the two to the trait, and whether this follows conventional Mendelian homozygous morphs [dark (dd) or light (ll)], and hence give inheritance patterns. Lastly, we examine the morph ratio of rise to continuous polymorphism along the plumage spec- this newly colonized population and explore whether (1) it trum. For gyrfalcons, which show a full spectrum from pure differs between the sexes of breeding adults, and (2) it has white to pure black and many variants in-between, a more changed over time. complex inheritance pattern is suggested, with colour being controlled by two genes, one controlling pigment production Methods and the other restricting pigment distribution in feathers, with alleles in one gene having dominance and alleles in the other We monitored the black sparrowhawk population on the gene being co-dominant (Chang et al., 2010). Cape Peninsula between 2001 and 2010. The study area fea- Although several studies support a genetic basis to plumage tures a matrix of habitats including urban gardens, alien pine variation, relatively few have demonstrated the stability of an (Pinus spp.) and Eucalyptus (Eucalyptus spp.) plantations, and individual’s morph as it ages (Lowther, 1961; Lank et al., small pockets of indigenous Afromontane forest and Fynbos. 1995; Brommer, Ahola & Karstinen, 2005). Criticism has been Altitudes where the birds breed range from sea level to about made of some studies which assume that plumage morph pat- 300 m, and the climate is temperate, with locally variable terns remain constant over the course of an individual’s life winter rainfall (Cowling, MacDonald & Simmons, 1996). (Roulin, 2004). However, in the only study to examine this Mean annual rainfall is c.1250 mm, with average minimum question in raptors, Briggs, Woodbridge & Collopy (2010b) and maximum monthly temperatures of 12 and 21°C, respec- found that plumage morph and patterning was invariant over tively (South African Weather Service). time in 18 Swainson’s hawks that were photographed at least Monitoring was conducted during the breeding season 2 years apart. (March–November; Sebele, 2012) each year. Nests were Among raptors, polymorphism occurs frequently in the located by surveying suitable stands of trees during the breed- genus Accipiter, with 11 of the 46 species displaying different ing season, searching for calling sparrowhawks, prey remains, colour morphs (Ferguson-Lees & Christie, 2001). However, whitewash and nest structures. Territories were visited regu- no empirical research into polymorphism has focused on any larly (approximately monthly) throughout the season until species from this genus. Polymorphic species in this genus breeding was detected and then breeding attempts were moni- often show a similar polymorphic adult plumage, with a tored until conclusion. Where possible, we identified the standard type, for example, common morph (light breast and morphs (dark or light) and sex of both parents attending a underwing coverts) and a rarer dark adult morph, which tends nest, which was possible in around 90% of breeding attempts. to be black on the breast and underwing coverts (Ferguson- The species is easy to sex, with males weighing around 40% Lees & Christie, 2001). The black sparrowhawk (Accipiter less than the females (unpublished data, see also Ferguson- melanoleucus) is a widely distributed Accipiter species occur- Lees & Christie, 2001). In this study, data were only used for ring throughout much of sub-Saharan Africa (Ferguson-Lees pairs where we knew the morph of each pair member. & Christie, 2001) and is usually described as showing these We fitted unique colour-ring combinations to as many two morphs, although with varying degrees of white under the breeding adult birds and 2–3-week-old nestlings as possible. chin. The adult dark morph of this species is usually classed as Adults were trapped on territories using a bal-chatri baited rare (Steyn, 1982; Kemp & Kemp, 1998; Ferguson-Lees & with live white pigeons (Columba livia – Berger & Mueller, Christie, 2001; Hockey, Dean & Ryan, 2005), although there 1959). Some of the birds ringed as chicks entered the breeding are no published details on morph frequencies across the population during the course of the study, and enabled us to species’ range. The juveniles also occur as two morphs (pale or determine their adult morphs, which they began to acquire rufous) although these do not apparently reflect their subse- after their first year. In total, 102 adults (50 males, 52 females) quent adult morphs (Ferguson-Lees & Christie, 2001). The and 131 chicks (76 males, 55 females – of which 33 were later species has recently expanded into South Africa’s Western resighted in adult plumage) were fitted with colour rings Cape (Sebele, 2012) where it has successfully colonized the during the course of the study.

