Sarah R. Pryke

Multiple receivers, multiple ornaments, and a trade-off between agonistic and epigamic signaling in a widowbird

Sexual displays often involve several different ornamental traits. Yet most indicator models of sexual selection based on a single receiver (usually a choosy female) find that multiple handicap signals should be unstable. Here we study reasons for this contradiction, analyzing signal function, signal content, and trade‐offs between signals in the polygynous red‐collared widowbird Euplectes ardens. Males have both a long, graduated tail and a red carotenoid collar badge. Territory‐holding “residents” have slightly shorter tails than the nonbreeding “floaters,” but their carotenoid collars are 40% larger, and they have (on the basis of reflectance spectrometry and objective colorimetry) a 23‐nm more long‐wave (“redder”) hue than floaters. This corroborates experimental evidence that the red collar is selected by male contest competition, whereas female choice is based almost exclusively on male tail length. Tail length is negatively correlated with the carotenoid signal, which together with body size and condition explains 55% of the variation in tail length. The trade‐off in tail length and carotenoid investment is steeper among residents, suggesting an interaction with costs of territory defense. We propose that the “multiple receiver hypothesis” can explain the coexistence of multiple handicap signals. Furthermore, the trade‐off between signal expressions might contribute to the inverse relation between nuptial tail elongation and coloration in the genus Euplectes (bishops and widowbirds).

Red dominates black: agonistic signalling among head morphs in the colour polymorphic Gouldian finch

Recent sexual selection studies on the evolution of bird colouration have mainly focused on signals with a high level of condition-dependent variation, with much less attention given to colour traits whose expression is genetically controlled. Here, we experimentally tested the relative importance of a genetic colour polymorphism in determining male dominance in the Gouldian finch (Erythrura gouldiae), a species displaying three completely discrete but naturally co-occurring genetically inherited phenotypes; yellow-, red- (carotenoid) and black-headed (melanin) morphs. First, in staged dominance contests between unfamiliar birds of different head morphs, red-headed males dominated black-headed males, both of which dominated the yellow-headed birds. Second, within morphs, the intensity and size of the strongly ultraviolet-blue collar determined the outcome of these contests, and among the red-headed males, redder males dominated less chromatic birds. Lastly, when the dominance signal of red-headed birds was experimentally destabilized (i.e. blackened or reddened), naturally red-headed morphs continued to dominate both the black-and yellow-headed morphs. Together, these results suggest that intrinsic dominance-related behavioural differences between the three colour morphs, which are likely to influence the relative fitness of each morph, contribute to the complex selective patterns maintaining these three discrete phenotypes in relatively stable frequencies in wild populations.

Agonistic carotenoid signalling in male red-collared widowbirds: aggression related to the colour signal of both the territory owner and model intruder

Carotenoid colour displays are widely assumed to be honest indicators of individual health or quality, primarily in mate attraction. Here we show that sexually dimorphic carotenoid ornamentation functions as an agonistic signal in male red-collared widowbirds, Euplectes ardens. Mounted male models differing (within natural limits) in the intensity of carotenoid signalling were presented to wild resident males as simulated intruders, perched or made to ‘fly’ across the territory with the elongated tail folded or keeled. Perched mounts were generally ignored, and stronger aggression towards ‘flying’ models with a keeled tail (i.e. as in courtship display) than a folded tail suggests the tail display is used to assess the intention of intruding males. Territory owners were less aggressive towards models with intense collar display, suggesting that carotenoid coloration functions as a badge of status in this species. The level of aggressive response was also related to the resident’s own badge in that males with larger, redder collars responded more aggressively to the models. In addition, males with a larger collar signal defended larger territories and spent less time in territory defence. Apart from the collar size and ‘redness’, no other morphological variable predicted the aggressive response of territorial males. Given the previously demonstrated insignificance of the collar in female mate choice, we suggest that the nuptial carotenoid coloration is an honest signal of dominance or fighting ability, sexually selected through male contest competition over territories.  2001 The Association for the Study of Animal Behaviour

