Behavioral Ecology Vol. 9 No. 4: 32*-327
Genes, copying, and female mate choice:
shifting thresholds
Lee Alan Dugatkin
Department of Biology, The University of Louisville, Louisville, KY 40292, USA
Recent experimental work on guppics (PoeciUa nticulata) has crammed the strength of genetic and cultural (copying) factors
in determining female mate choice. Using females from a population with a heritable preference for the amount of orange
body color possessed by males, prior work discovered that a threshold difference in orange color among males existed below
which females would choose a less orange male if they observed another female choose that male, but above which they
consistently preferred the more orange of the males, regardless of whether they viewed another female prefer the less orange
male. I tested whether this threshold can be shifted by increasing the amount of mate-copying information available to a female.
I demonstrate that when a female has the opportunity to see two different model females independently prefer the less orange
of two males or a single female near a drab male for a longer period of time (twice as long as in prior work), the observer
female prefers this drab male even when males dramatically differ in orange coloration. Kty words: guppies, mate choice, mate
copying, PoeciUa reticulata, sexual selection. [Behav Ecoi 9:323-327 (1998)]
W
ile the definition of "culture" has been debated in
anthropological circles for decades (Boyd and Richerson, 1985), evidence from anthropology and psychology indicates that cultural transmission of traits plays a role in behavioral evolution (Bonner, 1980; Boyd and Richerson, 1985;
Cavalli-Sforza and Feldman, 1981; Heyes and Galef, 1996).
One simple but common mode of cultural transmission is
copying. Although social psychologists have been studying imitative behavior since Romanes (1895, 1898), widi the exception of work on imprinting, ethologists and evolutionary ecologists have only recently begun studying this subject. Over the
last 15 years, a theoretical framework for understanding the
evolution of copying has begun to emerge, as population geneticists, anthropologists, and evolutionary ecologists have
started to develop models for the evolution of cultural behavior, including imitation (Boyd and Richerson, 1985; CavalliSforza and Feldman, 1981; Findlay, 1991; Kirkpatrick and Dugatkin, 1994; Laland, 1994a,b; Servedio and Kirkpatrick,
1996). Cultural transmission; particularly via imitation, is ubiquitous in humans, but it has also been found in nonhumans
in the context of foraging in rats (see Galef, 1996, for a review), song learning in birds (Slater et aL, 1988), mate choice
in fish (Dugatkin, 1992, 1996a,b; Dugatkin and Godin, 1992,
1993), and a variety of other situations (see Bonner, 1980;
Boyd and Richerson, 1985; Cavalli-Sforza and Feldman, 1981;
Heyes and Galef, 1996; Zentall and Galef, 1988).
In their "dual inheritance" model, Boyd and Richerson
(1985) show that the forces that bring about changes in gene
frequencies—natural selection, drift, mutation, and migration—have analogs within the realm of cultural evolution.
Boyd and Richerson's (1985) work demonstrates how cultural
change can be studied with techniques similar to those developed by population geneticists, how cultural and genetic
evolution can operate in the same or opposite directions, and
how either can be the predominate force, depending on the
particular scenario (Richerson and Boyd, 1989).
A female's choice of mates is almost certainly influenced by
both cultural as well as innate factors. Evolutionary models of
sexual selection typically assume strict genetic control of all
Received 2 June 1997; reviled 6 November 1997; accepted 26 November 1997.
O 1998 International Society for Behavioral Ecology
aspects of mate choice (Grafen, 1990; Kirkpatrick, 1982;
Lande, 1982; CDonald, 1980; Pomiankowksi et aL, 1989; but
see Kirkpatrick and Dugatkin, 1994; Laland, 1994a,b; Servadio
and Kirkpatrick, 1996), and even more mechanistic approaches to the study of how females go about deciding between
males (Zuk et al., 1990) do not include "social" factors, such
as the choices made by others. Social factors such as mate
copying, however, may be conceptually intriguing because genetic models of sexual selection suggest that female mate
choice may coevolve with the male trait being chosen (see
Andersson, 1994, for a review). If copying plays a role in how
females choose their mates, then the coevolution of male trait
and female preference may be influenced by cultural evolution in ways that may be distinct from genetic evolution (Boyd
and Richerson, 1985). Furthermore, studying culture in the
context of female mate choice may also allow us to experimentally examine the evolution of a trait (female preference)
when both innate and cultural factors are operating simultaneously (see below).
