First Cousin Preference vs. Mate Choice Copying in Determining Japanese Quail Female Mate Choice
I propose to compare the relative strengths of mate choice copying, a social influence, and first cousin preference, a genetic influence, in determining the mate choice of female Japanese quail. Female quail have a strong genetic preference for selecting first cousins as mates; they prefer unrelated males far less, and siblings even less so (Bateson 1982). Quail also practice mate choice copying (Galef & White 1998). I allow a focus female quail to witness a sibling or unrelated male being chosen by a model female, and then let the focus female chose between a first cousin and the selected male, thus pitting genetic and social influences against each other. The female’s choice provides important information about the influence of copying on overall mate choice (about which there is little prior evidence), including the possible presence of a threshold between copying and genetic factors. Such information is extremely valuable in constructing a model of sexual selection that accurately accounts for both genetic and social influences.
Sexual selection has been viewed as a significant factor in trait evolution in animals since Darwin (1871). Dugatkin (1992) points out that while male-male intrasexual competition has long been accepted as a mainstay of sexual selection, only in the last quarter-century have biologists gathered substantial evidence for female mate choice as another primary motivator. This evidence has almost exclusively supported mate choice as a genetically determined trait. However, significant findings in recent years point to social cues as alternate mechanisms for mate choice.
One such social cue is a phenomenon known as mate choice copying, in which one female exhibits an increased desire to mate with a male because she has witnessed another female choose him as a mate. Such a strategy has obvious advantages if independent mate choice is costly and results in the selection of a better than average mate: the copier derives the benefit of a better mate without incurring the cost of her own analysis and selection. In fact, Losey et al. (1986) found that under proper conditions MCC can be a conditional evolutionarily stable strategy.
Hoglund et al. provided the first empirical support of mate choice copying in 1990 with a field study of black grouse; however, while much of the data supported MCC, it did not isolate copying as the only possible explanation for the mate selection of female black grouse. This inherent difficulty in controlling for extraneous mechanisms in field experiments was circumvented by Dugatkin (1992), whose excellent series of lab experiments on guppies succeeded in isolating MCC as a definitive factor in the mate choice of female guppies. His findings strongly promoted the inclusion of copying in future sexual selection models.
Dugatkin and Godin proceeded to showcase the strength of MCC in an experiment in which female guppies reversed their initial mate preference due to mate choice copying (1992). This finding sparked inquiries about the strength of the influence of copying in mate choice relative to the influence of standard genetic preferences common in many animals. In 1996 Dugatkin showed that there is a threshold of attractiveness in male guppies under which copying can be used to reverse results in females, but over which genetic preference dominates. Such a result has significant implications: copying, a social influence, is a strong enough factor in female mate choice to actually compete with genetic influences, which were long held as the only factors. Clearly additional studies, such as this proposed experiment, are necessary to verify or counter such a noteworthy result. The scarcity of concrete evidence about copying coupled with its potentially large implications provides ample motivation for further investigation.
The Japanese quail, Coturnix japonica, has several advantageous characteristics for laboratory use, including short development and life cycles (up to four generations per year), rapid maturation, high prolificacy, quick adaptation to laboratory conditions, disease resistance, and relatively low food consumption (Canadian Council on Animal Care, 1984). In addition, females lay up to 300 eggs per year, making it especially easy to obtain large numbers of siblings.
Furthermore, Galef and White (1998, 1999) established that female Japanese quail demonstrate mate choice copying under strict laboratory conditions. Westneat et al. (2000) outline several alternate sources of nonindependent mate choice that might be misinterpreted as mate choice copying, such as the magnification of male traits after mating, a female’s potential association to a location (as opposed to a male), and an increase in female sexual receptivity simply from watching a mating – all of which Galef and White successfully controlled for.
Japanese quail also appear to have a strong genetic preference for mating with first cousins. Bateson (1982) showed that both male and female quail spend significantly more time near first cousins than they do near siblings or unrelated individuals. Considering these results along with Bateson’s observation that the quail made courtship displays during his experiment, and with his earlier finding (1978) that time spent near another quail is strongly linked to copulation preference, I conclude that quail prefer first cousins as sexual partners. This influence on mate choice provides the necessary genetic selection basis against which to test mate choice copying.
Furthermore, in Bateson’s study, females preferred first cousins to unrelated quail by a ratio of roughly 2:1, and first cousins to siblings 3:1. I attempt to utilize the varying strengths of these preferences to determine whether there is a threshold between genetic and social factors similar to the threshold Dugatkin found in guppies. By using both siblings and unrelated males, I present the females with different levels of choice: they must choose between first cousins and very unattractive males (siblings) who have been chosen by the model females, and between first cousins and only somewhat unattractive (unrelated) males with mate choice. The females may in fact treat these two cases similarly. However, if they do not then I can infer, from the relative preferences of the siblings and unrelated males, the threshold at which the copying influence starts to outweigh the genetic influence. Hence, I propose to run two experiments, one with siblings and one with unrelated males.
32 male and 16 female Japanese quail are acquired from a commercial breeder with the following constraints:
1. There are four groups of twelve birds each; the birds in each group are unrelated to the birds in all other groups.
2. Within each group, there are two subgroups of six siblings, each consisting of four males and two females; the two subgroups are first cousins.