Resightings of individual birds occurred mainly at breeding 40 territories, but also through occasional observation away 35 from breeding territories, via reporting and photographs 30 taken by the authors and by members of the public. Photographs were taken of birds in adult plumage after 25 being caught for ringing, or by using a 300-mm telephoto lens 20 when birds were perched near the nest. Only photographs that

Frequency 15 showed the chin, throat, breast and flanks (hereafter front) 10 were used for scoring coloration. Two observers (A. A.’s data were used in the final analysis for ease of analysis) scored 5 the percentage of white plumage on the front of birds in 0 0 5 10 15 20 25 30 40 45 55 60 65 75 85 95 35 50 70 80 90 each photo. This approach to scoring plumage visually has 100 been used in other studies, both with the birds in the hand % white plumage on front (Brommer et al., 2005) and using photographs (Briggs et al., Figure 1 The frequency distribution of birds displaying different 2010b). Neither observer had knowledge of the other’s scores, amounts of white plumage on their throat, chin, breast, and flanks, and nor of the identity of the photographed bird. whether they were classified as either dark (solid bars) or light (open To explore morph frequencies between sexes and years, we bars) in the field. White plumage percentages were visually estimated used the data from all breeding pairs whose morphs were from 135 photos. The data show there is a clear bimodal pattern and identified in each year (n = 245 pair years, between 2001 and justify the division of birds into either dark or light morphs. 2010). However, this led to some level of pseudo-replication, since some birds featured in multiple years. For this reason, we ran a separate analysis, analysing the morph ratio of all pairs in the first year of breeding only (i.e. excluding known or there was close agreement between different observers in the suspected pairs from subsequent years; n = 130 pairs). Pairs scores allocated to individual birds (R2 = 0.96, P < 0.0001). A and individuals were relatively faithful to nesting territories histogram of the scores clearly showed a discrete bimodal (unpublished data), and previously established or new pairs distribution in plumage coloration (Fig. 1). Birds described were classified based either on the pair’s colour rings (n = 43), as dark morphs or light morphs had on average 8% (range or in situations where only one bird was colour ringed, the 0–33%) and 84% (68–92%) white plumage on their front, combination of its colour rings and its partner’s morph and respectively. lack of colour rings (n = 48), or in cases where neither bird was For a subset of these data, where the sex was known (n = colour ringed (n = 39) we used only morph and sex combina- 125), we explored, for each morph type, whether the percent- tions that were previously present on that territory to deter- age of white plumage on the front differed between the sexes. mine whether they were new or previously established pairs. For light morphs, although sample size was small (n = 28), We tested whether there were any differences between the there appeared to be no difference in the percentage of white sexes in the percentage of white on the front using a general plumage between the sexes (males: 85.5 Ϯ 1.7%, females: 84.3 Ϯ 2 linear model, with arcsine square root transformed percentage 1.1%; c 1 = 0.54; P = 0.46). For dark morphs (n = 97), data as the response variable and the sex (M or F) as the although not quite statistically significant, there was a ten- explanatory variable. Analyses of the two morph types were dency for males to have less white than females (males: 7.4 Ϯ Ϯ 2 conducted separately. Changes in frequency of morphs over 0.8%, females: 10.4 1.1%; c 1 = 2.90; P = 0.08). time were analysed using a generalized linear model, with a For six colour-ringed individuals (three males and three binomial distribution and a logit link function. Whether a bird females; three dark morphs and three light morphs), we had was a dark morph or a white morph (1/0) was specified as the photos taken at least 4 years apart (range 4–11 years). From response variable and year (as a continuous variable) was then the scores given to these birds, it was apparent that the specified as the explanatory variable. These analyses were morphs did not change over the years, with the small differ- carried out for males and females separately. All analyses were ence between years not showing any directional change carried out in SAS version 9.1 (SAS Inc., 2004). Means are over time and was most likely attributable to observer error presented Ϯ 1 standard error. (Table 1).

