First
Cousin Preference vs. Mate Choice Copying in Determining Japanese Quail Female
Mate Choice
AJ Shankar
Project Summary
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.
Introduction
By isolating a genetic influence
and a social influence on mate choice and pitting them against each other, this
experiment allows for three possible valid outcomes. One hypothesis is that the
genetic preference for first cousins is so strong that it outweighs the social
factor of mate choice copying (MCC), even if the male selected by the model
female is unrelated to the focus female; in this case, the focus female
consistently chooses her first cousin. Another hypothesis is that instead,
copying exerts such a powerful influence on mate choice that the focus female
consistently picks the model female’s chosen mate, whether a sibling or an
unrelated individual, over her own first cousin – even though first cousins are
more genetically attractive. A final hypothesis, the one to which I subscribe,
is that there is a threshold of relative male attractiveness below which mate
choice copying exerts a stronger influence, and above which the genetic
preference wins out. That is, focus females who observe their siblings being
chosen as mates still tend to prefer first cousins, whereas those who see (more
attractive) unrelated males being chosen tend to pick them over first cousins.
Background
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.
Why the Japanese quail?
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.
Proposed Study
Acquisition and care of Japanese quail
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.
Experimental Setup
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.
Procedure for Experiment 1
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.
Procedure for Experiment 2
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
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.
Anticipated Significance of Results
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.
Possible Valid Results
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.
Figure 1
References
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.