- Email: [email protected]
Genetic variation in maternal yolk testosterone allocation predicts female mating decisions in Japanese quail
Animal Behaviour 157 (2019) 35e42
Contents lists available at ScienceDirect
Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav
Genetic variation in maternal yolk testosterone allocation predicts female mating decisions in Japanese quail Daniela Ledecka a, Michal Zeman a, b, Monika Okuliarova b, * a b
Institute of Animal Biochemistry and Genetics, Centre of Biosciences, Slovak Academy of Sciences, Bratislava, Slovakia Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakia
a r t i c l e i n f o Article history: Received 22 January 2019 Initial acceptance 2 April 2019 Final acceptance 29 July 2019 MS number 19-00057R Keywords: mate choice maternal investment plasticity reproduction yolk androgens
Maternal reproductive effort can be adjusted through the transfer of hormones into the eggs, where they influence embryo development, mediating short- and long-term maternal effects on offspring phenotype. While studies usually explore how females can increase their reproductive success through an allocation of yolk testosterone (T) under external environmental variability, it is less clear whether intrinsically driven interfemale differences in yolk T deposition may themselves predict female reproductive decisions. In our study, we used Japanese quail, Coturnix japonica, lines divergently selected for high (HET) and low (LET) egg T concentrations to examine whether this genetic variation in yolk T levels is linked to female mating decisions. First, we analysed line differences in male-typical reproductive behaviour and how this behavioural response is affected by female line identity. Males were tested with females from the same (match pairs) and opposite (cross pairs) lines. Next, female mate preferences were evaluated in a two-choice test in which females were allowed to choose between males from the same and opposite lines. We found no line differences in male copulatory behaviour. Interestingly, a shorter latency to copulate and a higher number of copulations were recorded in LET males when they were mated with HET than LET females. No differences between match and cross pairs were found in HET males. In the two-choice test, LET females displayed a preference for males from the same over the opposite line, but HET females did not discriminate between LET and HET males. Collectively, these results demonstrate that genetically high yolk T deposition is related to higher receptivity and reduced choosiness in female mate preferences in Japanese quail. Moreover, our results indicate an important link between maternal investment, reproductive physiology and female mating decisions, pointing out evolutionary implications and a role of variation in female mate choice in sexual selection. © 2019 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Female mate choice is a powerful mechanism, which promotes sexual selection and can be reflected in overall reproductive success (Andersson & Simmons, 2006). Females are expected to obtain direct (e.g. quality of paternal care) or indirect (e.g. genetic quality of offspring) benefits if they pair with preferred or highly attractive males (Jennions & Petrie, 1997). Moreover, in order to maximize reproductive success, females can adjust their maternal investment in response to the phenotypic traits of the mated males , Nakagawa, & Uller, 2012). Maternal reproductive (Horv athova effort can be adjusted in different ways, among which the adjustment in maternal hormones is often considered. Maternal hormones represent an important signalling pathway through which
* Correspondence: M. Okuliarova, Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University, Ilkovi cova 6, 841 04, Bratislava, Slovakia. E-mail address: [email protected] (M. Okuliarova).
early developmental stages may be shaped in response to the variability of the internal and external conditions experienced by the mother (Meylan, Miles, & Clobert, 2012). In birds, maternal hormones are transferred into the eggs, where they contribute to the embryonic milieu and can influence embryo development (Schwabl, 1996). Most research has focused on maternal yolk androgens, especially testosterone (T) and its short- and long-term effects on within-sex variability in the morphological, physiological and behavioural traits of offspring (Ruuskanen, 2015; von Engelhardt & Groothuis, 2011). Avian females show considerable plasticity in their yolk T deposition in response to a number of environmental and social stimuli (Bentz, Becker, & Navara, 2016; Guibert et al., 2010; Okuliarova, Sarnikova, Rettenbacher, Skrobanek, & Zeman, 2010). For example, an adjustment in yolk androgen deposition has been demonstrated for various morphological and behavioural characteristics of male phenotype associated with male attractiveness. In
https://doi.org/10.1016/j.anbehav.2019.08.022 0003-3472/© 2019 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
36
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42
these studies, females laid eggs with increased concentrations of yolk androgens if they mated with more colourful males (Safran, Pilz, McGraw, Correa, & Schwabl, 2008), watched males that displayed at a high rate (Loyau & Lacroix, 2010) or mated males showing high syllable repetitiveness in their songs (Kristofik et al., 2014). However, other studies have reported no or even a negative link between yolk T allocation and measures of male attractiveness pez-Rull & Gil, 2009; Mazuc, Chastel, & Sorci, 2003; Navara, Hill, (Lo & Mendonça, 2006) suggesting context- or species-specific costs and benefits of increased yolk T levels to females and offspring et al., 2012). This inconsistency in studies might also (Horv athova be explained by actual female mate preferences which may not always correspond with experimentally evaluated male attractiveness. Indeed, when female grey partridges, Perdix perdix, were allowed to mate with their preferred males they laid eggs with higher T concentrations (Garcia-Fernandez et al., 2010). Besides exogenous stimuli, interfemale differences in yolk T levels are for the most part caused by the intrinsic quality of females and heritable genetic variance (Egbert, Jackson, Rodgers, & nek, & Zeman, Schwabl, 2013; Okuliarova, Groothuis, Skrob a 2011). While many studies have explored how females can increase their reproductive success through the allocation of yolk T in response to the external environment, it is less clear whether intrinsically driven interfemale differences in yolk T deposition may themselves predict the reproductive decision making of females. The physiological link can be explained by the common underlying neuroendocrine mechanisms since variation in both yolk T transfer and mating decisions have been shown to involve changes in the reproductive hormones controlling the reproductive physiology and behaviour of females (Hirschenhauser, 2012; Lynch, Crews, Ryan, & Wilczynski, 2006; Okuliarova, Meddle, & Zeman, 2018). Females are not uniform in their mating preferences and this can arise from both genetic and nongenetic factors (Jennions & Petrie, 1997; Riebel, Holveck, Verhulst, & Fawcett, 2010). Recent studies imply that environmentally and intrinsically driven variation in the phenotypic traits and behaviour of females is an even more relevant determinant of mate choice decision than the trait variation of the chosen mate (Ah-King & Gowaty, 2016). In birds, interfemale variability ranging from choosy to indiscriminate behaviour has been related, for example, to female condition (Griggio & Hoi, 2010; Riebel, Naguib, & Gil, 2009), previous experiences (Campbell & Hauber, 2009), population density (Palokangas, Alatalo, & Korpim€ aki, 1992) and personality (Schuett, Godin, & Dall, 2011). Our study aimed to examine whether intrinsically driven interfemale differences in yolk T deposition are linked with female mating decisions. We used Japanese quail, Coturnix japonica, lines that were divergently selected for egg T concentrations and, as a result, exhibited a more than two-fold difference in the yolk T content between high (HET) and low (LET) egg T lines (Okuliarova, Groothuis, et al., 2011; Okuliarova, Kankova, Skrobanek, & Zeman, 2014). Our previous studies showed that quail from the HET line grew faster, without having a compromised innate immune response, than quail from the opposite LET line (Kankova, Zeman, & Okuliarova, 2012; Okuliarova, Kostal, & Zeman, 2011). Moreover, we found changed neuroendocrine mechanisms controlling reproduction in adult females, since HET quail showed a higher preovulatory peak of luteinizing hormone (LH) levels than females from the LET line (Okuliarova et al., 2018). In the present study, we first examined line differences in male-typical reproductive behaviour to evaluate phenotypic variation in a trait on which females can base their mate choice. Moreover, since female quail may significantly control the male copulatory response (Domjan, Mahometa, & Mills, 2003) we examined whether female line identity can influence male mating behaviour. To analyse the contribution of females, males were tested with females from the
same (match pairs) and the opposite line (cross pairs). In the second experiment, female mate preferences were evaluated in a twochoice test in which females were allowed to choose between males from the same and the opposite line. We predicted that females would display preferences between LET and HET males if there is sufficient phenotypic variation in a trait on which females base their mate choice. We expected that females would prefer males of the same line and match pairs would show a higher frequency of mating behaviour than cross pairs, since birds experienced only contact with conspecifics from the same line during the rearing and housing periods. On the other hand, if female mate preferences deviated from this expected pattern, interfemale variation in yolk T allocation may be considered as a predictor of female mating decisions. This hypothesis can be supported by common neuroendocrine mechanisms, controlling sex hormone biosynthesis, that are expected to be involved in both yolk T allocation and mate choice behaviour. Moreover, it suggests an important correlational link between maternal investment, reproductive physiology and female mating decisions, which will help us better understand the evolution of sexual selection. METHODS Animals and Housing Two lines of Japanese quail selected for contrasting yolk T concentrations were used in the study. Birds were bred and kept at the Institute of Animal Biochemistry and Genetics (IABG), the Slovak Academy of Sciences, Bratislava. The initial population of quail and the selection procedure are described in detail in previous papers (Okuliarova, Groothuis, et al., 2011; Okuliarova et al., 2014). From the age of 6 weeks, adult birds were housed in wire cages (in accordance with Directive 2010/63/EU of the European Parliament) in groups of one male and two females from the same line under a light:dark cycle of 14:10 h (lights on at 0600 hours) at a controlled temperature of 22 ± 1 C. Food (mash for laying hens) and water were available ad libitum. Ethical Note Quail were reared in an approved breeding facility of the IABG with the licence number SK PC 7010 Np. Animal care and the experiments were carried out in accordance with the laws and regulations of the Slovak Republic and approved by the Ethical Committee of the IABG and The State Veterinary and Food Administration of the Slovak Republic under the permit number Ro-2926/10-221. After the study the birds were retained as breeding stock and used to breed the next generation of Japanese quail lines selected for yolk T concentrations. Male Reproductive Behaviour Quail (12 animals per line and sex) were from the fourth generation of selection. They were tested at the age of 44 weeks. One day prior to the experiment, females were separated from males, and males remained individually in their home cages. All tests were performed in the same room in which the birds were housed to minimize stress from an unknown environment. Six standard home cages were used as the test cages and they were simultaneously monitored by a video camera. Each male was given two trials, one on each of 2 consecutive days. Males were tested with unfamiliar females from the same line (12 match pairs per line) in trial 1 and with unfamiliar females from the opposite line (12 cross pairs per line) in trial 2. The test procedure consisted of a 10 min acclimation period, during which the male was allowed to habituate to the test
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42
cage, and a 15 min recording period starting with the introduction of the female to the male. In Japanese quail, a male-typical sequence of copulatory behaviour involves chasing the female, grabbing the female's head or neck feathers, mounting the female's back with both feet and, if the male is successful, the sequence is terminated by cloacal contact movements (Mills, Crawford, Domjan, & Faure, 1997). Thus, after the female was put in the test cage, the following measures of male copulatory behaviour were quantified from videotapes: latency to chase, latency to copulate, number of copulations, duration of chasing that finished with copulation and duration of chasing that finished without copulation. Affiliative behaviour between the male and female was evaluated as proximity time, the time during which the male and female were together in the same quadrant of the test cage excluding time spent chasing. One pair from each line was excluded from behavioural analysis because the female had a deformed leg. Female Mate Choice Quail (10 animals per line and sex) were from the eighth generation of selection and they were tested at the age of 11 weeks. Quail from each line were raised separately in mixed-sex flocks of 20 birds until the age of 7 weeks. Thereafter, they were placed into breeding cages and housed in line-specific groups of two females and one male. The target males, used in the experiment, were placed into individual cages. Experimental birds were assigned to tetrads consisting of two focal females (one from each line) and two target males (one from each line). Thus, each female from the same tetrad had equivalent opportunity to choose between the same pair of target males. Tests were performed in a plastic white box (13040 cm and 40 cm high) with a transparent Plexiglas lid and front wall. The box was divided into three compartments by two transparent partitions: a middle compartment (80 cm) and two end compartments (25 cm), one containing an LET male and another containing an HET male. The middle compartment was divided into a central zone (20 cm) and two preference zones in front of each end compartment (30 cm). For the focal female, preference zones for the male from the same and opposite lines represented match and cross zones, respectively. The experimental procedure (Appendix Fig. A1) began when males from the same tetrad (one from each line) were put into the end compartments. Subsequently, the first focal female of the tetrad was placed into the central zone of the middle compartment and her behaviour was recorded for 10 min. The same procedure was repeated with the second focal female of the same tetrad. All focal females were given three trials within 6 days. The sides of the match and cross preference zones and the order in which females from the same tetrads were tested were changed between trials. We recorded the latency to leave the central zone and the time spent in the central, match and cross zones. The percentage of the time that was spent in either the match or the cross zone, corrected for the latency to leave the central zone, was calculated and averaged for the three trials. Two females from the HET line did not leave the central zone during all three trials and, therefore, were excluded from the analysis.