Results Inheritance patterns of morphs

Polymorphism classiﬁcation and individual We observed 33 birds (17 males, 16 females) in adult plumage that were colour ringed as chicks at nests where we also knew variance over time the morphs of both attending parents. These birds were pro- We had 135 photographs of individual adult birds which duced in 18 different territories and from the parental colour- showed their front adequately to score the percentage of ing combinations they came from 18 different pairings. white plumage. These photos came from 42 different territo- Thirteen dark x dark pairings produced 13 dark morph ries in the study area. Scores from the two observers did not offspring (8 males, 5 females) and no light morphs, whereas differ signiﬁcantly (paired t-test – t1,134 =-1.18, P = 0.23) and from 19 dark x light pairings, 13 dark morph offspring (6

Table 1 Percentage of white plumage estimated from photographs of breeding black sparrowhawks, with photos spanning 4 or more years.

Percentage of white on the front (chin, throat, breast and ﬂanks) Sex Morph Mean (ϮSD) 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 Male L 78.2 (Ϯ2.3) 75 – 80 78 80 Male L 84.4 (Ϯ1.4) 84 86 84 82 84 –––85–86 Male D 5.3 (Ϯ1.2) 6 – – 5 – 577445 Female L 88.8 (Ϯ3.0) 92 – 90 90 84 88 Female D 2.6 (Ϯ0.6) 3– 2 3 Female D 4.6 (Ϯ0.6) 54–5

SD, standard deviation.

Table 2 Inheritance patterns according to the morph of the male and 120 female parents and the morph (dark/light) of the offspring for all offspring and for male and female offspring separately. 100 Male parental morph Dark Light 80 All offspring 60 Female parental morph Dark 13/0 5/0 Light 8/6 1/0 40 Male offspring Female parental morph 20

Dark 8/0 3/0 Percentage of dark/light morphs Light 3/3 NA 0 Female offspring 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 Female parental morph Year Dark 5/0 2/0 Ϯ Light 5/3 1/0 Figure 2 Percentage ( 1 standard error) of dark morph male (solid line) and female (dashed line) black sparrowhawks in the population on the Birds were ringed as chicks with unique colour-ring combination. Inher- Cape Peninsula between 2001 and 2010, from the 244 pairs for which itance patterns appear to follow a simple one-locus, two-allele system the morphs of both birds were known. There were signiﬁcantly more whereby the light allele is dominant. Light birds are therefore hetero- dark morph males than females (P < 0.001), but the frequency of dark zygous with the genotype LL, or Ld, and dark birds are homozygous and morphs did not differ over time for either sex (P > 0.60). have the genotype dd.

Weinberg equilibrium conditions. We calculated an allelic males, 7 female) and 6 light morphs (3 males, 3 females) were frequency of 0.87 for the d allele and consequently 0.13 for the produced. We had only one record of a light x light pairing L allele. We therefore expect that a minimum of 22% of birds and this produced one dark offspring (Table 2). Inheritance are heterozygous light morphs (Ld) and only around 2% of was apparently autosomal rather than sex linked because, on birds are homozygous light morphs (LL). Stated differently, several occasions, birds produced offspring of the same sex of the white morphs the vast majority (92%) are heterozygous that differed from their own morph (Table 2). However, it was (Ld) while only 8% are homozygous (LL). interesting to note that light morph males produced no light morph offspring (from six cases), whereas light females pro- Morph frequencies over time and duced light offspring at c. the 1:1 ratio predicted, although between sexes admittedly sample size for this finding is small. From these data, inheritance of morph type appears to Over the entire study period, 76% of birds were dark morph, follow a simple Mendelian one-locus, two-allele system, with the frequency being significantly higher for males than 2 whereby the light allele is dominant. Light birds are therefore females (males: 83 Ϯ 2%, females 68 Ϯ 3%; c 1 = 14.85; P = homozygous or heterozygous (LL or Ld) and dark birds are 0.0001; Fig. 2). invariably homozygous (dd). Between 2001 and 2010, the frequency of the two morphs 2 Seventy-six per cent of birds in our population were dark did not change, either for the population as a whole (c 1 = 2 morphs (see later). Assuming these dark morphs are 0.16, P = 0.68), or for either sex (males: c 1 = 0.12, P = 0.72; 2 homozygous (dd – based on the inheritance patterns observed females: c 1 = 0.06, P = 0.80; Fig. 2). Using data only from the in this investigation), we can calculate the expected frequen- first year pairs were found breeding (to avoid issues of pseudo- cies of L and d alleles in our study population under Hardy– replication), the same patterns emerged. There was no change

