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Home , Aquilinae, Booted eagles, Common buzzard, Hieraaetus, Little eagle

Australian Field Ornithology 2020, 37, 124–128 http://dx.doi.org/10.20938/afo37124128

Inheritance of plumage morphs in Little morphnoides in northern New South

Candice Larkin* and S.J.S. Debus

Zoology, University of New , Armidale NSW 2351, *Corresponding author. Email: [email protected]

Abstract. and inheritance of plumage colour in the Little Hieraaetus morphnoides were studied in northern , by tallying records of parental morph combinations in breeding pairs and the morphs of their offspring in the 1980s, 2000s and 2017–2019 (n = 41 pair combinations). The average ratio in breeding adults was 4.9 light: 1 dark, with dark males outnumbering dark females (1.8:1). Light × light pairs always produced light young (n = 32). Dark male × light female pairs variously produced light and dark offspring of both sexes (n = 12). Light male × dark female pairs produced dark young of either sex (n = 4) and one light young of unknown sex. One dark × dark pair produced a dark young. We conclude a Mendelian inheritance pattern with the dark morph recessive. From a small sample of mixed pairs with a dark male, the ratio of offspring morphs did not differ significantly from that expected by the Hardy–Weinberg equation, but mixed pairs with a light male produced 4 dark offspring to one light, versus the expected Hardy–Weinberg ratio of 1.95 light: 1 dark. This outcome suggests a non-random transmission of the dark allele by heterozygous light males, and a similar pattern of inheritance to that in the related H. pennatus.

Introduction

Colour polymorphism is common in raptors, notably the (hawks and eagles) (e.g. Ferguson- Lees & Christie 2005; Bosch et al. 2019). A key question concerns the function of polymorphism and why it is evolutionarily stable (e.g. Galeotti et al. 2003; Roulin 2004). There may be a link with niche and breadth, use of open or semi-open , and a -rich diet, with the morphs having differential advantages in different habitats or lighting conditions (Galeotti et al. 2003; Roulin & Wink 2003). Among Australian raptors, the Brown Falco berigora has been considered to be polymorphic (e.g. Marchant & Higgins 1993). However, much of its plumage variation and so-called ‘morphs’, at least in south-eastern Australia, are related to age and gender (McDonald 2003), and the situation requires further resolution. Otherwise, the Figure 1. Adult light-morph in flight. Photo: Grey Goshawk novaehollandiae is polymorphic, David Whelan with grey and white morphs. Mixed pairs of that produce grey fledglings (Hollands 2003; SJSD pers. obs.) or white fledglings (R. Bilney pers. comm.), the latter presumably involving a heterozygous grey parent, and white pairs produce white offspring (Cupper & Cupper 1981), all of which suggests a simple dominant/recessive mechanism. The Little Eagle Hieraaetus morphnoides, like the other four species in the as currently constituted (Clark 2012; Lerner et al. 2017), is polymorphic, with discrete light and dark morphs (e.g. Ferguson-Lees & Christie 2005; Gjershaug et al. 2009). The defining character of the two morphs is the colour of the greater underwing-coverts, producing a solid dark underwing in the dark morph, which is also browner ventrally (Figures 1 and 2) (see e.g. Debus 1989, 2017; Marchant & Higgins 1993). An alleged rufous morph, represented by a single museum specimen and no field sightings or reports, is best regarded as an aberrant, Figure 2. Adult dark-morph Little Eagle in flight. Photo: exceptionally heavily pigmented light morph (Debus 1989; David Whelan Inheritance of plumage morphs in Little Eagle 125

