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The Possible Role of the Uropygial Gland on Mate Choice in Domestic Chicken

The Possible Role of the Uropygial Gland on Mate Choice in Domestic Chicken Hindawi Publishing Corporation International Journal of Zoology Volume 2011, Article ID 860801, 5 pages doi:10.1155/2011/860801 Review Article The Possible Role of the Uropygial Gland on Mate Choice in Domestic Chicken Atsushi Hirao Division of Anatomy & Embryology, Department of Anatomy, School of Medicine, Jichi Medical University, Shimotsuke, Tochigi 329-0498, Japan Correspondence should be addressed to Atsushi Hirao, jhirao@jichi.ac.jp Received 30 January 2011; Accepted 14 May 2011 Academic Editor: Hynek Burda Copyright © 2011 Atsushi Hirao. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. In avian mating systems, male domestic fowls are polygamous and mate with a number of selected members of the opposite sex. The factors that influence mating preference are considered to be visual cues. However, several studies have indicated that chemosensory cues also affect socio-sexual behavior, including mate choice and individual recognition. The female uropygial gland appears to provide odor for mate choice, as uropygial gland secretions are specific to individual body odor. Chicken olfactory bulbs possess efferent projections to the nucleus taeniae that are involved in copulatory behavior. From various reports, it appears that the uropygial gland has the potential to act as the source of social odor cues that dictate mate choice. In this review, evidence for the possible role of the uropygial gland on mate choice in domestic chickens is presented. However, it remains unclear whether a relationship exists between the uropygial gland and major histocompatibility complex-dependent mate choice. 1. Introduction shown by members of one sex, which leads to them being more likely to mate with certain members of the opposite sex Nearly all mammals emit chemical substances into their than with others [14]. surroundings and these substances have important effects The three aims of this review are to present the factors on mating behavior. For example, male house mice (Mus that evoke mate choice in domestic chickens, examine the musculus) scent mark with urine to attract females for possible role of the chicken uropygial gland as a source mating. Additionally, female mice are able to distinguish of social odor cues, and discuss whether uropygial gland between the odors of parasitized and unparasitized males and secretions affect MHC-dependent mate choice. are attracted to the odor of the latter [1–3]. It appears the odors that these mating preferences evoke can be attributed 2. What Signals Elicit Mate Choice in to the major histocompatibility complex (MHC) [4]. Domestic Chickens? In contrast to mammals, and as avian species have often been classified as anosmic or microsmatic [5–9], olfactory Mating behavior in domestic chickens has been described information is generally not considered to be involved in the in detail by previous investigators [15]. Prior to mating, a mating behavior of birds. However, several investigators have series of courtship displays take place before mating based on suggested that chemical cues, such as individual recognition a stimulus-response sequence initiated by males (Figure 1). and mate choice, affect avian social behavior [5–8, 10, 11]. Furthermore, several researchers have provided supporting In addition, the Blue Tit (Cyanistes caeruleus L.) can detect evidence that domestic fowls exhibit non-random mating chemical secretions of predators and exhibit antipredatory [16–18]. behavior to reduce the risk of predation [12]. More recently, it has been reported that the female chicken (Gallus gallus In domestic fowls, vision appears to play a central role in domesticus) uropygial gland is related to male mate choice mating behavior [19, 20]. As the size of sexual ornaments, [13]. Mate choice is defined as any pattern of behavior, such as combs, wattles, and spurs are under the control of 2 International Journal of Zoology Male Male Female Male Female Female (a) (b) (c) Figure 1: Photographs of sexual behavior exhibited by domestic chickens. (a) Courtship waltzing, (b) mounting, and (c) copulation. testosterone [21], these ornaments are regarded as signals in the escape from predators [37]. Taken together, these affecting mate choice.Zuk et al.