2 over time detected for either sex (males: c 1 = 0.02, P = 0.87; Curtis et al., 2005). Furthermore, because it is unlikely that 2 females: c 1 = 0.70, P = 0.40) and the frequency of dark these individuals would have experienced the same environ- morphs was significantly higher for males than females (males: mental conditions in the different years of their lives, it does 2 85 Ϯ 3%, females 73 Ϯ 4%; c 1 = 5.41; P = 0.02). suggest that environmental variables, such as weather, or body condition is relatively unimportant in determining the Discussion plumage patterns in this species, as Briggs et al. (2010b) also concluded. This result, together with our other findings on Our study showed that (1) black sparrowhawks in our study inheritance patterns (see later), further strengthens the argu- area display discrete polymorphism in plumage coloration; (2) ment that these plumage patterns may well be under genetic morph type and plumage patterns of individual birds change control. little, if at all, with age; (3) the observed inheritance pattern Observations of birds in adult plumage which were colour suggests that morph type is under genetic control consistent ringed as chicks with known parental morphs revealed that with a single Mendelian locus at which the light allele is domi- morph inheritance showed a classic Mendelian pattern. Dark nant; (4) the Cape Peninsula population shows a reversal of x dark crosses produced only dark offspring, dark x light the morph frequencies generally encountered in the rest of this crosses produced both dark and light morph offspring, and in species’ range, with over 75% of birds being dark morphs, and one instance a light x light cross produced a dark offspring. with significantly more dark morph males than females. Hartley (1976) also reports an instance of light x light black From our plumage scores, it was clear that although sparrowhawk pairing producing a dark morph bird. From there was considerable variation in the percentage of white these findings, it therefore appears that polymorphism in this plumage, black sparrowhawks show two distinct morphs, species is under genetic control with a one-locus, two-allele revealed as two clear modes on the histogram of percentage inheritance pattern, and that the light allele is dominant. Thus, white plumage (Fig. 1). White morphs usually had around light birds can be either homozygous (LL) or heterozygous 85–90% and never less than 70% white plumage on their front (dL), whereas dark morph birds are always homozygous (dd). whereas dark morphs usually had between 0–10% and never In this study, we have assumed no extra-pair paternity, which more than 35% white frontal plumage. There was clear sepa- although unlikely to be true, occurs at a relatively low rate ration of these modes, with no birds of intermediate plumage. among raptors (Mougeot, 2004). Our finding of no ‘impossi- Although not statistically significant, the percentage of white ble’ offspring from any pairings, given our predictions, also on the front of dark morph birds tended to be greater for suggests that extra-pair paternity was not particularly high or females than for males, potentially indicating that darker not high enough to disrupt these results. Several Accipiter spp. males may enjoy a selective advantage in this population. occurring across the globe show similar polymorphic patterns Similar sex differences have been observed for polymorphic to the black sparrowhawk (i.e. with dark or light morphs – barn owls (Tyto alba), with females on average more reddish Ferguson-Lees & Christie, 2001): it would be interesting to brown with more prominent black spotting than males know whether the same inheritance patterns also operate in (Roulin, 1999). It is also interesting that there were signifi- these species. We could not use our data on the morphs of cantly more light morph females in the population than males offspring from known parents to test accurately whether the (see later). However, whether the frequency of white morphs phenotypes of these offspring were as predicted from our in the population and the percentage of white on the front of assumed genetic inheritance patterns (i.e. one locus, two dark morph birds are in any way linked through similar selec- alleles, with the light allele being dominant), because the off- tive pressures is unknown. spring’s morph was only assigned once a bird was recruited Observation of known colour-ringed birds over time (4–11 into the adult population rather than as a chick. Thus, any years) provided strong evidence that plumage coloration in morph-linked differences in dispersal or juvenile survival this species is fixed and does not vary with age (within this would produce biased results. However, if we do assume equal study’s time frame). The species’ average life expectancy is juvenile survival rates between morphs, and given our esti- around 10 years (based on average annual adult survival rates mated distribution of genotypes [i.e. 92% of light birds being of 89% – unpublished data). Data from males and females of heterozygous (dL)], we would predict an approximate both plumage morphs suggested that the proportion of white dark : light morph ratio of 1:1.17 from our mixed-pair crosses. plumage on their front varied little with age. Indeed, the vari- However, from the 19 offspring recruited from mixed pairs, ation between years is probably attributable to observer error. we found a ratio of 2.2:1 in favour of dark morphs. Thus, Closer examination of the photographs of known birds sug- more than twice as many dark birds as expected were subse- gests that plumage variability in this species might be success- quently found breeding from these crosses. This in turn sug- fully used to identify individuals over time. For example, gests that either survival of white morphs prior to recruitment obvious features of the plumage, such as the location of dark is lower than that of dark morphs, or that light morphs dis- or light streaks, also appear to remain constant over time. This perse further away from our study areas, or that we have work therefore adds to that of Briggs et al. (2010b) in suggest- incorrectly identified the inheritance mechanism. Although ing that plumage patterns in polymorphic raptors persist over inheritance in our study was apparently not sex linked, no an individual’s lifetime, and provide further support for other light offspring were ever recruited from light fathers, and this studies that identify individuals in highly polymorphic popu- result largely explains the lower than predicted occurrence of lations by plumage alone (e.g. Krüger & Lindström, 2001; light birds recruited from mixed pairs; however, the sample