Marchant & Higgins 1993). The Little Eagle forages in or each of those studies. In 1980, nine breeding pairs were over a range of habitats from to , mainly monitored, four of these also monitored in 1981, and two or open woodland, and in monitored opportunistically through the mid-to-late 1980s. preys on a range of though mostly ; In 2006–2009, seven breeding pairs were monitored successful broods are usually of one fledgling (e.g. in 2006, four of these in 2007, four in 2008 (including a Marchant & Higgins 1993; Debus 2017). The species is ‘new’ pair), and two in 2009 (including a ‘new’ pair). In strongly sexually size-dimorphic (e.g. Marchant & Higgins 2017–2019, 12, nine and seven breeding pairs were 1993), meaning that members of a pair can be sexed monitored in each year, respectively, as new pairs were by size (when together) and breeding behaviour, and found while some previously known pairs continued to be fledglings can be sexed (with high likelihood) when with monitored (though many did not breed in the drought of the parent(s) (see also Bosch et al. 2019). 2019), for an overall total of 22 pairs. In each time period, the Eagles were not marked, so the identity of randomly Debus (1989) presented preliminary findings from the sighted adults (away from ) was uncertain and 1980s on the ratio of morphs in the Little Eagle and the not included in calculations for breeding pairs. Over the offspring morph of parental morph combinations, and decades, some pairs (territories) closest to Armidale city speculated on the genetics (possible sex-linkage and have been lost to urban expansion (e.g. Larkin et al. 2020), homozygosity/heterozygosity). Debus (2011) followed up but the study expanded to include additional pairs farther with quantification of offspring morphs from parental morph away. combinations in the same area (Northern Tablelands of New South Wales), from field studies in 2006–2009. Here The putative gender of offspring was assigned from visual we combine and expand those data with findings from assessment (through binoculars and telescope) of sexual a larger sample of pairs and their offspring in the same size-dimorphism of fledglings against their parent(s), based area in 2017–2019 (Larkin et al. 2020; CL & SJSD unpubl. on SJSD’s prior handling of adult and juvenile Little Eagles data). Meanwhile, a detailed analysis of morph ratios and of both sexes, although in some cases offspring gender inheritance patterns in the closely related Booted Eagle was not determined. To minimise disturbance to nests Hieraaetus pennatus (Bosch et al. 2019) provides some of this threatened species, -trees were not climbed, perspective on morphs and their inheritance in the Little nor nestlings handled or measured. Parentage was also Eagle. The morphs are lifelong plumage types, not age- putative (i.e. assumed no extra-pair copulations; no DNA related phases, and within morphs there is little colour investigation conducted), although extra-pair offspring in change from juvenile to adult, juveniles being ‘redder’ on raptors are rare (Roulin et al. 2004). the head and underbody than the respective adults (e.g. The Hardy–Weinberg equilibrium equation was used to Debus 1989). calculate the theoretical carrier (heterozygous) frequency, In our study we investigated the offspring morphs of based on the proportion of the recessive morph in the different parental morph combinations, in order to elucidate population (following e.g. Amar et al. 2013; Bosch et al. the mechanism of inheritance. We further hypothesise that 2019): the morphs may have differential survival or productivity p + q = 1, and p2 + 2pq + q2 = 1 in different environments as an area for potential future study (cf. relevant findings reported for the Booted Eagle where p is the frequency (% as a decimal) of the dominant by Bosch 2019 and Bosch et al. 2019). allele (here the light morph), q is the frequency of the recessive allele (here dark), and 2pq is the frequency of the heterozygous condition (here phenotypically light) Study area and methods in the population. The hypothesised homozygous and heterozygous proportions in the light morph in the sample The area sampled was centred on Armidale (30°30′S, population as a whole were then used in an online Hardy– 151°40′E) on the Northern Tablelands of New South Wales, Weinberg calculator (https://wpcalc.com/en/equilibrium- extending 60–80 km north-west to south, but mostly within hardy-weinberg/) to compare the observed versus expected a 20-km radius of the city. The study area is described frequency of offspring morph ratios in the combinations of by Debus & Ley (2009) and Larkin et al. (2020), and a light × dark parents in Table 1. contextual map is provided by Debus (2008). Locally, Little Eagles inhabit remnant eucalypt open forest and woodland in undulating country at ~1000 m above sea level, and Results their foraging extends into more open habitats (scattered woodland and adjoining pasture). The climate is temperate Plumage morphs in breeding pairs subhumid, with rainfall slightly summer-dominant. The number of pairs and their morph combinations In the 1980s, there were seven light × light pairs, one dark were tallied from studies of breeding pairs spanning male × light female pair and one light male × dark female three time periods: the 1980s (Debus 1989, 1991), 2000s pair known (n = 9 pairs). In the 2000s, there were seven (Debus 2011) and 2017–2019 (Larkin et al. 2020; SJSD light × light pairs, one dark male × light female pair, one & CL unpubl. data), not double-counting instances of the light male × dark female pair and one dark × dark pair same sex/morph combination (e.g. light × light pairs) in known (n = 10 pairs). In 2017–2019, there were 14 light × two territories in 2006–2009 and 2017–2019 where the light pairs, six dark male × light female pairs and two light same individuals might have been involved. Similarly, male × dark female pairs known (n = 22 pairs). The overall the numbers of progeny by morph and gender were ratio in the breeding population was 4.9 light: 1 dark, with tallied for these ‘pair-events’ where some pairs and their dark males outnumbering dark females by 1.8:1. Taking fledglings were monitored for 2–3 consecutive years in the larger sample size for 2017–2019 alone (n = 22 pairs), 126 Australian Field Ornithology C. Larkin & S.J.S. Debus

