Wile the definition of "culture" has been debated in
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1 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: (1998)] Wile 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; Cavalli- Sforza 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 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-
2 324 Behavioral Ecology Vol. 9 No. 4 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 (25-40% 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%). e D B C A hl-h D E C 8 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
3 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 = ± 5.1% (x ± 1 SD; range %). 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) 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-
4 326 Behavioral Ecology VoL 9 No. 4 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. B KKKkBMfTRS Andemon M, Sexual selection. Princeton, New Jersey. Princeton University Press. Bisazza A, Marconato A, Female mate choice, male-male competition and parental care in the river bullhead, Cotus gqbio. Anim Behav 36: Buchoff RJ, Gould JL, Rubenstein DI, Tail size and female choice in the guppy (PotdUa rtticuiata). Behav Ecol Sodobiol 17: BonnerJT, The evolution of culture in animak Princeton, New Jersey: Princeton Universiry Press. Boyd R, Richerson PJ, Culture and the evolutionary process. Chicago: University of Chicago Press. Bradbury JW, Andersson M (eds), Sexual selection: testing the alternatives. New York: Wiley-Interscience. Breden F, Stoner G, Male predaiion risk determines female preference in the Trinidadian guppy. Nature 329: Briggs SE, Godin JG, Dugatkin LA, Mate-choice copying under predation risk in the Trinidadian guppy (PotdUa rtticuiata). Behav Ecol 7: Brooks R, Copying and the repeatability of mate choice. Behav Ecol Sociobiol 39: CzvaUi*S ona LL, Feldman M, Cultural transmission and evolution: a quantitative approach. Princeton, New Jersey: Princeton University Press. Chitton-Brock TH, Hiraiwa-Hasegawa M, Robertson A, Mate choice on fallow deer leks. Nature 340: Chitton-Brock TH, McComb K, Experimental tests of copying and mate choice in fallow deer (Dama dama). Behav Ecol 4: Constanz G, Alloparental care in the tessellated darter, Eihtottoma oimsutu (Pisces: Percidae). Environ Biol Fun 14: Dugatkin LA, Sexual selection and imitation: females copy the mate choice of others. 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5 Dugatkin Genes, copying, and female mate choice 327 preferences. 1. Fisher and biased mutation. Evolution 45: Pruettjones SG, Independent versus non-independent mate choice: do females copy each other? Am Nat 140: Ridley M, Rechten C, Female sticklebacks prefer to spawn with males whose nests contain eggs. Behaviour 16: Rohwer S, Parental <-annikali<m of offspring and egg raiding as a courtship strategy. Am Nat 112: Romanes GJ, Mental evolution in animal* New York: Ap pel ton. Romanes GJ, Animal intelligence. London: Kegan Paul, Trench, Trubner and Co. Schhipp I, Marier C, Ryan M, Males benefit by mating with heterospecific females. Science Servedio MR, Kirkpatrick M, The evolution of mate choice copying by indirect selection. Am Nat 148: Shuster SM, Wade M, Female copying and sexual selection in a- marine isopod crustacean, Parxutrcas sadpta. Anim Behav 41: Slater PL, Eales L, Clayton N, Song learning in zebra finches: progress and prospects. Adv Study Behav 18:1-33. Stoner G, Breden F, Phenotypic differentiation in female preference related to geographic variation in male predauon risk in the Trinidad guppy. Behav Ecol Sociobiol 22: Unger LM, Sargent RC, Alloparental care in the fayh«h minnow, Ptmtphalo prowttiaz females prefer males with eggs. Behav Ecol Sociobiol 23: Zentall T, Galef BG, Social learning: psychological and biological perspectives. Hillsdale, New Jersey: Lawrence Eiibaum Associates. Zuk M, Johnson K, Thornhill R, Ligon JD, Mechanisms of female choice in red jungle fowl Evolution 44:
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