SEXUAL SELECTION OF MULTIPLE HANDICAPS IN THE RED‐COLLARED WIDOWBIRD: FEMALE CHOICE OF TAIL LENGTH BUT NOT CAROTENOID DISPLAY

Abstract.— Although sexual selection through female choice explains exaggerated male ornaments in many species, the evolution of the multicomponent nature of most sexual displays remains poorly understood. Theoretical models suggest that handicap signaling should converge on a single most informative quality indicator, whereas additional signals are more likely to be arbitrary Fisherian traits, amplifiers, or exploitations of receiver psychology. Male nuptial plumage in the highly polygynous red‐collared widowbird (Euplectes ardens) comprises two of the commonly advocated quality advertisements (handicaps) in birds: a long graduated tail and red carotenoid coloration. Here we use multivariate selection analysis to investigate female choice in relation to male tail length, color (reflectance) of the collar, other aspects of morphology, ectoparasite load, display rate, and territory quality. The order and total number of active nests obtained are used as measures of male reproductive success. We demonstrate a strong female preference and net sexual selection for long tails, but marginal or no effects of color, morphology, or territory quality. Tail length explained 47% of male reproductive success, an unusually strong fitness effect of natural ornament variation. Fluctuating tail asymmetry was unrelated to tail length, and had no impact on mating success. For the red collar, there was negative net selection on collar area, presumably via its negative relationship with tail length. None of the color variables (hue, chroma, and brightness) had significant selection differentials, but a partial effect (selection gradient) of chroma might represent a color preference when tail length is controlled for. We suggest that the red collar functions in male agonistic interactions, which has been strongly supported by subsequent work. Thus, female choice targets only one handicap, extreme tail elongation, disregarding or even selecting against the carotenoid display. We discuss whether long tails might be better indicators of genetic quality than carotenoid pigmentation. As regards the evolution of multiple ornaments, we propose that multiple handicap signaling is stable not because of multiple messages but because of multiple receivers, in this case females and males.

Frequency-dependent physiological trade-offs between competing colour morphs

Evolutionary theory suggests that alternative colour morphs (i.e. genetically controlled phenotypes) may derive similar fitness under frequency-dependent selection. Here we experimentally demonstrate opposing effects of frequency-dependent social environments on plasma hormone levels (testosterone and corticosterone) and immune function between red- and black-headed male morphs of the Gouldian finch (Erythrura gouldiae). Red-headed males are highly sensitive to changes in the social environment, especially towards the relative density of their own aggressive morph, exhibiting high stress responses and immunosuppression in socially competitive environments. In contrast, the non-aggressive black-headed males follow a more passive strategy that appears to buffer them against social stresses. The differential effect of hormones on aggressive behaviour and immune performance reinforces the contrasting behavioural strategies employed by these colour morphs, and highlights the importance of the social environment in determining the individual basis of behavioural and physiological responses.

The relative role of male vs. female mate choice in maintaining assortative pairing among discrete colour morphs

Mate choice has important evolutionary consequences because it influences assortative mating and the level of genetic variation maintained within populations. In species with genetically determined polymorphisms, nonrandom mate choice may affect the evolutionary stability and maintenance (or loss) of alternative phenotypes. We examined the mating pattern in the colour polymorphic Gouldian finch (Erythrura gouldiae), and the role of mate choice, both female and male, in maintaining the three discrete head colours (black, red and yellow). In both large captive and wild populations, Gouldian finches paired assortatively with respect to head colour. In mate choice trials, females showed a strong preference for mates with the most elaborate sexually dimorphic traits (i.e. more chromatic UV/blue plumage and longer pin‐tail feathers), but did not discriminate assortatively. Unexpectedly, however, males were particularly choosy, associating and pairing only with females of their own morph‐type. Although female mate choice is generally invoked as the major selective force maintaining conspicuous male colouration in sexually dichromatic species, and is typically thought to drive nonrandom mating, these findings suggest that mutual mate choice and male mate choice in particular, are an important yet neglected component of selection.