According to Pruettjones's (1992: 1001) definition, female
mate copying occurs when "the conditional probability of
choice of a given male by a female is either greater or less
than the absolute probability of choice depending on whether
that male mated previously or was avoided, respectively." Although copying has long been thought to play a role in lekmating birds and mammali (Bradbury and Andersson, 1987;
Hoglund et aL, 1990; IiU, 1974), the very nature of lek systems
makes experimental manipulation difficult In fact, most of
the empirical evidence for female mate copying gathered to
date is anecdotal or lacking all the proper control experiments (Outton-Brock et aL, 1989; Gibson et aL, 1991; Goldschmidt et aL, 1993; Hoglund et aL, 1990; Shuster and Wide,
1991; but see Qutton-Brock and McComb, 1993; McComb
and Qutton-Brock, 1994, for controlled experimental evidence that female fallow deer, Dama dama, do not mate
copy). For example, a number of studies in fishes suggest that
females prefer males that already have broods from prior matings (Bisazza and Marconato, 1988; Constanz, 1985; Goldschmidt et aL, 1993; Ridley and Rechten, 1981; UngeT and
Sargent, 1988) and that such preferences are a sign of mate
copying. These experiments, however, are in fact rather ambiguous, as females may prefer nests with eggs, not as a mechanism for mate copying, but because this dilutes the proba-
324
bility that their own eggs will be taken should a predator attack (Jamieson, 1995; Robwer, 1978).
The first controlled experimental evidence for female mate
copying was found in the guppy, PoectUa reticulata (Dugatkin,
1992; see Dugatkin, 1996a, for a review). Female guppies remembered the identity of males that were chosen by other
females and subsequently showed a strong preference for
those males (Dugatkin, 1992). Alternatives to mate-choice
copying, such as aquarium side biases on the part of the observer female, or group size (shoaling) effects, were examined
in control experiments, but did not account for the results.
Differential activity and courtship behavior of stimulus males
have also been ruled out as an alternative to mate-choice copying (Dugatkin, 1992). Since that study, mate-choice copying
has been detected in at least two other species, sailfin mollies
{Poeatia formosa, Schhipp et aL, 1994) and medaka (Oryxias
latipes, Grant and Green, 1995), and strong correlational evidence suggests it plays a role in black grouse (Tetrao tetrix,
Hoglund et aL, 1990, 1995) as well.
Female guppies from at least three separate rivers in Trinidad (Briggs et al., 1996; Dugatkin, 1992; Dugatkin and Godin,
1992, 1993; but see Brooks, 1996; Lafleur et aL, 1997) will
copy each other's choice of mates, but in the absence of matecopying opportunities, female guppies will choose between
males on the basis of a number of phenotypic traits such as
size, tail length, and color pattern (Bischoff et aL, 1985; Breden and Stoner, 1987; Houde, 1988; Houde and Endler, 1990;
Kodric-Brown, 1985; Stoner and Breden, 1988; see Endler and
Houde, 1995, for a review) and in some cases these preferences are based on genetic predispositions. For example, female guppies from the Paria River in Trinidad, West Indies,
have a genetically based preference for orange color in males
(Houde, 1988; Houde and Endler, 1990; also see Houde,
1992, for evidence that orange color is heritable in males).
Dugatkin (1996a) used the guppy system to examine the
relative importance of genetic predispositions and the tendency to copy in the context of female mate choice. In this
experiment, pairs of males in four treatments differed by an
average of 4, 12, 25, and 40% orange color (Le., percentage
of body covered by orange). In all cases, observer females
viewed a "model" female near the drabber (Le., less orange)
of two males. When males differed by 4, 12, or 25%, observer
females subsequently chose the less orange of the males, suggesting that social cues (via copying) can override a genetic
predisposition for orange color. When, however, males differed by 40%, observer females chose the male with more
orange, indicating that genetic predispositions swamp out any
social cues for this difference in coloration in males. Controls
documented that for all four treatments, when no model was
present, females consistently chose the more orange male
(Dugatkin, 1996b).
The above work clearly demonstrates a threshold area (2540% difference in orange color in males) below which social
cues outweigh genetic predispositions in mate choice and
above which the opposite is true. Can this threshold be shifted? If so, this will have serious implications for the way we
view the relationship between genes and social/cultural influences on behavior. Furthermore, where mate choice does not
involve copying, behavioral ecologists are interested in threshold effects on female choice [e.g., are they relative or absolute? (Zuk et aL, 1990)]. Here I report an experiment that
increased the social information available to an observer female and shows that when an observer has the opportunity
to see two different model females independently prefer the
less orange of two males, or see a single model female spend
more time with a drab male (twice as long as in prior work),
the observer prefers this male even when males dramatically
differ in orange coloration (Le., 40%).