37
et al., 2018). Mean intra- and interassay coefficients of variation were lower than 15%. Assay sensitivity was 1.5 pg of T per tube. Data Analysis Statistical analyses were performed in STATISTICA 7.0 (StatSoft, Tulsa, OK, U.S.A.). All measures obtained from behavioural tests were checked for their normal distribution using the KolmogoroveSmirnov test. Line differences were analysed either by the Student t test or the ManneWhitney U test, depending on whether they met the condition of normality. Likewise, within-line differences between match and cross pairs were evaluated by the paired t test or the Wilcoxon matched-pairs test for normally and non-normally distributed data, respectively. RESULTS Male Reproductive Behaviour The comparison of LET and HET males did not reveal significant differences in the behavioural measures of copulatory behaviour for the match or cross pairs (ManneWhitney U tests: for all measures P > 0.1; Table 1, Fig. 1). Similarly, total number of copulations, which males obtained in both match and cross pairs, did not differ between lines (median and interquartile range for LET and HET males: 1 (1.5) versus 2 (2.5); ManneWhitney U tests: U ¼ 46, N1 ] N2 ¼ 11, P ¼ 0.365). However, males from the LET line had a significantly shorter latency to copulate (Wilcoxon test: T ¼ 0, N ¼ 11, P < 0.05; Fig. 1a) and a higher number of copulations (Wilcoxon test: T ¼ 0, N ¼ 11, P < 0.05; Fig. 1b) when they were mated with HET than LET females, while there were no differences in the other recorded parameters (Table 1). In HET males, the latency to copulate (Wilcoxon test: T ¼ 14, N ¼ 11, P ¼ 0.575; Fig. 1a), number of copulations (Wilcoxon test: T ¼ 16.5, N ¼ 11, P ¼ 0.834; Fig. 1b) and other measures of copulatory behaviour (Table 1) did not differ between the match and cross pairs. Moreover, LET males tended to stay in the same quadrant longer if they were mated with HET than LET females (Wilcoxon test: T ¼ 14, N ¼ 11, P ¼ 0.091; Fig. 2), while HET males displayed no differences in proximity time between match and cross pairs (Wilcoxon test: T ¼ 23, N ¼ 11, P ¼ 0.374; Fig. 2). Female Mate Choice Females from the LET line preferred LET over HET males since they spent a significantly higher percentage of time in the match than the cross zone (paired t test: t9 ¼ 2.71, P < 0.05; Fig. 3a). In contrast, HET females did not show any preference between LET and HET males (paired t test: t7 ¼ -0.47, P ¼ 0.65; Fig. 3b). The percentage of time spent in the match zone did not differ between LET and HET females (t test: t16 ¼ 1.31, P ¼ 0.209), but the percentage of time spent in the cross zone tended to be lower in LET than HET females (t test: t16 ¼ -1.96, P ¼ 0.068; Fig. 3). No line differences were found in the latency to leave the central zone (mean ± SEM for LET and HET females: 290.3 ± 56.5 s versus 278.8 ± 60.5 s; t test: t16 ¼ 0.14, P ¼ 0.892).
Yolk Testosterone Assay
Yolk Testosterone Levels
Mean yolk T levels (based on two to three eggs collected per quail) were calculated for the LET and HET females included in the study to demonstrate that the lines differed in their yolk T deposition. Testosterone concentrations were analysed in the yolk after ether extraction by radioimmunoassay, according to a previously published protocol (Okuliarova, Groothuis, et al., 2011; Okuliarova
Females from the HET line laid eggs with significantly higher yolk T concentrations than those from the LET line. In females participating in the male copulatory behaviour test, mean (±SEM) yolk T levels were 8.4 ± 0.6 pg/mg and 17.8 ± 1.4 pg/mg yolk for the LET and HET quail, respectively (t test: t22 ¼ -6.19, P < 0.001). In the females used to analyse mate choice behaviour, mean yolk T levels
38
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42
Table 1 Behavioural measures of copulatory behaviour in male Japanese quail from low (LET, N ¼ 11) and high egg testosterone (HET, N ¼ 11) lines mated with females from the same (match) and opposite (cross) line LET males
Latency to chase (s) Chasing that finished with copulation (s) Chasing that finished without copulation (s)
Match vs Crossa
HET males
Match
Cross
Match
Cross
LET
HET
900 (865.5) 0 (0) 0 (106)
51 (462.5) 7 (15) 25 (37.5)
67 (169) 0 (11) 13 (43)
12 (128.5) 0 (22) 10 (18)
T¼8 P¼0.161 T¼5 P¼0.128 T¼15 P¼0.674
T¼17 P¼0.285 T¼15.5 P¼0.726 T¼17 P¼0.889
Data are given as medians and interquartile ranges in parentheses. a Results of Wilcoxon tests used to compare match and cross pairs for LET and HET males.
were 10.8 ± 0.8 pg/mg and 19.7 ± 2.5 pg/mg for the LET and HET quail, respectively (t test: t16 ¼ -3.81, P < 0.01). DISCUSSION Female reproductive decisions are usually influenced by many variables in order to maximize reproductive success. Here, we used two lines of Japanese quail divergently selected for low and high
Latency to copulate (s)
1100 (a)
*
880
660
440
220
0 LET
egg T levels to investigate whether intrinsically driven interfemale differences in yolk T deposition are linked with female mating decisions. Our results showed two interesting findings. First, when LET males were mated with HET females, they had a shorter latency to copulate and a higher number of copulations than in match pairs with LET females. Second, LET females showed a preference for males from the same line over the opposite line, but HET females did not discriminate between LET and HET males. Copulatory behaviour did not differ between LET and HET males, regardless of whether males were mated with females from the same or opposite line. In Japanese quail, it is well documented that sex differences in male-typical copulatory behaviour are determined by an organizational action of sex steroids during the sensitive period of embryonic development. Endogenously produced oestrogens demasculinize the brain of female embryos and, as a result, adult females never perform male-typical copulatory behaviour, even if their circulating T levels are experimentally increased (Balthazart, Cornil, Charlier, Taziaux, & Ball, 2008). Our results showed that sexual differentiation of the consummatory aspects of reproductive behaviour was not influenced by either a correlated response to selection for contrasting yolk T concentrations or yolk T-mediated maternal effects. In line with our results, studies using an injection of exogenous T into the egg found no effects of elevated yolk T levels on male-typical copulatory behaviour in Chinese quail, Coturnix chinensis (Uller, Eklof, &
HET
4 (b)
P = 0.091
3
Proximity time (s)
No. of copulations
600
* 2
1
450
300
150
0
0 LET
HET Match
Cross
Figure 1. (a) Latency to copulate and (b) number of copulations in male Japanese quail from low (LET, N ¼ 11) and high egg testosterone (HET, N ¼ 11) lines mated with females from the same (match) and opposite (cross) line. Data are given as box plots with medians (thick lines), lower and upper quartiles (box) and the highest and the lowest values within 1.5 interquartile range (whiskers). Dots represent individual data points in the group. *P < 0.05.
LET
HET Match
Cross
Figure 2. Time spent in proximity to the female by male Japanese quail from low (LET, N ¼ 11) and high egg testosterone (HET, N ¼ 11) lines mated with females from the same (match) and opposite (cross) line. Data are given as box plots with medians (thick lines), lower and upper quartiles (box) and the highest and the lowest values within 1.5 interquartile range (whiskers). Dots represent individual data points in the group.
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42
(a)
39
(b)
% Time in preference zone
* 100
100
75
75
50
50
25
25
0
0 Match
Cross
Match
Cross
Figure 3. Percentage of time spent in either match (close to the male from the same line) or cross (close to the male from the opposite line) zones by female Japanese quail from (a) low (LET, N ¼ 10) and (b) high egg testosterone (HET, N ¼ 8) lines. Data are given as means ± SEM. Dots represent individual data points in the group. *P < 0.05.
Andersson, 2005), as well as in Japanese quail (Schweitzer, Goldstein, Place, & Adkins-Regan, 2013). Conversely, in ringnecked pheasants, Phasianus colchicus, males hatched from Tinjected eggs obtained more copulations than control males, specifically with control females (Bonisoli-Alquati et al., 2011). Moreover, pair formation in rock pigeons, Columba livia, was changed from a random combination by in ovo T treatment, indicating that yolk T may promote disassortative pairing (Hsu, Dijkstra, & Groothuis, 2016). Interestingly, we recorded a shorter latency to copulate and a higher number of copulations in LET males when they were mated with HET compared to LET females. In contrast, HET males did not show any differences in copulatory behaviour when they were mated with females from the same or opposite line. These results demonstrate the importance of the female's contribution to copulatory interactions, as has been shown in many other species (Gowaty, 1994), including Japanese quail (Domjan et al., 2003). Female quail may control the copulatory response of males through the behavioural mechanism related to the duration of their immobility in the presence of the male (Domjan et al., 2003). This mechanism can also account for our results since we found a tendency towards higher affiliative behaviour between LET males and HET females than in pairs of LET males and LET females. Therefore, our results suggest that a genetically high deposition of T into the yolk can be associated with the higher receptivity of females. In quail, hormonal control of female sexual receptivity (especially squatting behaviour) is executed by oestrogens (Ball & Balthazart, 2009; Delville & Balthazart, 1987). Indeed, the current results are consistent with our previous findings, which demonstrated higher plasma oestradiol concentrations in HET than LET females (Okuliarova et al., 2014). Moreover, in Japanese quail, an increase in the female's receptivity may positively predict fertilization success (Domjan et al., 2003), indicating a reproductive benefit for females with a high yolk T deposition.
