The evolution of sex‐biased dispersal by pre‐dispersal copulation and fluctuating environment
2004; Wiley; Volume: 73; Issue: 6 Linguagem: Inglês
10.1111/j.0021-8790.2004.00878.x
ISSN1365-2656
Autores Tópico(s)Species Distribution and Climate Change
ResumoJournal of Animal EcologyVolume 73, Issue 6 p. 1115-1120 Free Access The evolution of sex-biased dispersal by pre-dispersal copulation and fluctuating environment TADAO HIROTA, Corresponding Author TADAO HIROTA Department of Biology, International Christian University, Mitaka, Tokyo, 181–8585 Japan Tadao Hirota, Department of Biology, International Christian University, Mitaka, Tokyo, 181–8585 Japan. Fax: +81 (422) 33 1449; E-mail: t_hirota@cc.tuat.ac.jpSearch for more papers by this author TADAO HIROTA, Corresponding Author TADAO HIROTA Department of Biology, International Christian University, Mitaka, Tokyo, 181–8585 Japan Tadao Hirota, Department of Biology, International Christian University, Mitaka, Tokyo, 181–8585 Japan. Fax: +81 (422) 33 1449; E-mail: t_hirota@cc.tuat.ac.jpSearch for more papers by this author First published: 29 October 2004 https://doi.org/10.1111/j.0021-8790.2004.00878.xCitations: 18AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Summary 1 Additional factors relevant to dispersal are necessary to establish a general theory that can explain the sex-biased dispersal pattern of most taxa. The present study evaluated the influence of pre-dispersal copulation on the evolution of sex-biased dispersal. The influence of fluctuating environment, population size and dispersal cost were also analysed. 2 The simulation models were designed on the basis of the life history of Pieris rapae crucivora, in which female butterflies disperse among local habitats after copulation although male butterflies remain in the natal habitat. In the first model, where females always copulate before dispersal, the evolution of female-biased dispersal was facilitated by the fluctuating environment, but was suppressed by the stable environment. However, the fluctuating environment also suppressed the sex-biased dispersal in the second model where female dispersers always copulate after dispersal. Thus, the interaction between the pre-dispersal copulation and the fluctuating environment is a sufficient condition for the evolution of sex-biased dispersal. 3 The present study is the first report to reveal the important influence of pre-dispersal copulation on the evolution of sex-biased dispersal. In addition, the sexual difference in dispersal pattern increased with the increase of local population size and the decrease of dispersal cost. Introduction Dispersal is an adaptive behaviour to avoid inbreeding depression (Crespi & Taylor 1990), kin competition (for example see Kaitala et al. 1989) and risk due to fluctuating environment (Levin et al. 1984; Roff 1994). Sex-biased dispersal is common among dispersing species. In monogamous birds the dispersal is biased to females (Greenwood & Harvey 1982). Among mammals, the dispersal is not sexually biased in monogamous species, whereas males disperse mainly in polygamous and promiscuous species (Dobson 1982). Several theoretical studies have discussed the evolutionary process of sex-biased dispersal. Gandon (1999) concluded that low relatedness, high inbreeding depression and low dispersal cost facilitate sex-biased dispersal. Perrin & Mazalov (2000) noticed the sexual difference in kin competition, and demonstrated that when females cannot exhaust resources and consequently the local resource competition is weak, the dispersal was biased to males. Those theoretical models assume that dispersers mate and reproduce after emigration. They do not consider mating systems where dispersers mate before emigration and reproduce in both the natal habitat and the destination. Post-dispersal copulation is adaptive when inbreeding depression is strong, when sperm mortality in female organs is too high for long dispersal and when pregnant females cannot migrate effectively. Among some species, however, the dispersers mate in the natal habitat and reproduce before emigration. Therefore, it is worthwhile analysing how pre-dispersal copulation influences the evolution of sex-biased dispersal. Some models have assumed stable and homogeneous habitats (for example, Gandon 1999; Perrin & Mazalov 2000), as fluctuating environment is not necessary for evolution of the dispersal strategy (Hamilton & May 1977). However, wild animals cannot always remain in stable and homogeneous habitats. Their environments fluctuate spatially and temporally. When temporal fluctuation causes the extinction of local populations, dispersal is advantageous to recolonize an empty habitat where resources are revived after extinction (Roff 1994). When the condition of local habitats fluctuates independently and temporally, offspring dispersal to different populations increases the long-term fitness (Levin et al. 1984). In the absence of temporal fluctuation, however, spatial heterozygosity decreases the emigration rate, because dispersal from source populations to sink populations is disadvantageous (Hastings 1983). Thus, temporal fluctuation has strong influences on dispersal strategy. In the present study, the influence of environmental fluctuation on the sex difference in dispersal pattern was also examined. The cabbage white butterfly, Pieris rapae crucivora, is a suitable animal for discussing the influence of pre-dispersal