Journal of Zoology •• (2012) ••–•• © 2012 The Authors. Journal of Zoology © 2012 The Zoological Society of London 5 Polymorphism in black sparrowhawks A. Amar, A. Koeslag and O. Curtis size (n = 6) for this finding was small. To investigate this ported the idea that dark morphs are usually the rare morph further will require the use of genetic markers to test the for this species, with only around 22% (n = 36) of birds being genotypes of the chicks produced. Many studies have now dark morphs (W. Tarboton, unpublished data). What might shown the importance of the melanocortin-1 receptor gene in explain the almost complete reversal in the frequency of the determining similar plumage polymorphisms in other bird different morphs in these two study populations? There species (Mundy, 2005) including for some (Gangoso et al., are two possible explanations for this pattern. Firstly, that it 2011) but not all raptor species (Hull et al., 2010). In future is simply a founder effect, with the first colonizing birds arriv- studies, we hope that the use of molecular markers will allow ing on the Cape Peninsula being dark morphs, purely by us to determine the morph genotype of the young chicks and chance. Alternatively, that this is an adaptive response to to examine whether juvenile and sub-adult survival differs different environmental conditions (e.g. the different rainfall between morphs. seasonality of the two regions). Both populations breed Our Hardy–Weinberg estimates suggested that 92% of the over the winter months (Sebele, 2012): this period coincides light morphs in our population were heterozygous. However, with the dry season in the north and east of South Africa, but while this statistic is useful, we acknowledge that the accuracy with the wet season in the south west of the country. Thus, of Hardy–Weinberg equation relies on a number of assump- individuals breeding in our study population are exposed tions, such as no selection, no non-random genetic drift and to far higher rainfall levels during the breeding period. no gene flow, which are unlikely to be strictly true in our study Recent reviews on the causes and functions of polymorphism population. For the current study, we have focused on poly- (Galeotti et al., 2003; Roulin, 2004) have both suggested a morphism of adult black sparrowhawks. However, juvenile strong link between light conditions and variations in black sparrowhawks are also polymorphic, displaying a pale plumage, with crypsis (background matching) likely to play a morph and a rufous morph (Ferguson-Lees & Christie, 2001). key role. Thus, it may be that dark morph birds in our study Initially, juvenile morphs were thought to be sex linked; population are at a selective advantage because they benefit however, pale and rufous juveniles of both sexes have been from improved hunting efficiency in the poorer light condi- found in the same nest (Ferguson-Lees & Christie, 2001). tions that would be associated with higher rainfall. As with Juvenile morph is also apparently not directly linked to adult most Accipiters, males provide most of the food during the phenotype, because of two rufous juveniles that were followed breeding season, feeding the female during the incubation and into adulthood, one became a light morph and the other a early nestling stage, and this could explain the different dark morph adult (Ferguson-Lees & Christie, 2001). Rather, morph frequencies between sexes if there is greater selection we hypothesize that juvenile morphs could be linked to the pressure for males to be dark than females. Similar relation- adult morph genotype in the following way: birds that carry ships between habitat background and colour-morph ratio the recessive dark allele would be rufous juveniles and those have been identified for other bird species (e.g. Rohwer, birds that are homozygous light morphs (LL) would be pale 1990). Alternatively, pressure