Female receptivity to males usually varies along with female mate preference (Jennions & Petrie, 1997). In Japanese quail, affiliative preferences have been demonstrated to predict the choice of a mate for copulation, as well as fertilization success (Persaud & Galef, 2005; White & Galef, 1999). In a two-choice test, we found that LET females displayed a preference for males from the same line, whereas HET females showed no preference between males from the same and opposite lines; in other words, HET females were less choosy. Generally, avian females select their prospective mates by plumage coloration and behavioural displays, which may signal male quality. However, in galliform species, ornate male plumage is probably not an accurate measure of male quality and females favour other phenotypic traits that signal male condition (Hagelin & Ligon, 2001). In the current study, we found no differences in the pattern of copulatory behaviour between LET and HET males but we cannot exclude line differences in other morphological or behavioural traits of male phenotype. In Japanese quail, social experiences have been shown to play a role in female mate preferences (Galef, 2008). Female quail display preferences for males they have seen mating with another female (Galef & White, 1998) or less aggressive males after observing aggressive interactions between males (Ophir & Galef, 2003). However, these effects were unlikely to influence mate choice behaviour in our study, since both males and females were unfamiliar and had not seen each other in mating or aggressive interactions with other partners. New insights from empirical and theoretical studies suggest that environmental circumstances and the intrinsic quality of the chooser sex are more likely to modify mating decisions than the phenotype of the chosen individual (Ah-King & Gowaty, 2016). Female mating preferences have been shown to vary in relation to both genetic and nongenetic factors, including female condition, previous experience or personality (Campbell & Hauber, 2009; Griggio & Hoi, 2010; Riebel et al., 2009; Schuett et al., 2011). In our study, females laying eggs with high yolk T levels were less
40
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42
discriminative in their mate preferences than females with comparable low yolk T deposition. Condition-dependent variation in female mate preferences predicts that females may experience different trade-offs between the costs and benefits of being more or less selective in their mate choice (Cotton, Small, & Pomiankowski, 2006). In general, female mate choice is considered to be a costly life history trait (Pomiankowski, 1987). Likewise, increased yolk T deposition may impose costs on the female in terms of a higher metabolic rate and a shorter life span (Tschirren et al., 2016; Tschirren, Postma, Gustafsson, Groothuis, & Doligez, 2014). Thus, we can expect that less discriminative mating behaviour in HET females may reflect the way in which they optimize costs for different life history traits. The benefits of choosing a particular mate may vary depending on the degree of relatedness between potential mates (Jennions & Petrie, 1997). To maintain an optimal balance between inbreeding and outbreeding, it is advantageous for females to choose males of intermediate relatedness (Bateson, 1982). In our study, both lines were reared separately in mixed-sex flocks, enabling early experiences with individuals from the same line, but not from the opposite line. Therefore, an adaptive explanation for reduced choosiness found in HET than LET females may reflect a strategy to minimize inbreeding risk and to increase genetic variability in HET offspring. Neuroendocrine mechanisms underlying variability in mating decisions are not yet well understood, although changes in the reproductive hormones controlling the reproductive physiology and behaviour of females are expected to be involved (Hirschenhauser, 2012; Lynch et al., 2006). In a study with darkeyed juncos, Junco hyemalis, females with experimentally increased plasma T levels showed reduced choosiness compared to control females (McGlothlin, Neudorf, Casto, Nolan, & Ketterson, 2004), indicating that T might play some role. However, our previous results demonstrated that selection for high yolk T levels did not result in permanently high T concentrations in the circulation of adult female Japanese quail, and we found no correlation between yolk and basal plasma T levels under constant conditions (Okuliarova, Groothuis, et al., 2011). Recently, we showed differences in the neuroendocrine control of the ovulatory cycle between LET and HET females (Okuliarova et al., 2018). Specifically, the preovulatory peak of LH was higher in HET than LET quail and these preovulatory LH levels correlated positively with increased preovulatory T concentrations in the plasma. Therefore, these results, together with our current study, suggest that the pattern of hormonal changes during the ovulatory cycle may provide a proximate mechanism for variation in female mate preferences. This is also consistent with results obtained in female túngara frogs, Physalaemus pustulosus, in which gonadotropin-induced hormonal changes near the time of ovulation were related to the highest receptivity to male cues and a decreased level of choosiness (Lynch et al., 2006). Since LET and HET females differ not only in their yolk T deposition but also in their exposure to yolk T levels during embryo development, we cannot exclude that such hormonemediated maternal effects may contribute to line differences in female mating decisions. Indeed, transgenerational epigenetic mechanisms have been shown to be involved in mate preference behaviour in rats, Rattus norvegicus, indicating an importance of this force in sexual selection (Crews et al., 2007). The effects of in ovo T treatment have been demonstrated in Japanese quail, in which males hatched from T-injected eggs displayed an affiliative preference towards familiar females, while control males did not have a preference between familiar and unfamiliar females (Schweitzer et al., 2013). In contrast, mate choice behaviour was not affected by the exposure to
elevated yolk T levels in female canaries, Serinus canaria (Vergauwen, Eens, & Muller, 2014). In conclusion, our results demonstrate an important link between maternal investment, reproductive physiology and female mating decisions in Japanese quail. Females from the genetic line with high yolk T levels displayed higher receptivity and were less choosy in their mate preferences than females from the opposite line with low T in their eggs. This correlative link may have several implications for the evolution of the variation in female mate preferences and for a role of this variation in sexual selection. Acknowledgments We thank two anonymous referees and the Editor Amanda Korstjens for their helpful comments on the manuscript. The study was supported by the Scientific Grant Agency of the Ministry of Education of the Slovak Republic VEGA 1/0686/15 and the Slovak Research and Development Agency APVV-17-0371. References Ah-King, M., & Gowaty, P. A. (2016). A conceptual review of mate choice: stochastic demography, within-sex phenotypic plasticity, and individual flexibility. Ecology and Evolution, 6(14), 4607e4642. https://doi.org/10.1002/ece3.2197. Andersson, M., & Simmons, L. W. (2006). Sexual selection and mate choice. Trends in Ecology and Evolution, 21(6), 296e302. https://doi.org/10.1016/j.tree.2006.03. 015. Ball, G. F., & Balthazart, J. (2009). Neuroendocrine regulation of reproductive behavior in birds. In D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrbach, & R. T. Rubin (Eds.), Hormones, Brain and Behavior (2nd ed., pp. 855e897). San Diego, CA: Academic Press. Balthazart, J., Cornil, C. A., Charlier, T. D., Taziaux, M., & Ball, G. F. (2008). Estradiol, a key endocrine signal in the sexual differentiation and activation of reproductive behavior in quail. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 311A(5), 323e345. https://doi.org/10.1002/jez.464. Bateson, P. (1982). Preferences for cousins in Japanese quail. Nature, 295, 236. https://doi.org/10.1038/295236a0. Bentz, A. B., Becker, D. J., & Navara, K. J. (2016). Evolutionary implications of interspecific variation in a maternal effect: A meta-analysis of yolk testosterone response to competition. Royal Society Open Science, 3(11), 160499. https://doi. org/10.1098/rsos.160499. Bonisoli-Alquati, A., Matteo, A., Ambrosini, R., Rubolini, D., Romano, M., Caprioli, M., et al. (2011). Effects of egg testosterone on female mate choice and male sexual behavior in the pheasant. Hormones and Behavior, 59(1), 75e82. https://doi.org/ 10.1016/j.yhbeh.2010.10.013. Campbell, D. L. M., & Hauber, M. E. (2009). Cross-fostering diminishes song discrimination in zebra finches (Taeniopygia guttata). Animal Cognition, 12(3), 481e490. https://doi.org/10.1007/s10071-008-0209-5. Cotton, S., Small, J., & Pomiankowski, A. (2006). Sexual selection and conditiondependent mate preferences. Current Biology, 16(17), R755eR765. https://doi. org/10.1016/j.cub.2006.08.022. Crews, D., Gore, A. C., Hsu, T. S., Dangleben, N. L., Spinetta, M., Schallert, T., et al. (2007). Transgenerational epigenetic imprints on mate preference. Proceedings of the National Academy of Sciences, 104(14), 5942e5946. https://doi.org/10. 1073/pnas.0610410104. Delville, Y., & Balthazart, J. (1987). Hormonal control of female sexual behavior in the Japanese quail. Hormones and Behavior, 21(3), 288e309. https://doi.org/10. 1016/0018-506X(87)90016-X. Domjan, M., Mahometa, M. J., & Mills, A. D. (2003). Relative contributions of the male and the female to sexual behavior and reproductive success in the Japanese quail (Coturnix japonica). Journal of Comparative Psychology, 117(4), 391e399. https://doi.org/10.1037/0735-7036.117.4.391. Egbert, J. R., Jackson, M. F., Rodgers, B. D., & Schwabl, H. (2013). Between-female variation in house sparrow yolk testosterone concentration is negatively associated with CYP19A1 (aromatase) mRNA expression in ovarian follicles. General and Comparative Endocrinology, 183, 53e62. https://doi.org/10.1016/j.ygcen. 2012.12.001. von Engelhardt, N., & Groothuis, T. G. G. (2011). Chapter 4 e Maternal hormones in avian eggs. In D. O. Norris, & K. H. Lopez (Eds.), Hormones and Reproduction of Vertebrates, Vol. 4: Birds (pp. 91e127). London, U.K.: Academic Press. Galef, B. G., Jr. (2008). Social influences on the mate choices of male and female Japanese quail. Comparative Cognition and Behavior Reviews, 3, 1e12. https://dx. doi.org/10.3819/ccbr.2008.30001. Galef, B. G., Jr., & White, D. J. (1998). Mate-choice copying in Japanese quail, Coturnix coturnix japonica. Animal Behaviour, 55(3), 545e552. https://doi.org/10.1006/ anbe.1997.0616. Garcia-Fernandez, V., Guasco, B., Tanvez, A., Lacroix, A., Cucco, M., Leboucher, G., et al. (2010). Influence of mating preferences on yolk testosterone in the grey
