Ethology Ecology & Evolution 19: 137-144, 2007
Mother-offspring correlation and mate-choice copying behavior in guppies L.A. Dugatkin
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and M. Druen
1
Department of Biology, University of Louisville, Louisville, KY 40292, USA Received 21 August 2006, accepted 12 January 2007
One broad, well-accepted definition of cultural transmission is the spreading of information by social learning or copying. The tendency to copy the action of others, however, may itself be a heritable trait. Here we measured the narrowsense heritability of the tendency of female guppies (Poecilia reticulata) to copy the mate choice of other females. Thirty-two female guppies were tested on their tendency to copy the mate choice of same-sized models. These 32 females produced a total of 83 female offspring, who upon reaching 11 weeks of age, were tested on their tendency to mate-choice copy. A significant positive correlation was found between the absolute time that mothers and their daughters spent near a male chosen by another (model) female. However, the correlation between the time that mothers and daughters spent near the male not chosen by the model female, and the correlation between mothers and daughters with respect to the proportion of time spent near a male chosen by a model, were not significant. Our data do not suggest that the tendency to copy the mate choice of others has a significant heritability. If it did, we would expect mothers and daughters to show similar scores on the proportion of time spent near a male chosen by a model, which is not the case. Instead, what appears to be a heritable trait is the absolute amount of time that a female spends near a male chosen by a model. Females in our study could do one of three things: spend time near a male chosen by a model, spend time near a male not chosen by a model, or spend time in the “neutral zone”. It appears that mothers and daughters behave similarly with respect to the first of these, but divide up their time between the second and third quite differently, thus producing the results we record here. key words:
mate-choice copying, heritability, parent-offspring correlation, sexual selection.
Introduction . . . Materials and methods Results . . . . Discussion . . . Acknowledgements . References . . .
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Department of Biology, University of Louisville, Louisville, KY 40292, USA. Corresponding author. Phone: 502-852-5943 (E-mail:
[email protected]).
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L.A. Dugatkin and M. Druen Introduction
At the most basic level, behavioral traits can spread from individual to individual in one of two ways: either through genetic transmission or via some form of cultural transmission such as social learning. While evidence for the former has been in the literature since the early 1900s, it is primarily over the last 30 years that evolutionary biologists and behavioral ecologists have focused their attention on the second form of transmission — this despite the fact social learning has been a mainstay of social psychology since the time of Darwin’s colleague, George Romanes (Romanes 1884). The importance of cultural transmission via social learning has now been documented in many behavioral venues, including foraging (Galef 1996, Laland & Williams 1997, Laland & Reader 1999, Galef & Giraldeau 2001, Brown & Laland 2003), song learning (Catchpole & Slater 1995) and mate choice in birds and fish (see below). With the growing realization that cultural transmission affects many different types of behavior, evolutionary biologists have become interested in the way in which genetic and cultural transmission can interact (Cavalli-Sforza & Feldman 1981, Boyd & Richerson 1985, Heyes & Galef 1996, Odling-Smee et al. 2003). For example, in their “dual inheritance” model, Boyd & Richerson (1985) argue that all of the forces that lead to changes in gene frequencies — natural selection, drift, mutation, and migration — have analogs within the realm of cultural evolution. Boyd & Richerson’s models demonstrate how cultural change can be studied with techniques similar to those developed by population geneticists (Boyd & Richerson 1985). Furthermore, they demonstrate how cultural evolution and genetic evolution can operate in the same or opposite directions and how either can be the predominate force, depending upon the particular scenario (Richerson & Boyd 1989). One ideal model system for examining the interaction of cultural and genetic transmission is female mate-choice copying, wherein females copy the mate choice of others in their population. Mate-choice copying has been uncovered in sage grouse (Centrocerus urophasianus; Gibson et al. 1991), black grouse (Tetrao tetrix; Hoglund et al. 1990, 1995), guppies (Poecilia reticulata; Dugatkin 1992, 1996; Dugatkin & Godin 1992, Dugatkin et al. 2002, but see Brooks 1996, Lafleur et al. 1997), sailfin mollies (Poecilia latipinna; Schlupp et al. 1994, Witte & Massmann 2003), medaka (Oryzias latipes; Grant & Green 1996), peacock blennies (Salaria pavo; Goncalves et al. 2003) and quail (Coturnix japonica; Galef & White 1998, White & Galef 2000), but not in fallow deer (Dama dama; Clutton-Brock & McComb 1993, McComb & CluttonBrock 1994), great snipe (Gallinago media; Fiske et al. 1996) or pied flycatchers (Ficedula hypoleuca; Slagsvold & Viljugrein 1999). Female mate-choice copying has been studied most extensively in the guppy (Poecilia reticulata). For example, Dugatkin (1992) ran six controlled experiments on mate choice in guppies — including controls for group size, side preferences and male courtship activity — and found that the data, as a whole, were only consistent with female mate-choice copying. Although it is always possible that some uncontrolled variable better explains what was called mate-choice copying, the 1992 experiments, or portions of them, have been replicated now in guppies from three different natural populations from Trinidad and Tobago, including guppies from the Quare (Briggs et al. 1996), Turure (Dugatkin & Godin 1993) and Paria (Dugatkin 1996) Rivers. In the guppy, mate-choice copying can, under some conditions, over-