copulation and fluctuating environment on the evolution of sex-biased dispersal. In P. rapae crucivora both sexes copulate in a natal habitat, and females emigrate more frequently than males (Ohsaki 1980; Yamamoto 1981). Female emigrants colonize and oviposit explosively at a habitat that is more than 1 km distant from the natal habitat (Ohsaki 1980), although they also deposit eggs during dispersal (Jones et al. 1980). Males also fly actively to search for mates (Yamamoto 1983; Hirota & Obara 2000a,b). However, males spend most of their time in the natal habitat, and rarely leave there until late in their life (Ohsaki 1980; Suzuki 1980). Thus, the dispersal of P. rapae crucivora is highly biased to females. P. rapae crucivora reproduces a larger number of smaller eggs and disperses longer than congeneric species (Ohsaki 1982). This butterfly is an r-strategist for adaptation to the fluctuating environment. While spontaneous crucifers are the essential food plants of P. rapae crucivora, cruciferous crops generate large patchy habitats (Ejima 1987). However, those farm habitats are disturbed frequently by early harvesting, pesticide-spraying and a change of crop (Yoshimura & Jansen 1996). The environmental change by farmers is unpredictable for butterflies because it does not always depend on the ecological factors, such as population density. Thus, P. rapae crucivora experiences an unpredictable fluctuating environment. In the present study, the simulation models based on the life history of P. rapae crucivora were built to analyse the influence of pre-dispersal copulation and fluctuating environment on sex-biased dispersal. In addition to these factors, the influence of dispersal cost and population size was also evaluated. The present models assumed that the allocation of reproductive efforts before and after dispersal was determined genetically, and simulated the evolutionary process of dispersal timing. Model 1 Model 1 is designed to evaluate how the fluctuating environment influences the sex difference in dispersal timing when females always copulate in the natal habitats. Individuals that have a similar life history to P. rapae crucivora (Fig. 1) are simulated to reproduce and disperse in a meta-population. The meta-population is comprised of 16 local habitats that are arranged in a 4 × 4 array (Fig. 2). The generation is assumed to be discrete. Each behaviour is accounted for as follows. Figure 1Open in figure viewerPowerPoint Flowchart of simulation models. Figure 2Open in figure viewerPowerPoint Location of habitats and the examples of dispersal. Butterflies disperse to the next habitat. For example, the butterflies who emerge at habitat A move to habitat B or C. The butterflies who emerge at habitat D move to habitat E, F, G or H. dispersal Ohsaki (1980) reported that newly emerged females are rarely recaptured in their natal habitats, but a few days after eclosion marked females are recaptured frequently in the same habitats more than 1 km from their birthplaces. Female dispersers also become philopatric in suitable habitats after natal dispersal. In this model, therefore, the dispersal is assumed to be performed once in a lifetime towards an adjacent habitat (Fig. 2). The dispersal direction is determined randomly. The dispersal is likely to cause an additional cost of increased mortality or reduced reproductive output. To evaluate the influence of dispersal cost, individuals are assumed to die at a constant rate by dispersal from the natal habitat to the next habitat. Four kinds of death rate, 0·00, 0·25, 0·50 and 0·75, are considered. It is assumed that dispersal timing of different sexes is determined by the different loci. It follows that individuals have two loci. One locus is expressed only for males, and the other locus is expressed only for females. Each locus has six alleles, which code the tactics that 0, 20, 40, 60, 80 or 100% of an adult lifetime, respectively, is spent after dispersal. Individuals are diploid. The expressed dispersal timing is a mean of both alleles. For example, an individual that has allele-20 and allele-40 spends 70% of an adult lifetime in a natal habitat and 30% after dispersal. In the initial condition, alleles of each individual were selected randomly from six alleles. No mutations were developed. copulation P. rapae crucivora females copulate twice on average in the field (Suzuki 1979). However, when females receive a spermatophore of normal size from males, they refuse another copulation for several days (Sugawara 1979; Rutowski et al. 1987; Oberhauser 1989; Kaitala & Wiklund 1995; Cook & Wedell 1999). Females oviposit explosively during this refractory period. It follows that most females invest the majority of their reproductive output before the second copulation (Suzuki 1978; Yamamoto & Ohtani 1979). Therefore, copulation with virgin females is the most valuable to males (Rutowski 1991). In fact, males optimize the time schedule of female searching behaviour to maximize the mating frequency with virgin females (Hirota et al. 2001). It is assumed therefore that females are functionally monogamous. In this model, females always copulate in the natal habitat before dispersal. The mating partner is selected from males that invest reproductive efforts to the females’ natal habitat. Although the mating partner is selected randomly, the competitive weight of males depends on the dispersal timing. The competitive weight increases with the time