Behavioral Ecology Vol. 9 No. 4
e
B
D
D
C
A
E
C
8
hl-H
Figure 1
A side view of the experimental apparatus, consisting of a
rectangular aquarium (40X20X25 cm, LXWXH) with a dear
Plexiglas rectangular container juxtaposed against each of its ends.
A, central Plexiglas cylinder; B, male chambers; C, area into which
model was placed; D, clear Plexiglas partition; and E, opaque
partition!. From Dugatkin (1996a).
MATERIALS AND METHODS
I used laboratory-reared males and females descended from
individuals captured in the Paria River of Northern Trinidad,
West Indies for all treatments. Because they are very receptive
to male courtship, only virgin females were tested. Juvenile
guppies were raised from birth in communal tanks. Once a
juvenile displayed any male characteristics (e.g., coloration,
development of gonopodium), it was immediately removed
from the communal tank. Throughout their development, females observed normal courtship and mating in tanks adjacent to their own. Soon after sexual maturity, females were
used in the trials described below.
The experimental apparatus used was identical to that of
Dugatkin (1996b) and shown in Figure 1. In each trial, I
placed an observer female in the central Plexiglas cylinder
and placed one male in each end chamber. These fish were
then given 5 rain to acclimate, during which time opaque
partitions blocked the observer female's view into both male
chambers. After the acclimation period, a second female, labeled die "model" female, was always placed near the less
orange of the two males (see below for more on male coloration), and hence if an observer female was copying the modeL less orange males would be preferred.
Although the model female was not allowed to freely
choose between the males (as she was always placed in an area
near the less orange male), the courtship behavior displayed
by the model female and the male nearest her was stereotypical guppy courting behavior (Iiley, 1966) and thus provided
an opportunity for the observer-female to see the model apparently choose a male. Four treatments were undertaken, as
described below.
Treatment 1 replicated the work of Dugatkin (1996b). After
placing the model into the experiment tank, I removed the
opaque partitions (E in Figure 1), and the two males and the
model female were in view of the observer female for a period
of 5 min. After this viewing period, the model female was
takenfromthe arena, as were both the Plexiglas partition that
kept her Bear one of the two males (B in Figure 1) aad the
Plexiglas cylinder that housed the observer female (A in Figure 1). I recorded the amount of time the observer female
then spent in the preference zone associated with each male
for 5 min (area C was the preference zone after the partitions
holding a model in place were removed; Figure 1). Only time
Dugatlrin • Genes, copying, and female mate choice
•all
in the preference zone near a given male was used when calculating which male a female spent the majority of her time
near. I tested 20 different observer females, each with a different pair of males.
EJ No model
ID 1 model/5 minute*
l model/10 minutei
Treatment 2
Treatment 2 was identical to treatment 1, with one important
exception. After the observer female viewed the model female
for 5 min, the exact same procedure was repeated 5 min later
using the same observer female and pair of males, but with a
different model (placed near the drabber male, after the original model was removed). After these two viewing periods, the
model female was taken from the arena, as were both the
Plexiglas partition that kept her near one of the two males
and the Plexiglas cylinder that housed the observer female. I
recorded the amount of time the observer female then spent
in the preference zone for 5 min. I tested 20 new observer
females, each with a different pair of males (the same male
pairs used in treatment 1).
Treatment 3
To control for time viewing a model (versus the number of
models as in treatment 2), treatment 1 was repeated, except
that a focal female had the opportunity to view a single model
for 10 min (rather than 5 min as in treatment 1). I tested 20
new observer females, each with a different pair of males (the
same male pairs used in treatment 1).
Treatment 4
Twenty control trials were undertaken in which the protocol
was identical to that of treatment 2, except that no model
females were present The same pairs of males tested in treatments 1, 2, and S were tested in the controls, but new females
were used.
Each trial of all four treatments had one "drab" male and
one more orange male. Fifty-five males were photographed
before the experiment and a Lasico (model 42-P) Planimeter
was used to calculate the area of the total body length of each
fish and the proportion of total body length covered by orange color. Let M denote the proportion of total body length
covered by orange color in the more orange of the two males
used in a trial; let L denote the proportion of total body
length covered by orange color in the less orange male, and
let Q = 1 — (L/M) (this is the same measure used in Dugatkin, 1996b, but due to a typographical error the formula was
listed as L/M in this prior work). For the 20 pairs of males
used in the experiments, Q = 40.32 ± 5.1% (x ± 1 SD; range
54.5-64.8%). Males in all trials were within 10% of each
other's total length. Although males were used more than
once over the course of the experiment, at least 3 days separated trials using the same individual.