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42 partridge. Animal Behaviour, 80(1), 45e49. https://doi.org/10.1016/j.anbehav. 2010.03.023. Gowaty, P. A. (1994). Architects of sperm competition. Trends in Ecology and Evolution, 9(5), 160e162. https://doi.org/10.1016/0169-5347(94)90076-0. Griggio, M., & Hoi, H. (2010). Only females in poor condition display a clear preference and prefer males with an average badge. BMC Evolutionary Biology, 10(1), 261. https://doi.org/10.1186/1471-2148-10-261. Guibert, F., Richard-Yris, M. A., Lumineau, S., Kotrschal, K., Guemene, D., Bertin, A., et al. (2010). Social instability in laying quail: consequences on yolk steroids and offspring's phenotype. PLoS One, 5(11), e14069. https://doi.org/10.1371/journal. pone.0014069. Hagelin, J. C., & Ligon, J. D. (2001). Female quail prefer testosterone-mediated traits, rather than the ornate plumage of males. Animal Behaviour, 61(2), 465e476. https://doi.org/10.1006/anbe.2000.1618. Hirschenhauser, K. (2012). Testosterone and partner compatibility: evidence and emerging questions. Ethology, 118(9), 799e811. https://doi.org/10.1111/j.14390310.2012.02087.x. thov Horva a, T., Nakagawa, S., & Uller, T. (2012). Strategic female reproductive investment in response to male attractiveness in birds. Proceedings of the Royal Society B: Biological Sciences, 279(1726), 163e170. https://doi.org/10.1098/rspb. 2011.0663. Hsu, B.-Y., Dijkstra, C., & Groothuis, T. G. (2016). No escape from mother's will: effects of maternal testosterone on offspring reproductive behaviour far into adulthood. Animal Behaviour, 117, 135e144. https://doi.org/10.1016/j.anbehav. 2016.05.004. Jennions, M.,D., & Petrie, M. (1997). Variation in mate choice and mating preferences: a review of causes and consequences. Biological Reviews, 72(2), 283e327. https://doi.org/10.1111/j.1469-185X.1997.tb00015.x. Kankova, Z., Zeman, M., & Okuliarova, M. (2012). Growth and innate immunity are not limited by selection for high egg testosterone content in Japanese quail. Journal of Experimental Biology, 215(4), 617e622. https://doi.org/10.1242/Jeb. 064030. Kristofik, J., Darolova, A., Majtan, J., Okuliarova, M., Zeman, M., & Hoi, H. (2014). Do females invest more into eggs when males sing more attractively? Postmating sexual selection strategies in a monogamous reed passerine. Ecology and Evolution, 4(8), 1328e1339. https://doi.org/10.1002/ece3.1034. pez-Rull, I., & Gil, D. (2009). Do female spotless starlings Sturnus unicolor adjust Lo maternal investment according to male attractiveness? Journal of Avian Biology, 40(3), 254e262. https://dx.doi.org/10.1111/j.1600-048X.2009.04553.x. Loyau, A., & Lacroix, F. (2010). Watching sexy displays improves hatching success and offspring growth through maternal allocation. Proceedings of the Royal Society B: Biological Sciences, 277(1699), 3453e3460. https://doi.org/10.1098/ rspb.2010.0473. Lynch, K. S., Crews, D., Ryan, M. J., & Wilczynski, W. (2006). Hormonal state influences aspects of female mate choice in the Túngara Frog (Physalaemus pustulosus). Hormones and Behavior, 49(4), 450e457. https://doi.org/10.1016/j. yhbeh.2005.10.001. Mazuc, J., Chastel, O., & Sorci, G. (2003). No evidence for differential maternal allocation to offspring in the house sparrow (Passer domesticus). Behavioral Ecology, 14(3), 340e346. https://doi.org/10.1093/beheco/14.3.340. McGlothlin, J. W., Neudorf, D. L. H., Casto, J. M., Nolan, V., & Ketterson, E. D. (2004). Elevated testosterone reduces choosiness in female darkeeyed juncos (Junco hyemalis): evidence for a hormonal constraint on sexual selection? Proceedings of the Royal Society B: Biological Sciences, 271(1546), 1377e1384. https://doi.org/ 10.1098/rspb.2004.2741. Meylan, S., Miles, D. B., & Clobert, J. (2012). Hormonally mediated maternal effects, individual strategy and global change. Philosophical Transactions of the Royal Society B: Biological Sciences, 367(1596), 1647e1664. https://doi.org/10.1098/ rstb.2012.0020. Mills, A. D., Crawford, L. L., Domjan, M., & Faure, J. M. (1997). The behavior of the Japanese or domestic quail Coturnix japonica. Neuroscience and Biobehavioral Reviews, 21(3), 261e281. https://doi.org/10.1016/S0149-7634(96)00028-0. Navara, K. J., Hill, G. E., & Mendonça, M. T. (2006). Yolk androgen deposition as a compensatory strategy. Behavioral Ecology and Sociobiology, 60(3), 392e398. https://doi.org/10.1007/s00265-006-0177-1. nek, P., & Zeman, M. (2011). Experimental Okuliarova, M., Groothuis, T. G. G., Skrob a evidence for genetic heritability of maternal hormone transfer to offspring. American Naturalist, 177(6), 824e834. https://doi.org/10.1086/659996. Okuliarova, M., Kankova, Z., Skrobanek, P., & Zeman, M. (2014). Bidirectional selection for yolk testosterone content in Japanese quail. Avian Biology Research, 7(1), 18e24. https://doi.org/10.3184/175815514X13903210973681.
41
Okuliarova, M., Kostal, L., & Zeman, M. (2011). Effects of divergent selection for yolk testosterone content on growth characteristics of Japanese quail. Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology, 160(1), 81e86. https://doi.org/10.1016/j.cbpa.2011.05.012. Okuliarova, M., Meddle, S. L., & Zeman, M. (2018). Egg deposition of maternal testosterone is primarily controlled by the preovulatory peak of luteinizing hormone in Japanese quail. General and Comparative Endocrinology, 256, 23e29. https://doi.org/10.1016/j.ygcen.2017.05.004. Okuliarova, M., Sarnikova, B., Rettenbacher, S., Skrobanek, P., & Zeman, M. (2010). Yolk testosterone and corticosterone in hierarchical follicles and laid eggs of Japanese quail exposed to long-term restraint stress. General and Comparative Endocrinology, 165(1), 91e96. https://doi.org/10.1016/j.ygcen.2009.06.007. Ophir, A. G., & Galef, B. G. (2003). Female Japanese quail that ‘eavesdrop’ on fighting males prefer losers to winners. Animal Behaviour, 66(2), 399e407. https://doi. org/10.1006/anbe.2003.2230. Palokangas, P., Alatalo, R. V., & Korpim€ aki, E. (1992). Female choice in the kestrel under different availability of mating options. Animal Behaviour, 43(4), 659e665. https://doi.org/10.1016/S0003-3472(05)81024-3. Persaud, K. N., & Galef, B. G. (2005). Eggs of a female Japanese quail are more likely to be fertilized by a male that she prefers. Journal of Comparative Psychology, 119(3), 251e256. https://doi.org/10.1037/0735-7036.119.3.251. Pomiankowski, A. (1987). The costs of choice in sexual selection. Journal of Theoretical Biology, 128(2), 195e218. https://doi.org/10.1016/S0022-5193(87)801698. Riebel, K., Holveck, M.-J., Verhulst, S., & Fawcett, T. (2010). Are high-quality mates always attractive? State-dependent mate preferences in birds and humans. Communicative & Integrative Biology, 3(3), 271e273. https://doi.org/10.4161/cib. 3.3.11557. Riebel, K., Naguib, M., & Gil, D. (2009). Experimental manipulation of the rearing environment influences adult female zebra finch song preferences. Animal Behaviour, 78(6), 1397e1404. https://doi.org/10.1016/j.anbehav.2009.09.011. Ruuskanen, S. (2015). Hormonally-mediated maternal effects in birds: Lessons from the flycatcher model system. General and Comparative Endocrinology, 224, 283e293. https://doi.org/10.1016/j.ygcen.2015.09.016. Safran, R. J., Pilz, K. M., McGraw, K. J., Correa, S. M., & Schwabl, H. (2008). Are yolk androgens and carotenoids in barn swallow eggs related to parental quality? Behavioral Ecology and Sociobiology, 62(3), 427e438. https://doi.org/10.1007/ s00265-007-0470-7. Schuett, W., Godin, J.-G. J., & Dall, S. R. X. (2011). Do female zebra finches, Taeniopygia guttata, choose their mates based on their ‘personality’? Ethology, 117(10), 908e917. https://doi.org/10.1111/j.1439-0310.2011.01945.x. Schwabl, H. (1996). Maternal testosterone in the avian egg enhances postnatal growth. Comparative Biochemistry and Physiology a-Physiology, 114(3), 271e276. https://doi.org/10.1016/0300-9629(96)00009-6. Schweitzer, C., Goldstein, M. H., Place, N. J., & Adkins-Regan, E. (2013). Long-lasting and sex-specific consequences of elevated egg yolk testosterone for social behavior in Japanese quail. Hormones and Behavior, 63(1), 80e87. https://doi. org/10.1016/j.yhbeh.2012.10.011. Tschirren, B., Postma, E., Gustafsson, L., Groothuis, T. G. G., & Doligez, B. (2014). Natural selection acts in opposite ways on correlated hormonal mediators of prenatal maternal effects in a wild bird population. Ecology Letters, 17(10), 1310e1315. https://doi.org/10.1111/Ele.12339. Tschirren, B., Ziegler, A. K., Canale, C. I., Okuliarova, M., Zeman, M., & Giraudeau, M. (2016). High yolk testosterone transfer is associated with an increased female metabolic rate. Physiological and Biochemical Zoology, 89(5), 448e452. https:// doi.org/10.1086/687571. Uller, T., Eklof, J., & Andersson, S. (2005). Female egg investment in relation to male sexual traits and the potential for transgenerational effects in sexual selection. Behavioral Ecology and Sociobiology, 57(6), 584e590. https://doi.org/10.1007/ s00265-004-0886-2. Vergauwen, J., Eens, M., & Muller, W. (2014). Consequences of experimentally elevated yolk testosterone levels for intra- and inter-sexual selection in canaries. Behavioral Ecology and Sociobiology, 68(8), 1299e1309. https://doi.org/ 10.1007/s00265-014-1740-9. White, D. J., & Galef, B. G., Jr. (1999). Affiliative preferences are stable and predict mate choices in both sexes of Japanese quail, Coturnix japonica. Animal Behaviour, 58(4), 865e871. https://doi.org/10.1006/anbe.1999.1210.
42
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42
Appendix
(a)
(b)
40 cm LET
LET
Match zone 25 cm
30 cm
Central zone 20 cm
HET
Cross zone
LET
Cross zone
40 cm
30 cm
HET
Central zone
HET
Match zone
25 cm
(c)
(days)
Trial 1
Trial 2
Trial 3
d1
d2
d6
Figure A1. Experimental design of female mate choice test in Japanese quail lines divergently selected for low (LET) and high (HET) egg testosterone levels. Quails were assigned to tetrads consisting of two focal females (one from each line) and two target males (one from each line). For the focal female, preference zones for the male from the same and opposite lines represented match and cross zones, respectively. A trial began when males from the same tetrad (one from each line) were put into the end compartments. Subsequently, (a) the first focal female of the tetrad was placed into the central zone and her behaviour was recorded for 10 min. Next, this female was removed and (b) the second focal female of the same tetrad was placed into the central zone and her behaviour was recorded for another 10 min. (c) All focal females were given three trials within 6 days. See Methods for further details.