Table 1. Parental morph combination and offspring morph offspring of either morph when the male is dark, and mostly in the Little Eagle near Armidale, New South Wales, dark offspring when the female is dark. We had only one presented as breeding ‘pair-events’ (i.e. a few cases of case of light offspring from a dark female. It appears that progeny over 2–3 consecutive years from individual pairs, although most events are for different pairs and/ female parental morph may strongly influence offspring or decades). Data pooled from the 1980s (Debus 1989, morph, although a larger sample size is required to 1991), 2006–2009 (Debus 2011) and 2017–2019 (Larkin et determine the ratio of dark to light offspring from mixed al. 2020; SJSD & CL unpubl. data). M = male, F = female; pairs in which the female is dark. Such mixed pairs in the ? = offspring gender unknown. Gender of fledged offspring Booted Eagle do produce some light offspring, though less based on sexual size-dimorphism against parent(s). frequently than dark offspring (Bosch et al. 2019). Bosch et al. (2020) found that (presumably heterozygous) light Pair combination Progeny × light Booted Eagle pairs occasionally produce a dark Light Dark young, but we detected no such instances in our sample M F ? M F ? size of light Little Eagle pairs. Light × Light (n = 32) 16 8 8 From the foregoing results, for the Little Eagle we Dark M × Light F (n = 12) 2 2 3 3 1 1 conclude a Mendelian inheritance pattern with the dark Light M × Dark F (n = 5) 1 2 1 1 morph recessive. The outcome of the Hardy–Weinberg calculations suggests a possible selective pairing through Dark × Dark (n = 1) 1 imprinting (e.g. Krüger et al. 2001 on Common Total pair-events = 50 buteo), and/or a possible non-random transmission of the dark allele by heterozygous light males. the ratio in the breeding population was 4.5 light: 1 dark, The findings of Martínez et al. (2016) and Bosch et al. with dark males recorded three times as frequently as dark (2019) on the Booted Eagle’s morphs are similar to ours on females. the Little Eagle. Both studies on the Booted Eagle variously found a predominance of the light morph in the population, though more dark females than dark males, and offspring Plumage morphs in progeny morph linked to the morph of the female parent. Those findings suggest a situation more complex in the Little Light × light parents (n = 32) always produced light Eagle than originally suggested by Debus (1989). Although offspring (n = 32; Table 1). Dark male × light female parents Bosch et al. (2019) similarly proposed a simple Mendelian (n = 12) produced young of either morph and gender inheritance with the light morph dominant, they suggested (n = 12), although light offspring were more frequent than two loci with epistasis (i.e. masking or modifying of the dark (1.4:1). A small sample of light male × dark female phenotype of one locus) and two alleles per locus, no sex- parents (n = 5) produced dark offspring of either gender linkage, and a transmission-ratio distortion in heterozygous (n = 4), and one light young of unknown gender. One dark × light-morph males. There is obvious scope for similar dark pair produced one dark male offspring. Many or most investigation in the Little Eagle. For instance, it is unclear offspring of undetermined gender were probably female, why dark female should outnumber dark because young males were often active and airborne early males in Mediterranean and the reverse for Little in the post-fledging period, whereas new female fledglings Eagles in Australia. This difference may relate to hunting were often reluctant to fly, stayed hidden in tree canopies success of males (the main food providers during the and could be difficult to see or judge relative size (SJSD breeding cycle), via a differential effect of morph colour in pers. obs.). Therefore, the sex-ratio of progeny may be the different environments. more even than suggested by Table 1. The ratio of light to The morph ratio in breeding pairs of Little Eagles near dark offspring overall was 4.0:1, similar to that in the adult Armidale was fairly similar (4.9 light: 1 dark) to that for breeding population, and among fledglings dark males the Northern Tablelands region based on the frequency outnumbered dark females by 3.0:1, again similar to the of sightings (3.3:1, reported by Debus 1989). Sample ratio in the adult population. sizes are too small to test for stability in the morph ratio Applying the theoretical Hardy–Weinberg equilibrium, over time. The morph ratio in fledglings appears similar to assuming no selective mating and no non-random genetic that in the adult population, consistent with the apparent transmission, of the pairs with a dark male and light female, philopatry of at least some juveniles that disperse or the expected number of chicks of each morph (1.92 light: migrate away from the natal territory for their first winter 1 dark) did not differ significantly from that obtained and then return to the general region (Rae et al. 2019). (1.4 light: 1 dark; χ2 = 0.4223, P >0.05). In contrast, for pairs There is regional variation in the morph ratio in Little with a light male and dark female (albeit a small sample), Eagles, with the dark morph most frequent in humid four dark and one light offspring were produced, versus the regions and the light morph most frequent in arid regions expected Hardy–Weinberg ratio of 1.95 light: 1 dark. (Debus 1989), suggesting differential selection on the morphs in different environments. Such is consistent with Gloger’s Rule (Romano et al. 2019). Comparative data are Discussion lacking on the fledgling morph ratio in, for example, humid versus arid regions to see if it tracks parental morph ratio Overall, our findings elaborate upon the inferences of within a given region. The morph ratio in the Booted Eagle Debus (1989, 2011) on the offspring morphs of different also varies regionally, with a similar trend in relation to arid parental morph combinations. That is, light pairs (almost?) versus humid environments (Gjershaug et al. 2009; Bosch always produce light offspring; mixed pairs produce 2019). Inheritance of plumage morphs in Little Eagle 127