I viewed fish behavior using a video camera (coupled to a
television monitor) mounted behind a black curtain. During
this period, both males and females displayed typical courtship activities, with males exhibiting sigmoid displays to females and females showing the "gliding" motion typically associated with courtship (Liley, 1966). The focal female was
classified as preferring a particular male if, over the course of
the test, she spent more time in the preference zone of that
male compared to the other male (Le., time spent outside
both preference zones was not used to determine female
choice). The mate choice of individual female guppies determined by such a preference test is known to correlate well
with their choice of mate when actual mating is allowed (Bischoff et aL, 1985; Dugatkin and Godin, 1992).
23 2 modela/S minute* each
"3
Treatment
Figure 2
The proportion of females that preferred the drabber male in the
four treatments.
RESULTS
The frequencies with which the drab males were preferred
across treatments is shown in Figure 2. When no model was
present, females preferred more orange males in 16 of 20
cases (treatment 4: G =7.7, df = 1, p < .01). When observers
saw a single model for 5 min, females also preferred the more
orange of two males in 16 of 20 trials (treatment 1; G -=7.7,
df = 1, p < .01). These two treatments replicate findings in
Dugatkin (1996b). In addition, a G test for heterogeneity
across all four treatments shows a significant effect (G^ =
15J36, df = 3, p < .005). An unplanned orthogonal comparison of frequencies revealed that this effect was due to a significant difference between treatments 2 / 3 (Le., the combined effect of treatments 2 and 3) and treatments 1/4 (G^,
= 15.47, df «= 1, p < .005). In other words, when males differed by 40% orange coloration, genetic predispositions for
orange overrode social cues when a single model was used for
5 min, but social cues masked such predispositions when an
observer saw two females sequentially prefer the less orange
male or a single model prefer the drab male for 10 (versus
5) min.
DISCUSSION
Historically, it has been difficult for behavioral biologists to
experimentally examine the relative importance of genetic
and cultural factors in shaping behavior. Because of prior
work done on both the genetics of female mate choice and
on mate copying, the guppy system is ideal for examining this
question. In an earlier study (Dugatkin, 1996b), I found that
cultural cues via imitation can "override" genetic preferences
for more orange males when males differ by small (12%) or
moderate (24%) amounts of orange and females observe a
single model near the less orange of the males for 5 min
When the difference in body color is great (40%), however,
imitation effects are blocked and females consistently prefer
more orange males (Dugatkin, 1996b). The present study
showed that this threshold ran be shifted such that much
drabber males (i.e., 40% less orange) are chosen if an observer sees two different females independently prefer the less
drab male or observe a female spend more time (10 versus 5
min) near a drab male. Although some models have exam-
326
ined the relationship between cultural and genetic preferences in the context of mate copying (Kirkpatrick and Dugatkin, 1994; Laland, 1994a,b; Servedio and Kirkpatrick,
1996), none of these models has examined the phenomenon
outlined here.
Most evolutionary models of female mate choice ignore the
role that copying may play in decision making. The work presented here (in conjunction with Briggs et aL, 1996; Dugatkin,
1992, 1996b; Dugatkin and Godin, 1992, 199S; Gibson et aL,
1991; Grant and Green, 1995; Hoglund et aL, 1990, 1995;
Schhipp et aL, 1994) suggests not only that copying plays a
significant role in female mate choice, but that the amount
of information available to females about the choice of others
moderates the relative importance of copying in comparison
to any genetic predispositions females may possess. Although
it may not be surprising that increasing the magnitude of a
stimulus in various ways (number, length of observation) increases the response to that stimulus, both the potential number of models and the time for which they are observed need
to-be examined theoretically and empirically to better understand precisely how these factors influence mate choice and
the interaction of genetic and social factors underlying sexual
selection in general.
The results presented here are the first of their kind denv.
onstrating that the threshold delineating the relative strength
of genetic versus social factors in determining mate choice not
only can be measured, but can be manipulated via the amount
of social information. This suggests an even stronger role for
social/cultural cues in the evolution of animal social behavior
than has been previously surmised (Dugatkin, 1996b). Furthermore, the general protocol developed here, though specific to mate choice in guppies, could easily be modified to .
test the relative strength of genetic and nongenetic factors on
the expression of a variety of traits in species in which at least
a baseline level of information is available about each factor.
I thank A. Dugatkin and D. Dugatkin for comment* on earlier drafts
of this paper.
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