Genetic Incompatibility Drives Sex Allocation and Maternal Investment in a Polymorphic Finch

Genetic compatibility may drive individual mate choice decisions because of predictable fitness effects associated with breeding with incompatible partners. In Gouldian finches (Erythrura gouldiae), females paired with genetically incompatible males of alternative color morphs overproduce sons, presumably to reduce investment in inviable daughters. We also observed a reduced overall investment in clutch size, egg size, and care to offspring resulting from incompatible matings. Within-female experimental pairings demonstrate that female birds have the ability to adaptively adjust the sex of their eggs and allocate resources on the basis of partner quality. Female Gouldian finches thus make cumulative strategic allocation decisions to minimize the costs of poor-quality pairings when faced with a genetically incompatible partner.

Carotenoid-based epaulettes reveal male competitive ability: experiments with resident and floater red-shouldered widowbirds

Many birds display carotenoid-based ornaments, which are typically considered to be honest indicators of individual health and condition. Experimental work on male red-shouldered widowbirds, Euplectes axillaris, has demonstrated a function of the carotenoid-based epaulettes in male contests and territory acquisition. Using two experiments, we investigated whether the natural variation in this colour signal reveals male competitive ability. Males with larger and redder (more longwave) epaulettes established territories to the exclusion of males with smaller and less red signals, which formed a large population of ‘floaters’. In an experiment in which we removed 42 resident males, these floaters rapidly filled up vacant territories. Among removed birds held in captivity, residents strongly dominated floaters in dyadic contests over access to an easily monopolized feeder (i.e. outside the context of territory defence). Only epaulette size predicted the outcome of these male contests. In addition, when competitors were experimentally given similar epaulette signals (removed or painted red to the average population size), the males were involved in more aggressive interactions than during unmanipulated contests, but residents continued to outcompete floaters. On release (after 8 days) to the breeding grounds, most residents (88%) rapidly reclaimed their territories from replacements. Combined, these results suggest that some intrinsic ‘resource-holding potential’, associated with the variation in epaulette signal, is primarily responsible for residents dominating nonresidents.  2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.

Low level of extrapair parentage in wild Zebra Finches

The captive zebra finch, Taeniopygia guttata, has become one of the key vertebrate model systems for studying a range of behavioural, physiological and neurological phenomena. In particular, this species has played a key role in developing our understanding of sexual selection and sperm competition. In contrast with the large number of studies using domesticated zebra finches, relatively few studies have focused on free-living populations of wild zebra finches. Investigating the incidence of extrapair paternity in zebra finches in the Australian desert, we found a very low level; 1.7% of 316 offspring from four of 80 broods fathered outside the pair bond. These numbers contrast with the high levels of extrapair paternity observed in domesticated aviary populations, and suggest a low level of sperm competition and sexual selection in natural populations. Our finding of such a low rate of extrapair paternity in the wild zebra finch suggests that it is one of the most genetically monogamous of all passerine species and that has important implications for future studies of this model organism in studies of sexual selection and reproductive biology. In addition, we found that 5.4% of 316 offspring were not related to either putative parent and hatched from eggs that had been dumped by intraspecific brood parasites.

Pronounced within-individual plasticity in sperm morphometry across social environments

Sperm morphometry (i.e., size and shape) and function are important determinants of male reproductive success and are thought to be under stabilizing selection. However, recent studies suggest that sperm morphometry can be a phenotypically plastic trait, which can be adjusted to varying conditions. We tested whether different behavioral strategies in aggression between aggressive red and nonaggressive black males of the color polymorphic Gouldian finch (Erythrura gouldiae) can influence sperm morphometry. We show pronounced within‐individual phenotypic plasticity in sperm morphometry of male Gouldian finches in three different social environments. Both red and black males placed in intermediate to high competitive environments (high frequency of red males) increased the relative length of their sperm midpiece. By contrast, red males placed in low to intermediate competitive environments (higher frequency of black males) increased the length of the sperm flagellum. Significant changes in stress and sex steroid hormone levels (in response to the competitive environment) appear to influence sperm traits in red but not in black males, suggesting that changes in hormonal levels are not solely responsible for the observed changes in sperm morphometry. These findings imply that males can adjust sperm morphometry across social environments.