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Ultraviolet Sexual Dimorphism and Assortative Mating in Blue Tits

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Ultraviolet Sexual Dimorphism and Assortative Mating in Blue Tits Ultraviolet sexual dimorphism and assortative mating in blue tits Sta¡an Andersson*, Jonas O« rnborg and Malte Andersson Department of Zoology, University of Go« teborg, Medicinaregatan 18, S- 413 90 Go« teborg, Sweden In spite of strong evidence for viability-based sexual selection and sex ratio adjustments, the blue tit, Parus caeruleus, is regarded as nearly sexually monomorphic and no epigamic signals have been found. The plumage coloration has not, however, been studied in relation to bird vision, which extends to the UV-A waveband (320^400 nm). Using molecular sex determination and UV/VIS spectrometry, we report here that blue tits are sexually dichromatic in UV/blue spectral purity (chroma) of the brilliant crown patch. It is displayed in courtship by horizontal posturing and erected nape feathers. A previously undescribed sexual dimorphism in crown size (controlling for body size) further supports its role as an epigamic orna- ment. Against `grey-brown' leaf litter and bark during pair formation in early spring, but also against green vegetation, UV contributes strongly to conspicuousness and sexual dimorphism. This should be further enhanced by the UV/bluish early morning skylight (`woodland shade') in which blue tits display. Among 18 breeding pairs, there was strong assortative mating with respect to UV chroma, but not size, of the crown ornament. We conclude that blue tits are markedly sex dimorphic in their own visual world, and that UV/violet coloration probably plays a role in blue tit mate acquisition. Keywords: UV vision; spectral re£ectance; colour signalling; sexual dichromatism; colour contrast; Parus caeruleus (Chen & Goldsmith 1986; Maier 1994; Bowmaker et al. 1. INTRODUCTION 1997). This cone seems to be present also in the blue tit The blue tit, Parus caeruleus, is the only regularly polygy- retina (N. Hart, unpublished observations). A lower spec- nous parid (Kempenaers 1995). Females acquire extra- tral limit at 320 nm of the avian visual range is indicated pair fertilizations from males with better survival than by lens transmission that cuts o¡ sharply in this region their social partner (Kempenaers et al. 1992), and even (Goldsmith 1990; Maier 1994). Although the adaptive adjust o¡spring sex ratio towards sons when mated to function of avian UV vision has long-remained obscure such high-quality males (Svensson & Nilsson 1996). This (Bennett & Cuthill 1994; Goldsmith 1994), there is now suggests viability-based sexual selection (Andersson 1994), accumulating evidence for colour-based mate choice in but a question left unanswered is how females judge the the UV (Bennett et al. 1996; Andersson & Amundsen quality of their mate (Kempenaers et al. 1992). 1997; Bennett et al. 1997). Recently, a potential acoustic signal was suggested from By using UV/VIS spectrometry over the 320^700 nm longer song strophes of extra-pair fathers, but in visual spectral window, we explore the possible sexual traits their leg length di¡ered from the within-pair dimorphism, signal quality and social function of the bril- fathers by only 0.4 mm (Kempenaers et al. 1997). This liant blue crown patch in blue tits. This plumage trait is slight di¡erence in tarsus length seems unlikely to be the displayed in agonistic and sexual interactions by hori- basis for discrimination between prospective mates. The zontal `head-forward' postures and erected nape feathers striking blue and yellow plumage suggests that visual (Stokes 1960). Therefore, the blue tit crown might also be ornamentation may be more likely. However, although used for signalling in the UV part of the spectrum. In a male blue tits in the hand often appear `brighter blue' breeding population of blue tits in south-western Sweden, than females (Perrins 1979), standard literature describes we ¢nd strong evidence to support this. the plumage as closely similar between the sexes (Cramp & Perrins 1993) and considers it to be of only secondary epigamic value (Stokes 1960). The main problem with 2. METHODS these conclusions is, however, that they are based on the Fieldwork was done in April to June 1995 in a deciduous forest UV-blind and yellow-biased human eye. with nestboxes in Gunnebo, 5 km SE of Go« teborg, Sweden. Birds Perception of UV-A (320^400 nm) is a common feature were captured with song playback in mistnets or nestbox traps, of birds, including Parus species and other passerines and transported to a nearby (55 min) cottage for morphometric (Bennett & Cuthill 1994), and is achieved through a UV and spectrometric measurements and preliminary sexing and cone mechanism absorbing maximally at 360^380 nm aging (1 or 2+ years old, see Svensson 1992). All birds were banded with unique colour combinations, excluding yellow and *Author for correspondence ([email protected]). blue hues matching the plumage. To con¢rm initial assignments