The birds are acquired 45-60 days after birth and are housed in individual stainless steel cages with dimensions of approximately 45 x 60 x 40 cm. Care of Japanese quail is well documented; I follow standard procedures for this experiment, providing them with unlimited water and commercial game bird food, such as the Purina Game Bird Startena 5419 used by Galef and White (1998).
To usher the birds into breeding condition, I subject them to a regimented 16:8 h light:dark cycle for 30 days, also suggested by Galef and White. At this point I attempt to familiarize the quail with the experimental setup, and accustom them to mating there. I pair unrelated males and females in the setup until the males start mounting multiple females in succession. Females are deemed ready to mate when they lay eggs every other or third day.
At this point I isolate the birds for 10 days before commencing the actual experiment.
I conduct all experiments in a wooden shed with a plexiglass top (Figure 1). The shed rests on an aluminum tray covered with absorbent paper pads. Across the middle of the shed floor is a painted dividing line and directly in the center is an individual holding cage. The shed is partitioned into three areas; during the experiment, each of the outer areas holds a male quail while the focus female stays in the middle. There are removable opaque partitions separating the three areas. During all experiments, quail are moved about via the accepted (and least disruptive) method of hand holding (Canadian Council on Animal Care, 1984). An overhead videocassette recorder is used to preserve the results for later analysis. A focus female is said to prefer a male if the amount of time she spends on his side of the area is greater than the amount of time she spends on the other side. Since, as Bateson showed (1978), there is a strong correlation between time spent near a potential mate and actual mate preference, this serves as a good measure for female mate choice.
Because practical concerns prevent me from acquiring the many quail necessary to eliminate any subject-pairing repetition, I use the following pairing scheme. Since each trial requires a focus female to be paired with a first cousin, and each female has four male first cousins, within each group there are sixteen such pairings. With four groups, therefore, there are 64 pairs of male-female first cousins. I use 32 for each experiment detailed below, 16 for each of the variable and control portions of Experiments 1 and 2. The third bird in each trial is easily selected: each focus female has a male sibling corresponding to each of her first cousins, and unrelated males are chosen from the 24 which are not related to the focus female. The model female (if there is one) is simply a female unrelated to the target male. For a given focus female, if the target male is a sibling, there are 12 such model females from which to choose; if he is unrelated to the focus female, there are eight. The trials are ordered so that no single bird is ever tested twice in a row, preventing excessive acclimatization or location cues.
With the shed’s opaque partitions in position, I place a focus female in the holding cage in the center area. I place one of her male siblings in the left area, and one of her male first cousins in the right area. In successive trials, I switch the placement of the two males. After one minute of acclimation time, I place an unrelated female (the model) within the area containing the sibling and remove the partitions. I leave the focus female in the center for 10 minutes; during that time she is able to see her sibling mating and her first cousin remaining celibate. If the chosen male fails to mount the model female, the data from this trial is discarded. Such an event rarely occurred in previous experiments with quail. Then, I remove the model female and free the focus female from the holding cage. During the next 10 minutes, I observe the amount of time she spends on each side of the area. This experiment is repeated 16 times, once for each female bird.
The procedure for this experiment is the same as that for Experiment 1, except that an unrelated male is substituted for the focus female’s sibling.
Controls for each experiment are handled as follows: each trial is re-run with the same two males, but the focus female is replaced with her sister, and the model female is not used. Since the sisters necessarily shared the same relationship with the two males in question, I expect that the sister will consistently pick the first cousin. Any consistent aberrations from this behavior may indicate possibly external influences on mate choice, and would motivate a reanalysis of the procedures for this experiment.
Female quail are not susceptible to other known forms of nonindependent mate choice (Galef and White 1998, 1999), so if mate choice copying does not exert a significant role, I expect that females consistently choose their first cousins in both of the experiments. However, if mate choice is a relevant influence, I expect to see some females choosing siblings or unrelated males, even though genetically they are most inclined to prefer first cousins.
Since female quail exhibit a stronger preference for first cousins over siblings than they do for first cousins over unrelated males, Experiment 2 should have as many or more focus females selecting unrelated males as Experiment 1 has selecting siblings. If this is not the case, or if the results are random and inconsistent across females, then most likely there are other factors that I have not taken into account; the methodology of this experiment must then be reviewed, and Dugatkin’s procedures for analyzing copying (1996) may also be called into question.
However, if there is a consistent dataset, this knowledge is valuable regardless of the result: it provides additional validation for Dugatkin’s model (1996) for experimentally examining the relative strengths of cultural and genetic effects on female mate choice. His model can then be applied with greater confidence to other species and conditions to gather additional information on the effects of social influence on female mate choice.
1. Most females choose their first cousins in both experiments.
Since Japanese quail exhibit MCC, this result implies that copying is dominated by the genetic preference for first cousins when the two strategies are in conflict. Copying may be a backup mechanism, which raises interesting questions as to how it evolved and when quail use it (perhaps when deciding between two unrelated males, for instance). This result contrasts with Dugatkin’s outcome with guppies, and may perhaps encourage a rethinking of the importance of social influences in mate choice.