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ride genetic predispositions that females display for certain male traits. For example, females from the Paria River have a heritable preference for mating with males with lots of orange body color; however, after observing another female (referred to as the model female) choose a drabber male, that drab male may be chosen as a mate by the observer guppy, suggesting an interesting interplay between genetic and cultural transmission (Dugatkin 1996, 1998). There is another manner, however, in which mate-choice copying may shed light on the interaction between genetic and cultural transmission, in that the tendency to copy the mate choice of others may itself be a heritable trait. While other work has found a genetic component to individual (or asocial) learning (Tang et al. 1999, Ferguson et al. 2001), no study to date has directly examined whether there is a genetic component to copying behavior (although work on “fast” and “slow” lines of great tits Parus major suggest a heritable component to copying in the context of foraging, this was not directly measured: Marchetti & Drent 2000; Drent et al. 2003; van Oers et al. 2004a, 2004b). To examine this possibility, we measured the narrow-sense heritability — a measure of additive genetic variance in a population — of the tendency of female guppies to spend time near a male chosen by another (model) female.
Materials and Methods We used guppies (Poecilia reticulata) descended from a population of fish from the Quare River in Trinidad and Tobago. We randomly selected and then isolated 32 pregnant females from four large (190 liter) stock tanks, each containing hundreds of guppies. The age of the pregnant females was not known. Once a female gave birth, each offspring was raised in an isolated individual aquarium. Females are particularly receptive to matings after parturition, and within 1 week after females gave birth, they were tested using standard mate preference tests to determine their tendency to copy the mate choice of others. All trials were videotaped from a camera mounted above the experimental apparatus (Fig. 1). Each female (referred to as a “focal” female) was placed into a clear Plexiglas cylinder in the center of a 37.85 liter test aquarium (50.8 × 30.5 × 26.6 cm) that had two smaller chambers (10 × 30.5 × 26.6 cm) immediately adjacent to it (one side chamber on left, one on right). A mature male was placed into each side chamber, and the males of each pair were chosen to be approximately equal in the percent of their body colored by orange pigment (mean difference in orange color = 0.26%) and lateral surface area (mean difference in lateral surface area = 0.10 cm2). A “model” female (size-matched to the focal female) was then placed behind a clear Plexiglas partition in the quarter of the tank nearest one of the males (which male was determined by the flip of a coin). The male adjacent to the model female underwent normal courtship behavior. After a 5 min viewing period, the model female and the clear partition keeping her near one of the males were removed (and a sham removal was performed on the opposite end of the aquarium). The focal female was then allowed to swim freely for 5 min, during which time the position of the focal female was recorded. For analysis of video recordings, the test aquarium was divided into quarters. The quarter of the tank adjacent to each male was labelled the “preference zone” for that male. Only time spent in preference zones was used for the regression analysis described below — i.e. any time spent outside the preferences zones, and hence in the middle 2/4 of the tank, was not used for analysis. Females were given such preference tests once a day for 4 days, and each day, a different set of males and a different model female were used for a given subject. The mean number of seconds spent in the preference zone of the male that was near the model was
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B
C
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Fig. 1. — An overhead view of the experimental apparatus. (A) clear Plexiglas cylinder, (B) male chambers, and (C) sections which served two functions: during the observation period a model female could be placed in one of the C compartments (behind a see-through partition) and, during the choice period, C served as a preference zone.
averaged for the four tests, as was the time spent in the preference zone near the male that was not adjacent to the model. Prior work has demonstrated that in guppies, the amount of time that females spent in the preference zone near each male in such tests correlates well with their behavior when actual mating is allowed (Bischoff et al. 1985, Dugatkin & Godin 1992), and the proportion of time spent near the male adjacent to the model female is indicative of mate-choice copying behavior (for more on this see: Dugatkin 1992, Dugatkin & Godin 1992, Dugatkin et al. 2002). That is, females who spend more time in the preference zone of male 1 than in that of male 2 are more likely to mate with male 1, when given the possibility. More generally, prior work in guppies strongly indicates that the tendency to mate-choice copy can be estimated using the proportion of time that females spent in the preference zone of a male that had been adjacent to the model. Each of the offspring born to the 32 females described above was raised in isolation in an individual aquarium measuring 10 × 10 × 18.4 cm. Gravel lined the bottom of these aquaria, and all four sides were covered with white paper for visual isolation. As these offspring matured, male offspring were returned to stock tanks, but each female offspring remained in its individual aquarium until sexual maturity at 11 weeks of age (mean number (± se) of female offspring/clutch = 2.59 ± 1.07). At that time, all female offspring were tested on their tendency to copy the choice of other females, using the same protocol employed to test their mothers (new model females and males were used in offspring trials; i.e. mothers and daughters were not tested using the same model, or the same males). For each clutch of offspring, the mean amount of time spent near each male was calculated (i.e., a single score was obtained for each clutch of daughters).