[22] and Johnsen and Zuk reports suggest that volatile compounds in uropygial gland [23] suggested that longer, redder combs in male red jungle secretions act as chemical cues, and may reflect the social fowls (Gallus gallus) were preferred by females of the species. status of birds. Graves et al. [24] also reported that male chickens having In the case of domestic chickens, uropygial gland secre- lager combs were selected more often by female birds. A tions rarely contain waxes [28], which are fundamental to recent study on male wattles reported that male wattle size waterproofing and maintaining the flexibility of feathers significantly reduces orienting latency in tidbitting display [28]. This finding suggests that the secretions possess another [25]. From these reports, the comb and wattle size of male function besides waterproofing. Indeed, the red jungle fowl chickens and red jungle fowls appears to act as a dominant emits an individual body odor that is produced by aliphatic signal influencing mate selection by female birds. carboxylic acids [38]. Moreover, trained mice are able On the other hand, there is little evidence that chemical to discriminate between these odors at the level of the signals are involved in mate choice in domestic chickens. individual [38]. Based on this evidence, chicken uropygial Recently, however, it has been further suggested that the gland secretions have the potential to function as social odor female uropygial gland provides an olfactory cue mediating cues. mate choice. For instance, male domestic chickens mate significantly more with female birds possessing uropygial 4. Utilization of Olfactory Cues for Mating glands than with uropygial-glandectomized females [13]. Systems in Domestic Chicken Additionally, this mate preference disappeared in males subjected to olfactory sensory deprivation [13]. Thus, to In contrast to previous works on avian olfactory function, investigate secretions from the uropygial gland as the source electrophysiological studies have provided evidence that of odor cues merits further study. domestic fowls are indeed capable of perceiving odor cues. For example, chicken olfactory bulbs respond to odor stimuli [39, 40]. In addition, an in situ hybridization study 3. Is the Chicken Uropygial Gland a Source of revealed that a number of olfactory receptor genes have Social Odor? been characterized in the olfactory epithelium [41]. Recently, Avian species with scent glands that emit strong odors are a second class within the odorant receptor family, termed rarely observed. Thus, it is generally considered that birds do trace amine-associated receptors (TAARs), was identified. not use chemical information in mating behavior. However, Certain mouse TAARs are able to perceive volatile amines birds possess the relatively large uropygial gland at the base present in urine, and one TAAR was found that recognizes of their tail feathers (Figure 2)[9, 26–28] which produces a a pheromone compound [42, 43]. From these results, it is large amount of volatile and nonvolatile compounds in the suggested that one function of TAARs involves the detection form of a waxy fluid that is spread on feathers as a part of social cues [42, 43]. Moreover, database searches have of plumage maintenance [9, 26–28]. Furthermore, volatile revealed that domestic chickens possess three functional compounds in uropygial gland secretions exhibit seasonal TAAR genes [44], and a protein sequence of chicken TAARs changes [29–32]. A few recent studies have suggested that has also been determined [45]. More recently, Gomez and gland secretions include socio-ecological information, which Celii [46] have established a culture method of olfactory allows distinction of species, gender, and even individuals sensory neurons, which is a powerful tool for in vitro studies [33, 34]. Moreover, several reports have shown that volatile aimed at understanding olfactory perception in domestic compounds in uropygial gland secretions are responsible for chickens. odors with specific functions [32, 35, 36]. For example, the Olfactory bulbs of domestic chickens are innervated by gland secretions of some birds contain volatile compounds efferent fibers [47] and possess similar projection sites to that contribute to an unpleasant odor emitted to aid that of other birds [48–50]. Moreover, chicken olfactory International Journal of Zoology 3 (a) (b) Figure 2: Photographs of the domestic chicken uropygial gland. (a) Lateral and (b) dorsal view of an adult uropygial gland. l: lobe, p: papilla. Scale bars indicate 1 cm. bulbs project to the nucleus taeniae [47]. In Japanese degradation [28]. These findings are supported by a study quail (Coturnix japonica), a lesion of this nucleus causes a that demonstrated that chicken uropygial gland secretions significant reduction in the frequency of copulation [51]. reduce the levels of these microorganisms on feathers Based on these findings, domestic chickens appear to possess [69]. Taken together, these reports suggest that chemical functional olfactory systems that influence mating behavior. defenses provided by the uropygial gland may reflect the Behavioral investigations have also demonstrated that status of disease-resistance. It is assumed that uropygial domestic chickens react to various olfactory stimuli [52]. It gland secretions contain MHC proteins. Unfortunately, this seems that chemical information plays an important role for possibility has not been explored. The issue should be their life. However, the direct evidence that domestic chicken examined to understand MHC-dependent mate choice in might use chemosensory cues to assess mating behavior is domestic chickens. rarely reported. In other birds, such as mallard ducks (Anas platyrhynchos), bilateral olfactory nerve sectioning signifi- 