Contents lists available at ScienceDirect
Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav
Genetic variation in maternal yolk testosterone allocation predicts female mating decisions in Japanese quail Daniela Ledecka a, Michal Zeman a, b, Monika Okuliarova b, * a b
Institute of Animal Biochemistry and Genetics, Centre of Biosciences, Slovak Academy of Sciences, Bratislava, Slovakia Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakia
a r t i c l e i n f o Article history: Received 22 January 2019 Initial acceptance 2 April 2019 Final acceptance 29 July 2019 MS number 19-00057R Keywords: mate choice maternal investment plasticity reproduction yolk androgens
Maternal reproductive effort can be adjusted through the transfer of hormones into the eggs, where they influence embryo development, mediating short- and long-term maternal effects on offspring phenotype. While studies usually explore how females can increase their reproductive success through an allocation of yolk testosterone (T) under external environmental variability, it is less clear whether intrinsically driven interfemale differences in yolk T deposition may themselves predict female reproductive decisions. In our study, we used Japanese quail, Coturnix japonica, lines divergently selected for high (HET) and low (LET) egg T concentrations to examine whether this genetic variation in yolk T levels is linked to female mating decisions. First, we analysed line differences in male-typical reproductive behaviour and how this behavioural response is affected by female line identity. Males were tested with females from the same (match pairs) and opposite (cross pairs) lines. Next, female mate preferences were evaluated in a two-choice test in which females were allowed to choose between males from the same and opposite lines. We found no line differences in male copulatory behaviour. Interestingly, a shorter latency to copulate and a higher number of copulations were recorded in LET males when they were mated with HET than LET females. No differences between match and cross pairs were found in HET males. In the two-choice test, LET females displayed a preference for males from the same over the opposite line, but HET females did not discriminate between LET and HET males. Collectively, these results demonstrate that genetically high yolk T deposition is related to higher receptivity and reduced choosiness in female mate preferences in Japanese quail. Moreover, our results indicate an important link between maternal investment, reproductive physiology and female mating decisions, pointing out evolutionary implications and a role of variation in female mate choice in sexual selection. © 2019 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Female mate choice is a powerful mechanism, which promotes sexual selection and can be reflected in overall reproductive success (Andersson & Simmons, 2006). Females are expected to obtain direct (e.g. quality of paternal care) or indirect (e.g. genetic quality of offspring) benefits if they pair with preferred or highly attractive males (Jennions & Petrie, 1997). Moreover, in order to maximize reproductive success, females can adjust their maternal investment in response to the phenotypic traits of the mated males , Nakagawa, & Uller, 2012). Maternal reproductive (Horv athova effort can be adjusted in different ways, among which the adjustment in maternal hormones is often considered. Maternal hormones represent an important signalling pathway through which
* Correspondence: M. Okuliarova, Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University, Ilkovi cova 6, 841 04, Bratislava, Slovakia. E-mail address: [email protected] (M. Okuliarova).
early developmental stages may be shaped in response to the variability of the internal and external conditions experienced by the mother (Meylan, Miles, & Clobert, 2012). In birds, maternal hormones are transferred into the eggs, where they contribute to the embryonic milieu and can influence embryo development (Schwabl, 1996). Most research has focused on maternal yolk androgens, especially testosterone (T) and its short- and long-term effects on within-sex variability in the morphological, physiological and behavioural traits of offspring (Ruuskanen, 2015; von Engelhardt & Groothuis, 2011). Avian females show considerable plasticity in their yolk T deposition in response to a number of environmental and social stimuli (Bentz, Becker, & Navara, 2016; Guibert et al., 2010; Okuliarova, Sarnikova, Rettenbacher, Skrobanek, & Zeman, 2010). For example, an adjustment in yolk androgen deposition has been demonstrated for various morphological and behavioural characteristics of male phenotype associated with male attractiveness. In
https://doi.org/10.1016/j.anbehav.2019.08.022 0003-3472/© 2019 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
36
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42
these studies, females laid eggs with increased concentrations of yolk androgens if they mated with more colourful males (Safran, Pilz, McGraw, Correa, & Schwabl, 2008), watched males that displayed at a high rate (Loyau & Lacroix, 2010) or mated males showing high syllable repetitiveness in their songs (Kristofik et al., 2014). However, other studies have reported no or even a negative link between yolk T allocation and measures of male attractiveness pez-Rull & Gil, 2009; Mazuc, Chastel, & Sorci, 2003; Navara, Hill, (Lo & Mendonça, 2006) suggesting context- or species-specific costs and benefits of increased yolk T levels to females and offspring et al., 2012). This inconsistency in studies might also (Horv athova be explained by actual female mate preferences which may not always correspond with experimentally evaluated male attractiveness. Indeed, when female grey partridges, Perdix perdix, were allowed to mate with their preferred males they laid eggs with higher T concentrations (Garcia-Fernandez et al., 2010). Besides exogenous stimuli, interfemale differences in yolk T levels are for the most part caused by the intrinsic quality of females and heritable genetic variance (Egbert, Jackson, Rodgers, & nek, & Zeman, Schwabl, 2013; Okuliarova, Groothuis, Skrob a 2011). While many studies have explored how females can increase their reproductive success through the allocation of yolk T in response to the external environment, it is less clear whether intrinsically driven interfemale differences in yolk T deposition may themselves predict the reproductive decision making of females. The physiological link can be explained by the common underlying neuroendocrine mechanisms since variation in both yolk T transfer and mating decisions have been shown to involve changes in the reproductive hormones controlling the reproductive physiology and behaviour of females (Hirschenhauser, 2012; Lynch, Crews, Ryan, & Wilczynski, 2006; Okuliarova, Meddle, & Zeman, 2018). Females are not uniform in their mating preferences and this can arise from both genetic and nongenetic factors (Jennions & Petrie, 1997; Riebel, Holveck, Verhulst, & Fawcett, 2010). Recent studies imply that environmentally and intrinsically driven variation in the phenotypic traits and behaviour of females is an even more relevant determinant of mate choice decision than the trait variation of the chosen mate (Ah-King & Gowaty, 2016). In birds, interfemale variability ranging from choosy to indiscriminate behaviour has been related, for example, to female condition (Griggio & Hoi, 2010; Riebel, Naguib, & Gil, 2009), previous experiences (Campbell & Hauber, 2009), population density (Palokangas, Alatalo, & Korpim€ aki, 1992) and personality (Schuett, Godin, & Dall, 2011). Our study aimed to examine whether intrinsically driven interfemale differences in yolk T deposition are linked with female mating decisions. We used Japanese quail, Coturnix japonica, lines that were divergently selected for egg T concentrations and, as a result, exhibited a more than two-fold difference in the yolk T content between high (HET) and low (LET) egg T lines (Okuliarova, Groothuis, et al., 2011; Okuliarova, Kankova, Skrobanek, & Zeman, 2014). Our previous studies showed that quail from the HET line grew faster, without having a compromised innate immune response, than quail from the opposite LET line (Kankova, Zeman, & Okuliarova, 2012; Okuliarova, Kostal, & Zeman, 2011). Moreover, we found changed neuroendocrine mechanisms controlling reproduction in adult females, since HET quail showed a higher preovulatory peak of luteinizing hormone (LH) levels than females from the LET line (Okuliarova et al., 2018). In the present study, we first examined line differences in male-typical reproductive behaviour to evaluate phenotypic variation in a trait on which females can base their mate choice. Moreover, since female quail may significantly control the male copulatory response (Domjan, Mahometa, & Mills, 2003) we examined whether female line identity can influence male mating behaviour. To analyse the contribution of females, males were tested with females from the
same (match pairs) and the opposite line (cross pairs). In the second experiment, female mate preferences were evaluated in a twochoice test in which females were allowed to choose between males from the same and the opposite line. We predicted that females would display preferences between LET and HET males if there is sufficient phenotypic variation in a trait on which females base their mate choice. We expected that females would prefer males of the same line and match pairs would show a higher frequency of mating behaviour than cross pairs, since birds experienced only contact with conspecifics from the same line during the rearing and housing periods. On the other hand, if female mate preferences deviated from this expected pattern, interfemale variation in yolk T allocation may be considered as a predictor of female mating decisions. This hypothesis can be supported by common neuroendocrine mechanisms, controlling sex hormone biosynthesis, that are expected to be involved in both yolk T allocation and mate choice behaviour. Moreover, it suggests an important correlational link between maternal investment, reproductive physiology and female mating decisions, which will help us better understand the evolution of sexual selection. METHODS Animals and Housing Two lines of Japanese quail selected for contrasting yolk T concentrations were used in the study. Birds were bred and kept at the Institute of Animal Biochemistry and Genetics (IABG), the Slovak Academy of Sciences, Bratislava. The initial population of quail and the selection procedure are described in detail in previous papers (Okuliarova, Groothuis, et al., 2011; Okuliarova et al., 2014). From the age of 6 weeks, adult birds were housed in wire cages (in accordance with Directive 2010/63/EU of the European Parliament) in groups of one male and two females from the same line under a light:dark cycle of 14:10 h (lights on at 0600 hours) at a controlled temperature of 22 ± 1 C. Food (mash for laying hens) and water were available ad libitum. Ethical Note Quail were reared in an approved breeding facility of the IABG with the licence number SK PC 7010 Np. Animal care and the experiments were carried out in accordance with the laws and regulations of the Slovak Republic and approved by the Ethical Committee of the IABG and The State Veterinary and Food Administration of the Slovak Republic under the permit number Ro-2926/10-221. After the study the birds were retained as breeding stock and used to breed the next generation of Japanese quail lines selected for yolk T concentrations. Male Reproductive Behaviour Quail (12 animals per line and sex) were from the fourth generation of selection. They were tested at the age of 44 weeks. One day prior to the experiment, females were separated from males, and males remained individually in their home cages. All tests were performed in the same room in which the birds were housed to minimize stress from an unknown environment. Six standard home cages were used as the test cages and they were simultaneously monitored by a video camera. Each male was given two trials, one on each of 2 consecutive days. Males were tested with unfamiliar females from the same line (12 match pairs per line) in trial 1 and with unfamiliar females from the opposite line (12 cross pairs per line) in trial 2. The test procedure consisted of a 10 min acclimation period, during which the male was allowed to habituate to the test
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42
cage, and a 15 min recording period starting with the introduction of the female to the male. In Japanese quail, a male-typical sequence of copulatory behaviour involves chasing the female, grabbing the female's head or neck feathers, mounting the female's back with both feet and, if the male is successful, the sequence is terminated by cloacal contact movements (Mills, Crawford, Domjan, & Faure, 1997). Thus, after the female was put in the test cage, the following measures of male copulatory behaviour were quantified from videotapes: latency to chase, latency to copulate, number of copulations, duration of chasing that finished with copulation and duration of chasing that finished without copulation. Affiliative behaviour between the male and female was evaluated as proximity time, the time during which the male and female were together in the same quadrant of the test cage excluding time spent chasing. One pair from each line was excluded from behavioural analysis because the female had a deformed leg. Female Mate Choice Quail (10 animals per line and sex) were from the eighth generation of selection and they were tested at the age of 11 weeks. Quail from each line were raised separately in mixed-sex flocks of 20 birds until the age of 7 weeks. Thereafter, they were placed into breeding cages and housed in line-specific groups of two females and one male. The target males, used in the experiment, were placed into individual cages. Experimental birds were assigned to tetrads consisting of two focal females (one from each line) and two target males (one from each line). Thus, each female from the same tetrad had equivalent opportunity to choose between the same pair of target males. Tests were performed in a plastic white box (13040 cm and 40 cm high) with a transparent Plexiglas lid and front wall. The box was divided into three compartments by two transparent partitions: a middle compartment (80 cm) and two end compartments (25 cm), one containing an LET male and another containing an HET male. The middle compartment was divided into a central zone (20 cm) and two preference zones in front of each end compartment (30 cm). For the focal female, preference zones for the male from the same and opposite lines represented match and cross zones, respectively. The experimental procedure (Appendix Fig. A1) began when males from the same tetrad (one from each line) were put into the end compartments. Subsequently, the first focal female of the tetrad was placed into the central zone of the middle compartment and her behaviour was recorded for 10 min. The same procedure was repeated with the second focal female of the same tetrad. All focal females were given three trials within 6 days. The sides of the match and cross preference zones and the order in which females from the same tetrads were tested were changed between trials. We recorded the latency to leave the central zone and the time spent in the central, match and cross zones. The percentage of the time that was spent in either the match or the cross zone, corrected for the latency to leave the central zone, was calculated and averaged for the three trials. Two females from the HET line did not leave the central zone during all three trials and, therefore, were excluded from the analysis.