from parasites may be greater morphs. Unfortunately, we do not yet have the data to test in these wet conditions which may favour dark morphs, this hypothesis (e.g. from enough chicks with known morphs). as different raptor morphs can show different immune The higher frequency of dark morph males as compared responses (Gangoso et al., 2011) and subsequent parasite with females was an interesting result. One possible explana- loads (Chakarov, Boerner & Kruger, 2008). It is also possible tion for this could be that dark morph males survive better that dark morph birds have a thermal advantage in these than dark morph females, and thus more dark morph males colder wet conditions or that darker birds are able to with- are recruited into the population. Again, an alternative expla- stand the feather degrading bacteria which may be more nation could be that females disperse further than males and abundant or virulent in such conditions (Burtt & Ichida, that immigrant females come from population with a lower 2004). To test further whether the unique morph ratios found frequency of dark morphs. However, of the six light birds in this population are likely to be an adaptive trait, future recruited into the population, three were male and three were research will focus on whether dark morphs have any selective female. Alternatively, this difference could have come about advantage by comparing reproductive output and survival through mate choice, for example, if males actively select light with light morph birds: the findings presented here lay the females or if females actively select dark males, such similar foundations for this future research. mate choice has been reported for other species (Knapton & Falls, 1983; O’Donald, 1983), and therefore remains a poten- Acknowledgements tial explanation for this finding. Dark morph adults were the more common (> 75%) morph We are very grateful to Sharon Yodaiken and Gerry Meihui- in our population, which contrasts with most other sources zen for all their help in the field. We are also grateful to that suggest that dark morphs are the rarer morph for this Jacqueline Bishop and Gareth Tate who helped improve the species (Steyn, 1982; Kemp & Kemp, 1998; Ferguson-Lees & manuscript immensely. We thank Warwick Tarboton for pro- Christie, 2001; Hockey et al., 2005). We are unaware of any viding unpublished information on the morphs of his study published data on the morph frequency from other popula- population. Thanks are also due to Lovelater Sebele, Fitzum tions. However, unpublished data from a population studied Baldi and Rowan Martin for useful discussions and advice. in eastern Mpumalanga (formerly known as the Transvaal), We thank M. Boerner and an anonymous reviewer for their South Africa (for details, see Tarboton & Allan, 1984), sup- comments which greatly improved the manuscript. We are

6 Journal of Zoology •• (2012) ••–•• © 2012 The Authors. Journal of Zoology © 2012 The Zoological Society of London A. Amar, A. Koeslag and O. Curtis Polymorphism in black sparrowhawks also grateful to all the land owners who have granted us access Galeotti, P., Rubolini, D., Dunn, P.O. & Fasola, M. (2003). to carry out fieldwork on their land, and we are particularly Colour polymorphism in birds: causes and functions. grateful to South African National Parks for access to the J. Evol. Biol. 16, 635–646. Table Mountain National Park. Gangoso, L., Grande, J.M., Ducrest, A.L., Figuerola, J., Bortolotti, G.R., Andrés, J.A. & Roulin, A. (2011). MC1R-dependent, melanin-based colour polymorphism is References associated with cell-mediated response in the Eleonora’s falcon. J. Evol. Biol. 24, 2055–2063. Berger, D.D. & Mueller, H.C. (1959). The bal-chatri: a trap Hartley, R. (1976). Some notes on the plumages of the black for the birds of prey. Bird-Banding 30, 18–26. sparrowhawk. 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