6. Conclusions and Future Work cantly reduced the number of social and mating behavior [53]. In Japanese quail, bilateral nostril sealing decreased the It is known that male domestic chickens prefer to mate number of mating behavior [6, 54]. To understand the role with certain members of the opposite sex, with previous of olfaction in mating behavior, it is at least necessary to workssuggesting thatvisualcuesplayacentralrolein perform similar experiments in domestic chickens. mating behavior. Undoubtedly, domestic chickens depend predominantly on visual information to function, while olfaction appears to play a role in their life. Chemical cues 5. Is MHC-Dependent Mate Choice in Chickens from the uropygial gland may compensate for information Mediated by the Uropygial Gland? that vision is not able to detect. In mice, MHC-based mate selection is proposed to involve Finally, future investigations on the uropygial gland the detection of male odors by females that leads to mating and mate choice in domestic chickens should consider two with males carrying dissimilar MHC genes, and results important issues. Firstly, although MHC genes heavily affect in progeny with disease-resistance genes [55–60]. In avian mate choice [4] in mammals through olfaction, it remains species, although a few investigators have suggested that unclear whether uropygial gland secretions contain MHC mate choice might be affected by olfaction [32, 61, 62], proteins. Resolving this issue is necessary to understand mate there is little evidence for the direct relation between MHC- choice in domestic chickens. Secondly, the localization of dependent mate choice and the uropygial gland. olfactory receptors which are able to perceive social odor cues However, recent studies suggest the possibility that MHC has not been examined. For instance, mouse V2 receptors genes are related to mate choice in birds. According to are able to perceive odor substances in urine and therefore research of outbred populations, house sparrows (Passer play an important role in MHC-dependent mate choice [4]. domesticus) appear to exhibit MHC-based mate choice To determine the localization of such olfactory receptors [63]. Moreover, female house sparrows seem to utilize in domestic chickens, it is first necessary to elucidate the olfactory cues for MHC-dependent mating preference [64]. mechanisms of perceiving social odor. Male red jungle fowls show several cryptic preferences by allocating additional sperm to MHC-dissimilar females [65]. 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The Possible Role of the Uropygial Gland on Mate Choice in Domestic Chicken

International Journal of Zoology , Volume 2011 – Jul 7, 2011

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Abstract

Hindawi Publishing Corporation International Journal of Zoology Volume 2011, Article ID 860801, 5 pages doi:10.1155/2011/860801 Review Article The Possible Role of the Uropygial Gland on Mate Choice in Domestic Chicken Atsushi Hirao Division of Anatomy & Embryology, Department of Anatomy, School of Medicine, Jichi Medical University, Shimotsuke, Tochigi 329-0498, Japan Correspondence should be addressed to Atsushi Hirao, jhirao@jichi.ac.jp Received 30 January 2011; Accepted 14 May 2011 Academic Editor: Hynek Burda Copyright © 2011 Atsushi Hirao. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. In avian mating systems, male domestic fowls are polygamous and mate with a number of selected members of the opposite sex. The factors that influence mating preference are considered to be visual cues. However, several studies have indicated that chemosensory cues also affect socio-sexual behavior, including mate choice and individual recognition. The female uropygial gland appears to provide odor for mate choice, as uropygial gland secretions are specific to individual body odor. Chicken olfactory bulbs possess efferent projections to the nucleus taeniae that are involved in copulatory behavior. From various reports, it appears that the uropygial gland has the potential to act as the source of social odor cues that dictate mate choice. In this review, evidence for the possible role of the uropygial gland on mate choice in domestic chickens is presented. However, it remains unclear whether a relationship exists between the uropygial gland and major histocompatibility complex-dependent mate choice. 