37
et al., 2018). Mean intra- and interassay coefficients of variation were lower than 15%. Assay sensitivity was 1.5 pg of T per tube. Data Analysis Statistical analyses were performed in STATISTICA 7.0 (StatSoft, Tulsa, OK, U.S.A.). All measures obtained from behavioural tests were checked for their normal distribution using the KolmogoroveSmirnov test. Line differences were analysed either by the Student t test or the ManneWhitney U test, depending on whether they met the condition of normality. Likewise, within-line differences between match and cross pairs were evaluated by the paired t test or the Wilcoxon matched-pairs test for normally and non-normally distributed data, respectively. RESULTS Male Reproductive Behaviour The comparison of LET and HET males did not reveal significant differences in the behavioural measures of copulatory behaviour for the match or cross pairs (ManneWhitney U tests: for all measures P > 0.1; Table 1, Fig. 1). Similarly, total number of copulations, which males obtained in both match and cross pairs, did not differ between lines (median and interquartile range for LET and HET males: 1 (1.5) versus 2 (2.5); ManneWhitney U tests: U ¼ 46, N1 ] N2 ¼ 11, P ¼ 0.365). However, males from the LET line had a significantly shorter latency to copulate (Wilcoxon test: T ¼ 0, N ¼ 11, P < 0.05; Fig. 1a) and a higher number of copulations (Wilcoxon test: T ¼ 0, N ¼ 11, P < 0.05; Fig. 1b) when they were mated with HET than LET females, while there were no differences in the other recorded parameters (Table 1). In HET males, the latency to copulate (Wilcoxon test: T ¼ 14, N ¼ 11, P ¼ 0.575; Fig. 1a), number of copulations (Wilcoxon test: T ¼ 16.5, N ¼ 11, P ¼ 0.834; Fig. 1b) and other measures of copulatory behaviour (Table 1) did not differ between the match and cross pairs. Moreover, LET males tended to stay in the same quadrant longer if they were mated with HET than LET females (Wilcoxon test: T ¼ 14, N ¼ 11, P ¼ 0.091; Fig. 2), while HET males displayed no differences in proximity time between match and cross pairs (Wilcoxon test: T ¼ 23, N ¼ 11, P ¼ 0.374; Fig. 2). Female Mate Choice Females from the LET line preferred LET over HET males since they spent a significantly higher percentage of time in the match than the cross zone (paired t test: t9 ¼ 2.71, P < 0.05; Fig. 3a). In contrast, HET females did not show any preference between LET and HET males (paired t test: t7 ¼ -0.47, P ¼ 0.65; Fig. 3b). The percentage of time spent in the match zone did not differ between LET and HET females (t test: t16 ¼ 1.31, P ¼ 0.209), but the percentage of time spent in the cross zone tended to be lower in LET than HET females (t test: t16 ¼ -1.96, P ¼ 0.068; Fig. 3). No line differences were found in the latency to leave the central zone (mean ± SEM for LET and HET females: 290.3 ± 56.5 s versus 278.8 ± 60.5 s; t test: t16 ¼ 0.14, P ¼ 0.892).
Yolk Testosterone Assay
Yolk Testosterone Levels
Mean yolk T levels (based on two to three eggs collected per quail) were calculated for the LET and HET females included in the study to demonstrate that the lines differed in their yolk T deposition. Testosterone concentrations were analysed in the yolk after ether extraction by radioimmunoassay, according to a previously published protocol (Okuliarova, Groothuis, et al., 2011; Okuliarova
Females from the HET line laid eggs with significantly higher yolk T concentrations than those from the LET line. In females participating in the male copulatory behaviour test, mean (±SEM) yolk T levels were 8.4 ± 0.6 pg/mg and 17.8 ± 1.4 pg/mg yolk for the LET and HET quail, respectively (t test: t22 ¼ -6.19, P < 0.001). In the females used to analyse mate choice behaviour, mean yolk T levels
38
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42
Table 1 Behavioural measures of copulatory behaviour in male Japanese quail from low (LET, N ¼ 11) and high egg testosterone (HET, N ¼ 11) lines mated with females from the same (match) and opposite (cross) line LET males
Latency to chase (s) Chasing that finished with copulation (s) Chasing that finished without copulation (s)
Match vs Crossa
HET males
Match
Cross
Match
Cross
LET
HET
900 (865.5) 0 (0) 0 (106)
51 (462.5) 7 (15) 25 (37.5)
67 (169) 0 (11) 13 (43)
12 (128.5) 0 (22) 10 (18)
T¼8 P¼0.161 T¼5 P¼0.128 T¼15 P¼0.674
T¼17 P¼0.285 T¼15.5 P¼0.726 T¼17 P¼0.889
Data are given as medians and interquartile ranges in parentheses. a Results of Wilcoxon tests used to compare match and cross pairs for LET and HET males.
were 10.8 ± 0.8 pg/mg and 19.7 ± 2.5 pg/mg for the LET and HET quail, respectively (t test: t16 ¼ -3.81, P < 0.01). DISCUSSION Female reproductive decisions are usually influenced by many variables in order to maximize reproductive success. Here, we used two lines of Japanese quail divergently selected for low and high
Latency to copulate (s)
1100 (a)
*
880
660
440
220
0 LET
egg T levels to investigate whether intrinsically driven interfemale differences in yolk T deposition are linked with female mating decisions. Our results showed two interesting findings. First, when LET males were mated with HET females, they had a shorter latency to copulate and a higher number of copulations than in match pairs with LET females. Second, LET females showed a preference for males from the same line over the opposite line, but HET females did not discriminate between LET and HET males. Copulatory behaviour did not differ between LET and HET males, regardless of whether males were mated with females from the same or opposite line. In Japanese quail, it is well documented that sex differences in male-typical copulatory behaviour are determined by an organizational action of sex steroids during the sensitive period of embryonic development. Endogenously produced oestrogens demasculinize the brain of female embryos and, as a result, adult females never perform male-typical copulatory behaviour, even if their circulating T levels are experimentally increased (Balthazart, Cornil, Charlier, Taziaux, & Ball, 2008). Our results showed that sexual differentiation of the consummatory aspects of reproductive behaviour was not influenced by either a correlated response to selection for contrasting yolk T concentrations or yolk T-mediated maternal effects. In line with our results, studies using an injection of exogenous T into the egg found no effects of elevated yolk T levels on male-typical copulatory behaviour in Chinese quail, Coturnix chinensis (Uller, Eklof, &
HET
4 (b)
P = 0.091
3
Proximity time (s)
No. of copulations
600
* 2
1
450
300
150
0
0 LET
HET Match
Cross
Figure 1. (a) Latency to copulate and (b) number of copulations in male Japanese quail from low (LET, N ¼ 11) and high egg testosterone (HET, N ¼ 11) lines mated with females from the same (match) and opposite (cross) line. Data are given as box plots with medians (thick lines), lower and upper quartiles (box) and the highest and the lowest values within 1.5 interquartile range (whiskers). Dots represent individual data points in the group. *P < 0.05.
LET
HET Match
Cross
Figure 2. Time spent in proximity to the female by male Japanese quail from low (LET, N ¼ 11) and high egg testosterone (HET, N ¼ 11) lines mated with females from the same (match) and opposite (cross) line. Data are given as box plots with medians (thick lines), lower and upper quartiles (box) and the highest and the lowest values within 1.5 interquartile range (whiskers). Dots represent individual data points in the group.
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42
(a)
39
(b)
% Time in preference zone
* 100
100
75
75
50
50
25
25
0
0 Match
Cross
Match
Cross
Figure 3. Percentage of time spent in either match (close to the male from the same line) or cross (close to the male from the opposite line) zones by female Japanese quail from (a) low (LET, N ¼ 10) and (b) high egg testosterone (HET, N ¼ 8) lines. Data are given as means ± SEM. Dots represent individual data points in the group. *P < 0.05.
Andersson, 2005), as well as in Japanese quail (Schweitzer, Goldstein, Place, & Adkins-Regan, 2013). Conversely, in ringnecked pheasants, Phasianus colchicus, males hatched from Tinjected eggs obtained more copulations than control males, specifically with control females (Bonisoli-Alquati et al., 2011). Moreover, pair formation in rock pigeons, Columba livia, was changed from a random combination by in ovo T treatment, indicating that yolk T may promote disassortative pairing (Hsu, Dijkstra, & Groothuis, 2016). Interestingly, we recorded a shorter latency to copulate and a higher number of copulations in LET males when they were mated with HET compared to LET females. In contrast, HET males did not show any differences in copulatory behaviour when they were mated with females from the same or opposite line. These results demonstrate the importance of the female's contribution to copulatory interactions, as has been shown in many other species (Gowaty, 1994), including Japanese quail (Domjan et al., 2003). Female quail may control the copulatory response of males through the behavioural mechanism related to the duration of their immobility in the presence of the male (Domjan et al., 2003). This mechanism can also account for our results since we found a tendency towards higher affiliative behaviour between LET males and HET females than in pairs of LET males and LET females. Therefore, our results suggest that a genetically high deposition of T into the yolk can be associated with the higher receptivity of females. In quail, hormonal control of female sexual receptivity (especially squatting behaviour) is executed by oestrogens (Ball & Balthazart, 2009; Delville & Balthazart, 1987). Indeed, the current results are consistent with our previous findings, which demonstrated higher plasma oestradiol concentrations in HET than LET females (Okuliarova et al., 2014). Moreover, in Japanese quail, an increase in the female's receptivity may positively predict fertilization success (Domjan et al., 2003), indicating a reproductive benefit for females with a high yolk T deposition.
