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

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