males spend in the habitat. That is, the male who stays throughout his life in a habitat will encounter females twice as frequently as the male who spends half of his life in the same habitat. It is assumed that males are polygamous, because male butterflies were observed to copulate multiple times in a day (Bissoondath & Wiklund 1996). oviposition The clutch size is set to be a hundred. Females allocate their eggs before and after dispersal according to the dispersal timing. Two specifically expressed sex loci are segregated independently. The birth sex ratio is even, and offspring are set to be male at the probability of 0·5. The number of individuals that develop from an egg into an adult butterfly is limited by the carrying capacity of each habitat. When the total number of eggs is more than the carrying capacity of a habitat, the individuals are selected randomly from eggs regardless of sex and genotype. Under a stable environment, the carrying capacity of all habitats is constant over all generations. Three kinds of carrying capacities, 10, 50 and 100, are considered to evaluate the influence of population size. In a fluctuating environment, the carrying capacity of each habitat is set randomly at a certain range and is changed with alternation of generations. Three kinds of range, 0–20, 0–100 or 0–200, are considered. In the initial condition, the same number of males and females are allocated into each habitat to reach the carrying capacity. In the fluctuating environment, individuals of mean carrying capacity are allocated to each habitat in the first generation at an even sex ratio. Each simulation is terminated when two loci relevant to dispersal are fixed. The simulation is replicated 20 times for each condition. results of model 1 In a stable environment, a small carrying capacity and low dispersal cost bring forward the dispersal timing and consequently increase the reproductive efforts after dispersal (Fig. 3). The dispersal does not evolve when the carrying capacity is 50 and the dispersal cost is 0·5 or more and when the carrying capacity is 10 and the dispersal cost is 0·25 or more. In other conditions, females disperse slightly earlier than males. However, those differences are small. Figure 3Open in figure viewerPowerPoint The resultant allele frequency of males (left) and females (right) in constant environment. Circle sizes represent the frequency of fixed alleles. K is the carrying capacity of local populations. The cost is the death rate in dispersion. In a fluctuating environment, the non-dispersal strategy, allele-0, is not fixed at a female specifically expressed locus regardless of carrying capacity and dispersal cost (Fig. 4). When the mean carrying capacity is 100 and the dispersal cost is 0·75, allele-0 coexists with allele-20 at a female specifically expressed locus for more than 10 000 generations in all trials. This suggests that the optimal dispersal timing is more than 0 and less than 20. On the other hand, allele-0 is fixed at a male specifically expressed locus (Fig. 4). The fixation of allele-0 is frequent, especially when the mean carrying capacity is 50 or more. Therefore, the sexual difference of dispersal timing is large, especially for a larger carrying capacity. Figure 4Open in figure viewerPowerPoint The resultant allele frequency of males (left) and females (right) in fluctuating environment. Circle sizes represent the frequency of fixed alleles. K is the mean carrying capacity of local populations and the fluctuating range. The cost is the death rate in dispersion. The asterisk (*) shows that allele-0 and allele-20 coexist for more than 10 thousand generations in all trials. Thus, a fluctuating environment facilitates female-biased dispersal where females always copulate before dispersal. Model 2 Model 2 is designed to evaluate how pre-dispersal copulation influences the sex-biased dispersal. This model is basically the same as model 1, but female dispersers are not allowed to copulate before emigration (Fig. 1). Female dispersers always reproduce after dispersal, whereas female non-dispersers copulate and oviposit only in the natal habitat. Whether females disperse or not depends on a female specifically expressed locus. This locus has six alleles, which code the emigration rates of 0, 20, 40, 60, 80 or 100%, respectively. Because individuals are diploid, the expressed emigration rate is a mean of both alleles. For example, the female that has allele-20 and allele-40 disperses at the probability of 30%. How the dispersal timing of both sexes evolves is simulated in the fluctuating environment with different carrying capacities and dispersal costs. results of model 2 In model 2, the high dispersal cost causes extinction of local populations. When the mean carrying capacity is 10 and dispersal cost is 0·75, all populations became extinct in the early generation (Fig. 5). When the mean carrying capacity is 50 or more and dispersal cost is 0·5 or more, allele-0 is sometimes fixed at a female specifically expressed locus (Fig. 5). However, the populations of non-dispersers cannot persist in a temporally fluctuating environment, as the vacant habitats are not recolonized. It follows that all populations became extinct after the fixation of allele-0 in the fluctuating environment where the carrying capacity becomes zero stochastically (Fig. 5; black parts of circles). Figure 5Open in figure viewerPowerPoint The resultant allele frequency of