Female receptivity to males usually varies along with female mate preference (Jennions & Petrie, 1997). In Japanese quail, affiliative preferences have been demonstrated to predict the choice of a mate for copulation, as well as fertilization success (Persaud & Galef, 2005; White & Galef, 1999). In a two-choice test, we found that LET females displayed a preference for males from the same line, whereas HET females showed no preference between males from the same and opposite lines; in other words, HET females were less choosy. Generally, avian females select their prospective mates by plumage coloration and behavioural displays, which may signal male quality. However, in galliform species, ornate male plumage is probably not an accurate measure of male quality and females favour other phenotypic traits that signal male condition (Hagelin & Ligon, 2001). In the current study, we found no differences in the pattern of copulatory behaviour between LET and HET males but we cannot exclude line differences in other morphological or behavioural traits of male phenotype. In Japanese quail, social experiences have been shown to play a role in female mate preferences (Galef, 2008). Female quail display preferences for males they have seen mating with another female (Galef & White, 1998) or less aggressive males after observing aggressive interactions between males (Ophir & Galef, 2003). However, these effects were unlikely to influence mate choice behaviour in our study, since both males and females were unfamiliar and had not seen each other in mating or aggressive interactions with other partners. New insights from empirical and theoretical studies suggest that environmental circumstances and the intrinsic quality of the chooser sex are more likely to modify mating decisions than the phenotype of the chosen individual (Ah-King & Gowaty, 2016). Female mating preferences have been shown to vary in relation to both genetic and nongenetic factors, including female condition, previous experience or personality (Campbell & Hauber, 2009; Griggio & Hoi, 2010; Riebel et al., 2009; Schuett et al., 2011). In our study, females laying eggs with high yolk T levels were less
40
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42
discriminative in their mate preferences than females with comparable low yolk T deposition. Condition-dependent variation in female mate preferences predicts that females may experience different trade-offs between the costs and benefits of being more or less selective in their mate choice (Cotton, Small, & Pomiankowski, 2006). In general, female mate choice is considered to be a costly life history trait (Pomiankowski, 1987). Likewise, increased yolk T deposition may impose costs on the female in terms of a higher metabolic rate and a shorter life span (Tschirren et al., 2016; Tschirren, Postma, Gustafsson, Groothuis, & Doligez, 2014). Thus, we can expect that less discriminative mating behaviour in HET females may reflect the way in which they optimize costs for different life history traits. The benefits of choosing a particular mate may vary depending on the degree of relatedness between potential mates (Jennions & Petrie, 1997). To maintain an optimal balance between inbreeding and outbreeding, it is advantageous for females to choose males of intermediate relatedness (Bateson, 1982). In our study, both lines were reared separately in mixed-sex flocks, enabling early experiences with individuals from the same line, but not from the opposite line. Therefore, an adaptive explanation for reduced choosiness found in HET than LET females may reflect a strategy to minimize inbreeding risk and to increase genetic variability in HET offspring. Neuroendocrine mechanisms underlying variability in mating decisions are not yet well understood, although changes in the reproductive hormones controlling the reproductive physiology and behaviour of females are expected to be involved (Hirschenhauser, 2012; Lynch et al., 2006). In a study with darkeyed juncos, Junco hyemalis, females with experimentally increased plasma T levels showed reduced choosiness compared to control females (McGlothlin, Neudorf, Casto, Nolan, & Ketterson, 2004), indicating that T might play some role. However, our previous results demonstrated that selection for high yolk T levels did not result in permanently high T concentrations in the circulation of adult female Japanese quail, and we found no correlation between yolk and basal plasma T levels under constant conditions (Okuliarova, Groothuis, et al., 2011). Recently, we showed differences in the neuroendocrine control of the ovulatory cycle between LET and HET females (Okuliarova et al., 2018). Specifically, the preovulatory peak of LH was higher in HET than LET quail and these preovulatory LH levels correlated positively with increased preovulatory T concentrations in the plasma. Therefore, these results, together with our current study, suggest that the pattern of hormonal changes during the ovulatory cycle may provide a proximate mechanism for variation in female mate preferences. This is also consistent with results obtained in female túngara frogs, Physalaemus pustulosus, in which gonadotropin-induced hormonal changes near the time of ovulation were related to the highest receptivity to male cues and a decreased level of choosiness (Lynch et al., 2006). Since LET and HET females differ not only in their yolk T deposition but also in their exposure to yolk T levels during embryo development, we cannot exclude that such hormonemediated maternal effects may contribute to line differences in female mating decisions. Indeed, transgenerational epigenetic mechanisms have been shown to be involved in mate preference behaviour in rats, Rattus norvegicus, indicating an importance of this force in sexual selection (Crews et al., 2007). The effects of in ovo T treatment have been demonstrated in Japanese quail, in which males hatched from T-injected eggs displayed an affiliative preference towards familiar females, while control males did not have a preference between familiar and unfamiliar females (Schweitzer et al., 2013). In contrast, mate choice behaviour was not affected by the exposure to
elevated yolk T levels in female canaries, Serinus canaria (Vergauwen, Eens, & Muller, 2014). In conclusion, our results demonstrate an important link between maternal investment, reproductive physiology and female mating decisions in Japanese quail. Females from the genetic line with high yolk T levels displayed higher receptivity and were less choosy in their mate preferences than females from the opposite line with low T in their eggs. This correlative link may have several implications for the evolution of the variation in female mate preferences and for a role of this variation in sexual selection. Acknowledgments We thank two anonymous referees and the Editor Amanda Korstjens for their helpful comments on the manuscript. The study was supported by the Scientific Grant Agency of the Ministry of Education of the Slovak Republic VEGA 1/0686/15 and the Slovak Research and Development Agency APVV-17-0371. References Ah-King, M., & Gowaty, P. A. (2016). A conceptual review of mate choice: stochastic demography, within-sex phenotypic plasticity, and individual flexibility. Ecology and Evolution, 6(14), 4607e4642. https://doi.org/10.1002/ece3.2197. Andersson, M., & Simmons, L. W. (2006). Sexual selection and mate choice. Trends in Ecology and Evolution, 21(6), 296e302. https://doi.org/10.1016/j.tree.2006.03. 015. Ball, G. F., & Balthazart, J. (2009). Neuroendocrine regulation of reproductive behavior in birds. In D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrbach, & R. T. Rubin (Eds.), Hormones, Brain and Behavior (2nd ed., pp. 855e897). San Diego, CA: Academic Press. Balthazart, J., Cornil, C. A., Charlier, T. D., Taziaux, M., & Ball, G. F. (2008). Estradiol, a key endocrine signal in the sexual differentiation and activation of reproductive behavior in quail. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 311A(5), 323e345. https://doi.org/10.1002/jez.464. Bateson, P. (1982). Preferences for cousins in Japanese quail. Nature, 295, 236. https://doi.org/10.1038/295236a0. Bentz, A. B., Becker, D. J., & Navara, K. J. (2016). Evolutionary implications of interspecific variation in a maternal effect: A meta-analysis of yolk testosterone response to competition. Royal Society Open Science, 3(11), 160499. https://doi. org/10.1098/rsos.160499. Bonisoli-Alquati, A., Matteo, A., Ambrosini, R., Rubolini, D., Romano, M., Caprioli, M., et al. (2011). Effects of egg testosterone on female mate choice and male sexual behavior in the pheasant. Hormones and Behavior, 59(1), 75e82. https://doi.org/ 10.1016/j.yhbeh.2010.10.013. Campbell, D. L. M., & Hauber, M. E. (2009). Cross-fostering diminishes song discrimination in zebra finches (Taeniopygia guttata). Animal Cognition, 12(3), 481e490. https://doi.org/10.1007/s10071-008-0209-5. Cotton, S., Small, J., & Pomiankowski, A. (2006). Sexual selection and conditiondependent mate preferences. Current Biology, 16(17), R755eR765. https://doi. org/10.1016/j.cub.2006.08.022. Crews, D., Gore, A. C., Hsu, T. S., Dangleben, N. L., Spinetta, M., Schallert, T., et al. (2007). Transgenerational epigenetic imprints on mate preference. Proceedings of the National Academy of Sciences, 104(14), 5942e5946. https://doi.org/10. 1073/pnas.0610410104. Delville, Y., & Balthazart, J. (1987). Hormonal control of female sexual behavior in the Japanese quail. Hormones and Behavior, 21(3), 288e309. https://doi.org/10. 1016/0018-506X(87)90016-X. Domjan, M., Mahometa, M. J., & Mills, A. D. (2003). Relative contributions of the male and the female to sexual behavior and reproductive success in the Japanese quail (Coturnix japonica). Journal of Comparative Psychology, 117(4), 391e399. https://doi.org/10.1037/0735-7036.117.4.391. Egbert, J. R., Jackson, M. F., Rodgers, B. D., & Schwabl, H. (2013). Between-female variation in house sparrow yolk testosterone concentration is negatively associated with CYP19A1 (aromatase) mRNA expression in ovarian follicles. General and Comparative Endocrinology, 183, 53e62. https://doi.org/10.1016/j.ygcen. 2012.12.001. von Engelhardt, N., & Groothuis, T. G. G. (2011). Chapter 4 e Maternal hormones in avian eggs. In D. O. Norris, & K. H. Lopez (Eds.), Hormones and Reproduction of Vertebrates, Vol. 4: Birds (pp. 91e127). London, U.K.: Academic Press. Galef, B. G., Jr. (2008). Social influences on the mate choices of male and female Japanese quail. Comparative Cognition and Behavior Reviews, 3, 1e12. https://dx. doi.org/10.3819/ccbr.2008.30001. Galef, B. G., Jr., & White, D. J. (1998). Mate-choice copying in Japanese quail, Coturnix coturnix japonica. Animal Behaviour, 55(3), 545e552. https://doi.org/10.1006/ anbe.1997.0616. Garcia-Fernandez, V., Guasco, B., Tanvez, A., Lacroix, A., Cucco, M., Leboucher, G., et al. (2010). Influence of mating preferences on yolk testosterone in the grey