2. Most females choose their first cousins in Experiment 1, but most choose the unrelated male in Experiment 2.
The Experiment 2 results indicate that part of the time mate choice copying outweighs the genetic preference for first cousins. In certain cases, then, social cues are as relevant as genetic ones in determining mate choice, and so should be incorporated into new models of sexual selection. This case provides additional support for Dugatkin’s threshold result (1996). Are such thresholds common? Can they be evaluated and determined in terms of direct reproductive success, or are there other factors involved? Further experiments should be performed that refine the location of the threshold with respect to the first cousin bias, and also analyze the reproductive success of females who mate with siblings, cousins, and unrelated males.
3. Most females choose their siblings in Experiment 1 and unrelated males in Experiment 2.
This is a truly remarkable result. It is the first evidence of a social influence consistently outweighing a genetic one in determining mate choice, and requires a radical restructuring of commonly held conceptions about mate choice. Wade and Pruett-Jones (1990) have shown that copying increases the variance in male reproductive success and therefore may be a prime actuator of sexual selection. If, for instance, male traits and female preferences for them were genetically linked, then a new trait would not require the favor of a large number of females to spread. Instead, a lucky male could produce many offspring with his unique traits – and preferences for these traits – simply because he mated early and was consistently chosen thereafter through mate copying. Furthermore, White and Galef (2000) provide evidence that copying can be generalized as well: females may have an increased tendency to mate not only with the chosen male, but also with other males that share his characteristics. Thus, if MCC is a primary strategy for mate choice, sexually selected traits could gain prominence very rapidly. This could have two possible effects: on the one hand, any trait which already has a genetic preference would benefit from the independent selection that arises as a result, after which MCC would kick in and induce many other females, including those who did not have a preference for that trait, to mate with males bearing it as well. The growth and spread of previously established traits would thus be phenomenally accelerated. On the other hand, MCC may act negatively, preventing any one trait from gaining too much prominence or becoming too costly. The barrier to entry for a new, less costly trait would be lower than in a purely genetic model, since by the same logic, if a few females independently select for the new trait, many others would follow suite via copying. While each of these claims is entirely unjustified, it is regardless clear that the impact of such a large cultural and social influence on mate choice likely requires the substantial reworking of current models of sexual selection.
The study of the effect of social cues on mate choice is a burgeoning field. Initial experiments show promising results, but with so few test species and conditions, the effect of mate choice copying on female mate choice may be grossly misestimated. This proposed experiment is vital to more accurately assess the value of copying. Any meaningful result, whether positive or negative, is constructive. With so few results already published, an experiment such as this is likely to have a significant impact, whether as a building block in the new, modified theory of mate choice, or as critical evidence that stands against it.
Bateson, P. 1978. Sexual imprinting and optimal outbreeding. Nature, 273, 659-660.
Bateson, P. 1982. Preferences for cousins in Japanese quail. Nature, 295, 236-237.
Canadian Council on Animal Care. 1984. Guide to the care and use of experimental animals. Found online at http://www.ccac.ca/guides/english/toc_v2.htm.
Darwin, C. 1871. The descent of man and selection in relation to sex. London: John Murray.
Dugatkin, L.A. 1992. Sexual selection and imitation: females copy the mate choice of others. American Naturalist, 139, 1384-1389.
Dugatkin, L. A. 1996. The interface between culturally-based preferences and genetic preferences: Female mate choice in Poecilia reticulata. Proceedings of the National Academy of Sciences, 93, 2770-2773.
Dugatkin, L. A. & Godin, J.–G. 1992. Reversal of female mate choice by copying in the guppy (Poecilia reticulata). Proceedings of the Royal Society of London, Series B, 249, 179-184.
Galef, B. G., Jr. & White, D.J. 1998. Mate-choice copying in Japanese quail, Coturnix coturnix japonica. Animal Behavior, 55, 542-552.
Hoglund, J., Alatalo, R. V. & Lundberg, A. 1990. Copying the mate choice of others? Observations on female black grouse. Behavior, 114, 221-231.
Losey, G. S., F. G. Stanton, T. M. Telecky, W. A. Tyler III & Zoology 691 Graduate Seminar Class. 1986. Copying others: An evolutionarily stable strategy for mate choice - a model. American Naturalist, 128, 653-664.
Wade, M. J. & Pruett-Jones, S. G. 1990. Female copying increases the variance in male mating success. Proceedings of the National Academy of Sciences, 87, 5749-5753.
Westneat, D. F., Walters, A., McCarthy, T. M., Hatch, M. I., Hein & W. K. 2000. Alternative mechanisms of nonindependent mate choice. Animal Behavior, 59, 467-476.
White, D.J. & Galef, B. G., Jr. 1999. Mate-choice copying and conspecific cuing in Japanese quail, Coturnix coturnix japonica. Animal Behavior, 57, 465-473.
White, D.J. & Galef, B. G., Jr. 2000. ‘Culture’ in quail: social influences on mate choices of female Coturnix japonica. Animal Behavior, 59, 975-979.