males (left) and females (right) in fluctuating environment. Circle sizes represent the frequency of fixed alleles. The black area of the circles represents the frequency of extinction after fixation. K is the mean carrying capacity of local populations and the fluctuating range. The cost is the death rate in dispersion. The asterisk (*) shows that all populations disappeared before fixation. When the populations are maintained persistently after fixation, the low dispersal cost brings forward the male dispersal and increases the emigration rate of females (Fig. 5). Larger carrying capacity delays males’ dispersal and slightly decrease females’ emigration rate. The influence of carrying capacity does not differ between sexes. This is in contrast to the result of model 1, where the sexual difference of dispersal timing is large, especially at larger carrying capacity. Therefore, the reproductive efforts after dispersal did not differ between the sexes. Thus, when some females copulate after dispersal, sex-dependent dispersal does not evolve in the fluctuating environment. Discussion In model 1, where females always copulate before dispersal, the fluctuating environment facilitates the female-biased dispersal. However, in model 2 where female dispersers always copulate after emigration, sex-dependent dispersal does not evolve in the fluctuating environment. It follows that the interaction between the fluctuating environment and pre-dispersal copulation is crucial to the evolution of female-biased dispersal. This interaction is caused by sexual differences of the way to spread the risk. In the fluctuating environment where source habitats of high quality disappear stochastically, it is advantageous in the long view for females to allocate some reproductive output to source habitats for spreading the risk (Yoshimura & Jansen 1996; Jansen & Yoshimura 1998). In the present models, because local habitats disappear stochastically in the fluctuating environment, females have to disperse even when dispersal entails cost. In model 1 the dispersal of moderate timing realizes the bet-hedging strategy where females oviposit before and after dispersal. In model 2, where females can reproduce at only one habitat, female emigration are also selected, since the genes coding emigration are distributed to different habitats and some of them can increase in the habitats with good conditions (Levin et al. 1984). Thus, in the fluctuating environment females have to disperse by themselves for spreading the risk. On the other hand, males are not necessary to disperse in model 1 where their mating partners spread the risk by dispersal after copulation and oviposition at different habitats. Especially when dispersal cost is high, it is advantageous for males to search for and copulate with females in a natal habitat. It follows that male dispersal is selected against in the fluctuating environment of model 1, although female dispersal is selected strongly (Fig. 4). This tendency is obvious when carrying capacity is larger, as small carrying capacity facilitates dispersal irrespective of sex, as discussed below for further details. However, selection pressure for spreading the risk brings forward the dispersal timing of females slightly more than that of males, even when carrying capacity is small. In contrast to model 1, males have to disperse by their own selves for spreading the risk in model 2 where females do not disperse after copulation (Fig. 5). Thus, whether or not females distribute males’ genes by dispersal after copulation has a crucial influence on males’ dispersal strategy. A smaller carrying capacity facilitates the early dispersal and increases the emigration rate (3-5). For lower population density, the kin competition increases and, consequently, dispersal is selected (Gandon 1999). In addition, the small population size causes bias of the sex ratio, since the sex of individuals is determined stochastically in the current models. The bias of sex ratio increases the heterogeneity of intrasexual selection pressure among local populations. Especially when the adults that emerge in a habitat are male only or female only, the dispersal is advantageous because either emigration to other habitats or immigration of the other sex is necessary for copulation. It follows that small carrying capacity facilitates early dispersal even under the stable environment. This tendency is obvious for male in both models. However, female dispersal is almost independent on carrying capacity in the fluctuating environment of model 1 (Fig. 4). As mentioned above, females have to disperse by themselves for spreading the risk, whereas males are not necessary to disperse because their risk is spread by females’ dispersal after copulation. Therefore, in the fluctuating environment of model 1, a female-biased dispersal is evident for the larger carrying capacity. The lower dispersal cost brings forward the dispersal timing and increases the emigration rate (3-5). This is concordant with findings in previous models (Gandon 1999; Perrin & Mazalov 2000). For lower dispersal cost, the sexual difference in dispersal timing is larger in the fluctuating environment of model 1. This is because female dispersal is delayed by the high dispersal cost, whereas males remain in the natal habitat or disperse late regardless of the dispersal cost, especially for larger population size. 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