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42 partridge. Animal Behaviour, 80(1), 45e49. https://doi.org/10.1016/j.anbehav. 2010.03.023. Gowaty, P. A. (1994). Architects of sperm competition. Trends in Ecology and Evolution, 9(5), 160e162. https://doi.org/10.1016/0169-5347(94)90076-0. Griggio, M., & Hoi, H. (2010). Only females in poor condition display a clear preference and prefer males with an average badge. BMC Evolutionary Biology, 10(1), 261. https://doi.org/10.1186/1471-2148-10-261. Guibert, F., Richard-Yris, M. A., Lumineau, S., Kotrschal, K., Guemene, D., Bertin, A., et al. (2010). Social instability in laying quail: consequences on yolk steroids and offspring's phenotype. PLoS One, 5(11), e14069. https://doi.org/10.1371/journal. pone.0014069. Hagelin, J. C., & Ligon, J. D. (2001). Female quail prefer testosterone-mediated traits, rather than the ornate plumage of males. Animal Behaviour, 61(2), 465e476. https://doi.org/10.1006/anbe.2000.1618. Hirschenhauser, K. (2012). Testosterone and partner compatibility: evidence and emerging questions. Ethology, 118(9), 799e811. https://doi.org/10.1111/j.14390310.2012.02087.x. thov Horva a, T., Nakagawa, S., & Uller, T. (2012). Strategic female reproductive investment in response to male attractiveness in birds. Proceedings of the Royal Society B: Biological Sciences, 279(1726), 163e170. https://doi.org/10.1098/rspb. 2011.0663. Hsu, B.-Y., Dijkstra, C., & Groothuis, T. G. (2016). No escape from mother's will: effects of maternal testosterone on offspring reproductive behaviour far into adulthood. Animal Behaviour, 117, 135e144. https://doi.org/10.1016/j.anbehav. 2016.05.004. Jennions, M.,D., & Petrie, M. (1997). Variation in mate choice and mating preferences: a review of causes and consequences. Biological Reviews, 72(2), 283e327. https://doi.org/10.1111/j.1469-185X.1997.tb00015.x. Kankova, Z., Zeman, M., & Okuliarova, M. (2012). Growth and innate immunity are not limited by selection for high egg testosterone content in Japanese quail. Journal of Experimental Biology, 215(4), 617e622. https://doi.org/10.1242/Jeb. 064030. Kristofik, J., Darolova, A., Majtan, J., Okuliarova, M., Zeman, M., & Hoi, H. (2014). Do females invest more into eggs when males sing more attractively? Postmating sexual selection strategies in a monogamous reed passerine. Ecology and Evolution, 4(8), 1328e1339. https://doi.org/10.1002/ece3.1034. pez-Rull, I., & Gil, D. (2009). Do female spotless starlings Sturnus unicolor adjust Lo maternal investment according to male attractiveness? Journal of Avian Biology, 40(3), 254e262. https://dx.doi.org/10.1111/j.1600-048X.2009.04553.x. Loyau, A., & Lacroix, F. (2010). Watching sexy displays improves hatching success and offspring growth through maternal allocation. Proceedings of the Royal Society B: Biological Sciences, 277(1699), 3453e3460. https://doi.org/10.1098/ rspb.2010.0473. Lynch, K. S., Crews, D., Ryan, M. J., & Wilczynski, W. (2006). Hormonal state influences aspects of female mate choice in the Túngara Frog (Physalaemus pustulosus). Hormones and Behavior, 49(4), 450e457. https://doi.org/10.1016/j. yhbeh.2005.10.001. Mazuc, J., Chastel, O., & Sorci, G. (2003). No evidence for differential maternal allocation to offspring in the house sparrow (Passer domesticus). Behavioral Ecology, 14(3), 340e346. https://doi.org/10.1093/beheco/14.3.340. McGlothlin, J. W., Neudorf, D. L. H., Casto, J. M., Nolan, V., & Ketterson, E. D. (2004). Elevated testosterone reduces choosiness in female darkeeyed juncos (Junco hyemalis): evidence for a hormonal constraint on sexual selection? Proceedings of the Royal Society B: Biological Sciences, 271(1546), 1377e1384. https://doi.org/ 10.1098/rspb.2004.2741. Meylan, S., Miles, D. B., & Clobert, J. (2012). Hormonally mediated maternal effects, individual strategy and global change. Philosophical Transactions of the Royal Society B: Biological Sciences, 367(1596), 1647e1664. https://doi.org/10.1098/ rstb.2012.0020. Mills, A. D., Crawford, L. L., Domjan, M., & Faure, J. M. (1997). The behavior of the Japanese or domestic quail Coturnix japonica. Neuroscience and Biobehavioral Reviews, 21(3), 261e281. https://doi.org/10.1016/S0149-7634(96)00028-0. Navara, K. J., Hill, G. E., & Mendonça, M. T. (2006). Yolk androgen deposition as a compensatory strategy. Behavioral Ecology and Sociobiology, 60(3), 392e398. https://doi.org/10.1007/s00265-006-0177-1. nek, P., & Zeman, M. (2011). Experimental Okuliarova, M., Groothuis, T. G. G., Skrob a evidence for genetic heritability of maternal hormone transfer to offspring. American Naturalist, 177(6), 824e834. https://doi.org/10.1086/659996. Okuliarova, M., Kankova, Z., Skrobanek, P., & Zeman, M. (2014). Bidirectional selection for yolk testosterone content in Japanese quail. Avian Biology Research, 7(1), 18e24. https://doi.org/10.3184/175815514X13903210973681.
41
Okuliarova, M., Kostal, L., & Zeman, M. (2011). Effects of divergent selection for yolk testosterone content on growth characteristics of Japanese quail. Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology, 160(1), 81e86. https://doi.org/10.1016/j.cbpa.2011.05.012. Okuliarova, M., Meddle, S. L., & Zeman, M. (2018). Egg deposition of maternal testosterone is primarily controlled by the preovulatory peak of luteinizing hormone in Japanese quail. General and Comparative Endocrinology, 256, 23e29. https://doi.org/10.1016/j.ygcen.2017.05.004. Okuliarova, M., Sarnikova, B., Rettenbacher, S., Skrobanek, P., & Zeman, M. (2010). Yolk testosterone and corticosterone in hierarchical follicles and laid eggs of Japanese quail exposed to long-term restraint stress. General and Comparative Endocrinology, 165(1), 91e96. https://doi.org/10.1016/j.ygcen.2009.06.007. Ophir, A. G., & Galef, B. G. (2003). Female Japanese quail that ‘eavesdrop’ on fighting males prefer losers to winners. Animal Behaviour, 66(2), 399e407. https://doi. org/10.1006/anbe.2003.2230. Palokangas, P., Alatalo, R. V., & Korpim€ aki, E. (1992). Female choice in the kestrel under different availability of mating options. Animal Behaviour, 43(4), 659e665. https://doi.org/10.1016/S0003-3472(05)81024-3. Persaud, K. N., & Galef, B. G. (2005). Eggs of a female Japanese quail are more likely to be fertilized by a male that she prefers. Journal of Comparative Psychology, 119(3), 251e256. https://doi.org/10.1037/0735-7036.119.3.251. Pomiankowski, A. (1987). The costs of choice in sexual selection. Journal of Theoretical Biology, 128(2), 195e218. https://doi.org/10.1016/S0022-5193(87)801698. Riebel, K., Holveck, M.-J., Verhulst, S., & Fawcett, T. (2010). Are high-quality mates always attractive? State-dependent mate preferences in birds and humans. Communicative & Integrative Biology, 3(3), 271e273. https://doi.org/10.4161/cib. 3.3.11557. Riebel, K., Naguib, M., & Gil, D. (2009). Experimental manipulation of the rearing environment influences adult female zebra finch song preferences. Animal Behaviour, 78(6), 1397e1404. https://doi.org/10.1016/j.anbehav.2009.09.011. Ruuskanen, S. (2015). Hormonally-mediated maternal effects in birds: Lessons from the flycatcher model system. General and Comparative Endocrinology, 224, 283e293. https://doi.org/10.1016/j.ygcen.2015.09.016. Safran, R. J., Pilz, K. M., McGraw, K. J., Correa, S. M., & Schwabl, H. (2008). Are yolk androgens and carotenoids in barn swallow eggs related to parental quality? Behavioral Ecology and Sociobiology, 62(3), 427e438. https://doi.org/10.1007/ s00265-007-0470-7. Schuett, W., Godin, J.-G. J., & Dall, S. R. X. (2011). Do female zebra finches, Taeniopygia guttata, choose their mates based on their ‘personality’? Ethology, 117(10), 908e917. https://doi.org/10.1111/j.1439-0310.2011.01945.x. Schwabl, H. (1996). Maternal testosterone in the avian egg enhances postnatal growth. Comparative Biochemistry and Physiology a-Physiology, 114(3), 271e276. https://doi.org/10.1016/0300-9629(96)00009-6. Schweitzer, C., Goldstein, M. H., Place, N. J., & Adkins-Regan, E. (2013). Long-lasting and sex-specific consequences of elevated egg yolk testosterone for social behavior in Japanese quail. Hormones and Behavior, 63(1), 80e87. https://doi. org/10.1016/j.yhbeh.2012.10.011. Tschirren, B., Postma, E., Gustafsson, L., Groothuis, T. G. G., & Doligez, B. (2014). Natural selection acts in opposite ways on correlated hormonal mediators of prenatal maternal effects in a wild bird population. Ecology Letters, 17(10), 1310e1315. https://doi.org/10.1111/Ele.12339. Tschirren, B., Ziegler, A. K., Canale, C. I., Okuliarova, M., Zeman, M., & Giraudeau, M. (2016). High yolk testosterone transfer is associated with an increased female metabolic rate. Physiological and Biochemical Zoology, 89(5), 448e452. https:// doi.org/10.1086/687571. Uller, T., Eklof, J., & Andersson, S. (2005). Female egg investment in relation to male sexual traits and the potential for transgenerational effects in sexual selection. Behavioral Ecology and Sociobiology, 57(6), 584e590. https://doi.org/10.1007/ s00265-004-0886-2. Vergauwen, J., Eens, M., & Muller, W. (2014). Consequences of experimentally elevated yolk testosterone levels for intra- and inter-sexual selection in canaries. Behavioral Ecology and Sociobiology, 68(8), 1299e1309. https://doi.org/ 10.1007/s00265-014-1740-9. White, D. J., & Galef, B. G., Jr. (1999). Affiliative preferences are stable and predict mate choices in both sexes of Japanese quail, Coturnix japonica. Animal Behaviour, 58(4), 865e871. https://doi.org/10.1006/anbe.1999.1210.
42
D. Ledecka et al. / Animal Behaviour 157 (2019) 35e42
Appendix
(a)
(b)
40 cm LET
LET
Match zone 25 cm
30 cm
Central zone 20 cm
HET
Cross zone
LET
Cross zone
40 cm
30 cm
HET
Central zone
HET
Match zone
25 cm
(c)
(days)
Trial 1
Trial 2
Trial 3
d1
d2
d6
Figure A1. Experimental design of female mate choice test in Japanese quail lines divergently selected for low (LET) and high (HET) egg testosterone levels. Quails were assigned to tetrads consisting of two focal females (one from each line) and two target males (one from each line). For the focal female, preference zones for the male from the same and opposite lines represented match and cross zones, respectively. A trial began when males from the same tetrad (one from each line) were put into the end compartments. Subsequently, (a) the first focal female of the tetrad was placed into the central zone and her behaviour was recorded for 10 min. Next, this female was removed and (b) the second focal female of the same tetrad was placed into the central zone and her behaviour was recorded for another 10 min. (c) All focal females were given three trials within 6 days. See Methods for further details.