Juvenile Booted Eagle morphs have physiological Bosch, J. (2019). Clinal polymorphism variation in the Booted differences that affect body condition in nestlings and Eagle Hieraaetus pennatus: The influence of climate during the potentially their fitness in different environments, which breeding season. Study 66, 306–316. may maintain polymorphism in their populations (Galván Bosch, J., Calvo, J.F., Martínez, J.E., Baiges, C., Mestre, J. & Jiménez-Franco, M.V. (2020). Evidence of non-random mating et al. 2010). There was no effect of parental morph on in a colour polymorphic raptor, the Booted Eagle. Journal of Booted Eagle annual breeding productivity, although the Ornithology 161, 849–857. morphs may differ in survival, longevity, offspring quality Bosch, J., Mestre, J., Baiges, C., Martínez, J.E., Calvo, J.F. & and lifetime reproductive success (Martínez et al. 2016). Jiménez-Franco, M.V. (2019). 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(2010). that the few dark eaglets from light × light pairs suggest Antioxidant machinery differs between melanic and light a lower frequency of heterozygous light × light pairs nestlings of two polymorphic raptors. PLoS ONE 5 (10), e13369. than expected. Possible mechanisms suggested include Gjershaug, J.O., Lerner, H.R.L. & Diserud, O.H. (2009). heterozygous light males selecting mates of their mother’s and distribution of the Pygmy Eagle Aquila (Hieraaetus) weiskei colour (i.e. dark), or (presumably homozygous) light birds (: Accipitridae). Zootaxa 2326, 24–38. Hollands, D. (2003). Eagles, Hawks and of Australia. selecting heterozygous birds as mates by as yet unknown 2nd edn. Bloomings Books, Melbourne. cues (physical or behavioural). These aspects suggest Krüger, O., Lindström, J. & Amos, W. (2001). Maladaptive mate intriguing avenues for further research, but would require choice maintained by heterozygote advantage. 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