1. Introduction shown by members of one sex, which leads to them being more likely to mate with certain members of the opposite sex Nearly all mammals emit chemical substances into their than with others [14]. surroundings and these substances have important effects The three aims of this review are to present the factors on mating behavior. For example, male house mice (Mus that evoke mate choice in domestic chickens, examine the musculus) scent mark with urine to attract females for possible role of the chicken uropygial gland as a source mating. Additionally, female mice are able to distinguish of social odor cues, and discuss whether uropygial gland between the odors of parasitized and unparasitized males and secretions affect MHC-dependent mate choice. are attracted to the odor of the latter [1–3]. It appears the odors that these mating preferences evoke can be attributed 2. What Signals Elicit Mate Choice in to the major histocompatibility complex (MHC) [4]. Domestic Chickens? In contrast to mammals, and as avian species have often been classified as anosmic or microsmatic [5–9], olfactory Mating behavior in domestic chickens has been described information is generally not considered to be involved in the in detail by previous investigators [15]. Prior to mating, a mating behavior of birds. However, several investigators have series of courtship displays take place before mating based on suggested that chemical cues, such as individual recognition a stimulus-response sequence initiated by males (Figure 1). and mate choice, affect avian social behavior [5–8, 10, 11]. Furthermore, several researchers have provided supporting In addition, the Blue Tit (Cyanistes caeruleus L.) can detect evidence that domestic fowls exhibit non-random mating chemical secretions of predators and exhibit antipredatory [16–18]. behavior to reduce the risk of predation [12]. More recently, it has been reported that the female chicken (Gallus gallus In domestic fowls, vision appears to play a central role in domesticus) uropygial gland is related to male mate choice mating behavior [19, 20]. As the size of sexual ornaments, [13]. Mate choice is defined as any pattern of behavior, such as combs, wattles, and spurs are under the control of 2 International Journal of Zoology Male Male Female Male Female Female (a) (b) (c) Figure 1: Photographs of sexual behavior exhibited by domestic chickens. (a) Courtship waltzing, (b) mounting, and (c) copulation. testosterone [21], these ornaments are regarded as signals in the escape from predators [37]. Taken together, these affecting mate choice.Zuk et al.[22] and Johnsen and Zuk reports suggest that volatile compounds in uropygial gland [23] suggested that longer, redder combs in male red jungle secretions act as chemical cues, and may reflect the social fowls (Gallus gallus) were preferred by females of the species. status of birds. Graves et al. [24] also reported that male chickens having In the case of domestic chickens, uropygial gland secre- lager combs were selected more often by female birds. A tions rarely contain waxes [28], which are fundamental to recent study on male wattles reported that male wattle size waterproofing and maintaining the flexibility of feathers significantly reduces orienting latency in tidbitting display [28]. This finding suggests that the secretions possess another [25]. From these reports, the comb and wattle size of male function besides waterproofing. Indeed, the red jungle fowl chickens and red jungle fowls appears to act as a dominant emits an individual body odor that is produced by aliphatic signal influencing mate selection by female birds. carboxylic acids [38]. Moreover, trained mice are able On the other hand, there is little evidence that chemical to discriminate between these odors at the level of the signals are involved in mate choice in domestic chickens. individual [38]. Based on this evidence, chicken uropygial Recently, however, it has been further suggested that the gland secretions have the potential to function as social odor female uropygial gland provides an olfactory cue mediating cues. mate choice. For instance, male domestic chickens mate significantly more with female birds possessing uropygial 4. Utilization of Olfactory Cues for Mating glands than with uropygial-glandectomized females [13]. Systems in Domestic Chicken Additionally, this mate preference disappeared in males subjected to olfactory sensory deprivation [13]. Thus, to In contrast to previous works on avian olfactory function, investigate secretions from the uropygial gland as the source electrophysiological studies have provided evidence that of odor cues merits further study. domestic fowls are indeed capable of perceiving odor cues. For example, chicken olfactory bulbs respond to odor stimuli [39, 40]. In addition, an in situ hybridization study 3. Is the Chicken Uropygial Gland a Source of revealed that a number of olfactory receptor genes have Social Odor? been characterized in the olfactory epithelium [41]. Recently, Avian species with scent glands that emit strong odors are a second class within the odorant receptor family, termed rarely observed. Thus, it is generally considered that birds do trace amine-associated receptors (TAARs), was identified. not use chemical information in mating behavior. However, Certain mouse TAARs are able to perceive volatile amines birds possess the relatively large uropygial gland at the base present in urine, and one TAAR was found that recognizes of their tail feathers (Figure 2)[9, 26–28] which produces a a pheromone compound [42, 43]. From these results, it is large amount of volatile and nonvolatile compounds in the suggested that one function of TAARs involves the detection form of a waxy fluid that is spread on feathers as a part of social cues [42, 43]. Moreover, database searches have of plumage