Proc. R. Soc. Lond. B (1998) 265, 445^450 445 & 1998 The Royal Society Received 29 September 1997 Accepted 3 November 1997 446 S. Andersson and others UV dimorphism in blue tits to pairs, nestboxes were visited repeatedly during incubation to Variations in these measures were found to correlate strongly identify the individuals. (rs40.9) with the human CIELAB hue colorimetric (S. Andersson, unpublished data), and should be a reasonable (a) Sex determination predictors of hue variation in any colour opponency system. As morphological sexing criteria (mainly wing length; The conspicuousness of a colour signal depends critically on Svensson 1992) are not fully reliable, a small (50 ml) blood the adapting background against which it is seen. We estimated sample was also drawn from the carpal vein for molecular sex contrast objectively by a signal (Rs) versus background (Rb) identi¢cation according to Ellegren (1996). DNA was extracted re£ectance ratio ((Rs7Rb)/Rb)) (see Endler & Thery 1996). For with Qiagen blood amp kit (Qiagen Inc., Hilden, Germany). background spectra we measured the re£ectances from various With minor deviations from Ellegren's (1996) polymerase chain natural surfaces in the blue tit habitat, but we simplify here to reaction protocol, we used his primers 2945F, cfR and 3224R to two general surface re£ectance types in terrestrial, vegetated amplify a 630 b.p. fragment of the autosomal or Z-linked (i.e. habitats (Osorio & Bossomaier 1992). The ¢rst general back- both sexes) avian CHD gene, along with a 210 b.p. fragment ground type, `grey-brown', includes soil, bark and dead plants. from a W-linked copy of the same gene (i.e. only in females). These are characterized by low UV and then rather uniformly The products were visualized and size-determined (Pharmacia increasing re£ectance from 400 to 700 nm, gently for grey and 100 b.p. ladder) on agarose gels as one strong band for all indivi- dark brown and steeper for browns and reddish browns (¢gure duals, and a weaker additional band in females. 1a; see also Wyszecki & Stiles (1982), pp. 60^63). Because blue tit pair formation occurs before leaf emergence in Scandinavia (b) Re£ectance spectrometry (Cramp & Perrins 1993), and as the crown is displayed upwards Re£ected radiance from the central crown (and other plumage (Stokes 1960), it is viewed against the forest £oor which at this regions; Andersson & O« rnborg1998) was measured with a S1000 time of year consists mainly of dead leaf litter, grass and herbs. diode-array spectrometer (Ocean Optics Inc., Dunedin, USA), Bark and bare soil further contribute to the `grey-brown' back- and a trifurcated ¢bre optic probe with six 200 mm illuminating ground, whereas `leaf-green' colours (see below) are less ¢bres surrounding a 200 mm measuring ¢bre that accepted light common (except in habitats with much mosses or other ever- from a 288 solid angle. The probe was mounted inside a matt green plants). We use here the re£ectance from dead, dry oak black plastic tube (inner diameter 7 mm) with the end cut to leaves (¢gure 1a) to estimate the contrast against `grey-brown' 458. The tube end was held lightly against the crown plumage backgrounds. and rotated perpendicularly to the length axis of the head, From growing herbs and emerging leaves (early May on the providing 458/458 illumination and recording from an oval west coast of Swedish) the `grey-browns' gradually give way to 3 mmÂ3.8 mm measuring spot. One illumination ¢bre was the `leaf-green' spectrum common to most land plants (Osorio connected to an Ocean Optics LS-1 tungsten-halogen lamp, and & Bossomaier 1992). This has a typical peak (caused by chloro- the other to an UV-1A deuterium lamp (A.I.S. Inc., New Jersey, phyll) at about 550 nm, decreasing below 500 nm and into the USA). Together these light sources provided light from 280 to UV (¢gure 1a). Spectral shape variation is small and mainly in 730 nm, su¤cient for our target range of 320^700 nm. Using the the long wavelength end of the spectrum (Lythgoe 1979; Osorio C-spec software (Ancal Inc., Las Vegas, USA), spectral re£ec- & Bossomaier 1992). For the `leaf-green' background type, we use tance was measured in relation to a Spectralon (LabSphere here the average leaf re£ectance from three common tree species Inc., North Sutton, USA) white standard, an almost perfect in the blue tit habitat: maple (Acer platanifolius), birch (Betula di¡user (98^99% re£ectance from 300 to 750 nm) measured pubescens) and hazel (Corylus avellana) (¢gure 1a). before each scan. The re£ectance from each individual was aver- aged from ¢ve scans, removing the probe between each. 3. RESULTS (c) Objective colorimetrics (a) Sexual dimorphism Colour analyses, in terms of intensity (brightness) and spectral Forty-one blue tits (14 subadult and nine adult females, shape (hue, chroma), were restricted to the 320^700 nm spectral 12 subadult and six adult males) were measured (in total, window, as suggested by the lens transmission cut-o¡ at 320 nm 18 breeding pairs and ¢ve additional females).
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