Results
A significant non-zero slope was uncovered when regressing the mean amount of time a female spent near males that were chosen by the model female against the mean amount of time her daughters spent near males that had been chosen by model females (Fig. 2a: r2 = 0.14, P < 0.05; y = 81.3 + 0.36x, SE of slope = 0.15). However, the correlation between the time that mothers and daughters spent near the male away from the model female was not significant (Fig. 2b; r2 = 0.01, P >
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Mean number of seconds that daughters spent in the preference zone of the male chosen by the model
0.9; y = 106.26 + 0.01x, SE of slope = 0.17). Furthermore, the correlation between mothers and daughters with respect to the proportion of time spent near a male chosen by a model (r2 = 0.001, P > 0.6; y = 174.91 + 0.11x, SE of slope = 0.20) was not significant.
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Fig. 2. — (a) The mean number of seconds that daughters spent in the preference zone of a male preferred by others as a function of the mean number of seconds their mothers spent in the preference zone of a male preferred by others. Each point represents the mean value of all daughters in a clutch (N = 32 females, and hence 32 clutches). Any time spent in the middle two quarters of the tank was not used for this analysis. (b) The mean number of seconds that daughters spent in the preference zone of a male preferred by others as a function of the mean number of seconds their mothers spent in the preference zone of a male preferred by others. Each point represents the mean value of all daughters in a clutch. Any time spent in the middle 2/4 of the tank was not used for this analysis.
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L.A. Dugatkin and M. Druen Discussion
One consistent finding from previous work on mate-choice copying in guppies is that while the majority of females copy the mate choice of others, somewhere between 15-35% of females do not engage in mate-choice copying. Rather than define a female as a “copier” or not, here we set out to examine whether variation in the tendency to prefer a male as a function of the preference of others was due to genetic variance by using mother-offspring correlations. Our data do not suggest that the tendency to copy the mate choice of others has a significant heritability. If it did, we would expect mothers and daughters to show similar scores on the proportion of time spent near a male chosen by a model. That is, when mothers spend a large proportion of time near a male chosen by a model, their daughters should do likewise. Our data show that this is not the case. Instead, what appears to be a heritable trait is the absolute amount of time that a female spends near a male chosen by a model. If a mother spent x seconds near a male chosen by a model, her daughters were likely to spend a similar amount of time near a male chosen by a model. But, because there is no correlation between the time that mothers and daughters spend near the male not chosen by the model, nor in the proportion of time spent near a male chosen by the model, this is not equivalent to the tendency to mate-choice copy. Our findings are not as odd as they may at first appear to be. Females in our study could do one of three things: spend time near a male chosen by a model, spend time near a male not chosen by a model, or spend time in the “neutral zone”. It appears that mothers and daughters behave similarly with respect to the first of these, but divide up their time between the second and third quite differently, thus producing the results we record here. When a regression analysis examines a single parent and clutch of offspring, heritability is estimated as twice the slope of the regression line (Hartl & Clark 1997). Evidence from sailfin mollies (Poecilia latipinna), a species closely related to guppies, suggests that both sexes are influenced by the mate choice of others (Witte & Ryan 2002). If this generalization of both sexes being influenced by the mate choice of other applies to guppies, we estimate the heritability of the amount of time female guppies spend near males that have been chosen as twice the slope of the regression line (slope = 0.35), or approximately 0.70. If this trait is sex-limited, then the 0.70 may be an overestimate, and the true heritability may be closer to 0.35. It should, however, be noted that other aspects of the methodology employed here may have led to an underestimate of heritability. Females from the two generations tested were raised in different environments (stock tanks for generation 1, individual aquaria for generation 2), tested at different life-history stages (after giving birth in generation 1, as virgins in generation 2) and at different ages (unknown for generation 1, eleven weeks old for generation 2). Each of these differences makes the estimate of heritability described above a conservative estimate. For example, all else equal, the fact that mothers and their daughters were raised in very different environments (stock tanks vs individual aquaria) should tend to make them less similar, not more, and hence decrease heritability. Analogous arguments can be made for differences in life history and age.
Acknowledgements This work was funded by an NICHD grant to Lee Alan Dugatkin. We thank Dana Dugatkin, Perri Eason, Paul Ewald and two anonymous reviewers for comments and suggestions.
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