maintenance [9, 26–28]. Furthermore, volatile revealed that domestic chickens possess three functional compounds in uropygial gland secretions exhibit seasonal TAAR genes [44], and a protein sequence of chicken TAARs changes [29–32]. A few recent studies have suggested that has also been determined [45]. More recently, Gomez and gland secretions include socio-ecological information, which Celii [46] have established a culture method of olfactory allows distinction of species, gender, and even individuals sensory neurons, which is a powerful tool for in vitro studies [33, 34]. Moreover, several reports have shown that volatile aimed at understanding olfactory perception in domestic compounds in uropygial gland secretions are responsible for chickens. odors with specific functions [32, 35, 36]. For example, the Olfactory bulbs of domestic chickens are innervated by gland secretions of some birds contain volatile compounds efferent fibers [47] and possess similar projection sites to that contribute to an unpleasant odor emitted to aid that of other birds [48–50]. Moreover, chicken olfactory International Journal of Zoology 3 (a) (b) Figure 2: Photographs of the domestic chicken uropygial gland. (a) Lateral and (b) dorsal view of an adult uropygial gland. l: lobe, p: papilla. Scale bars indicate 1 cm. bulbs project to the nucleus taeniae [47]. In Japanese degradation [28]. These findings are supported by a study quail (Coturnix japonica), a lesion of this nucleus causes a that demonstrated that chicken uropygial gland secretions significant reduction in the frequency of copulation [51]. reduce the levels of these microorganisms on feathers Based on these findings, domestic chickens appear to possess [69]. Taken together, these reports suggest that chemical functional olfactory systems that influence mating behavior. defenses provided by the uropygial gland may reflect the Behavioral investigations have also demonstrated that status of disease-resistance. It is assumed that uropygial domestic chickens react to various olfactory stimuli [52]. It gland secretions contain MHC proteins. Unfortunately, this seems that chemical information plays an important role for possibility has not been explored. The issue should be their life. However, the direct evidence that domestic chicken examined to understand MHC-dependent mate choice in might use chemosensory cues to assess mating behavior is domestic chickens. rarely reported. In other birds, such as mallard ducks (Anas platyrhynchos), bilateral olfactory nerve sectioning signifi- 6. Conclusions and Future Work cantly reduced the number of social and mating behavior [53]. In Japanese quail, bilateral nostril sealing decreased the It is known that male domestic chickens prefer to mate number of mating behavior [6, 54]. To understand the role with certain members of the opposite sex, with previous of olfaction in mating behavior, it is at least necessary to workssuggesting thatvisualcuesplayacentralrolein perform similar experiments in domestic chickens. mating behavior. Undoubtedly, domestic chickens depend predominantly on visual information to function, while olfaction appears to play a role in their life. Chemical cues 5. Is MHC-Dependent Mate Choice in Chickens from the uropygial gland may compensate for information Mediated by the Uropygial Gland? that vision is not able to detect. In mice, MHC-based mate selection is proposed to involve Finally, future investigations on the uropygial gland the detection of male odors by females that leads to mating and mate choice in domestic chickens should consider two with males carrying dissimilar MHC genes, and results important issues. Firstly, although MHC genes heavily affect in progeny with disease-resistance genes [55–60]. In avian mate choice [4] in mammals through olfaction, it remains species, although a few investigators have suggested that unclear whether uropygial gland secretions contain MHC mate choice might be affected by olfaction [32, 61, 62], proteins. Resolving this issue is necessary to understand mate there is little evidence for the direct relation between MHC- choice in domestic chickens. Secondly, the localization of dependent mate choice and the uropygial gland. olfactory receptors which are able to perceive social odor cues However, recent studies suggest the possibility that MHC has not been examined. For instance, mouse V2 receptors genes are related to mate choice in birds. According to are able to perceive odor substances in urine and therefore research of outbred populations, house sparrows (Passer play an important role in MHC-dependent mate choice [4]. domesticus) appear to exhibit MHC-based mate choice To determine the localization of such olfactory receptors [63]. Moreover, female house sparrows seem to utilize in domestic chickens, it is first necessary to elucidate the olfactory cues for MHC-dependent mating preference [64]. mechanisms of perceiving social odor. Male red jungle fowls show several cryptic preferences by allocating additional sperm to MHC-dissimilar females [65]. 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