Journal of Heredity Advance Access originally published online on June 25, 2008
Journal of Heredity 2008 99(6):610-615; doi:10.1093/jhered/esn053
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Molecular Evidence for Multiple Paternity in a Feral Population of Green Swordtails
Centre for Evolutionary Biology, School of Animal Biology (M092), The University of Western Australia, Crawley, 6009, Australia (Simmons, Beveridge, and Evans)
Address correspondence to Leigh W. Simmons at the address above, or e-mail: lsimmons{at}cyllene.uwa.edu.au.
Genetic parentage analyses provide insights into mating systems and have revealed widespread evidence for polyandry in natural populations. Here, we use 5 microsatellite markers to estimate female mating rates in a feral population of green swordtails, Xiphophorus helleri, a live-bearing poeciliid fish that has become a model system in the study of precopulatory mate choice and mating competition. Although heralded as a potential model for investigating sperm competition as early as 1950, there has been no attempt to explore postcopulatory sexual selection in its mating system. We thus obtained information on the prevalence, and therefore biological relevance, of polyandry from a wild population. We genotyped the offspring from 14 wild-caught gravid females and determined the number of fathers in each brood using allele counting methods and the programs GERUD and PARENTAGE. Our analyses revealed that 57% (allele counts and GERUD) and 71% (PARENTAGE) of the sampled broods had at least 2 sires, with a global mean 1.74 fathers per brood. Paternity skew was generally high in mixed paternity broods so that our analyses almost certainly underestimate actual mating frequencies in the wild. Our data provide a solid underpinning for future studies of postcopulatory sexual selection in this species.
Polyandry, where females mate with multiple males within a single reproductive episode, is taxonomically widespread among animals and plants and has profound evolutionary effects on male and female reproductive biology. For example, a large body of theoretical and empirical work has addressed the adaptive value of polyandry for females (Keller and Reeve 1995; Zeh JA and Zeh DW 1996, 1997; Yasui 1997; Jennions and Petrie 2000; Simmons 2005). Polyandry also has important consequences for postcopulatory processes as selection will favor male traits that increase the relative success of competing ejaculates (Parker 1970; Simmons 2001) and/or female traits that bias fertilization toward preferred or compatible males (Thornhill 1983; Eberhard 1996). Although many studies have focused on these topics under experimental laboratory conditions, in many cases there is an urgent need to determine the prevalence, and therefore biological relevance, of polyandry in natural populations (Simmons et al. 2007). A key parameter in this regard is the estimate of the frequency of mixed paternity broods and the number of fathers contributing toward mixed paternity broods (Avise et al. 2002; Jones and Ardren 2003), as such data yield important information on the opportunity for postcopulatory sexual selection in natural populations.
Among fishes, poeciliids are particularly amenable to genetic parentage studies as they are livebearers, and entire broods can be collected from wild-caught gravid females for subsequent paternity analyses. Moreover, in many of these species, females mate promiscuously (Hildemann and Wagner 1954; Borowsky and Kallman 1976; Pitcher et al. 2003) and are capable of storing sperm for several months (Winge 1937; Constantz 1989; Potter and Kramer 2000). Because of these features of their reproductive biology, sperm competition is expected to be an important selective pressure in poeciliids (Hildemann and Wagner 1954; Constantz 1984; Evans and Magurran 2001).
A variety of genetic techniques have been used to estimate the levels of multiple paternity in natural populations of poeciliids, including the analysis of sex-linked phenotypes, allozymes, and microsatellites (Luo et al. 2005). These techniques have confirmed the occurrence of multiple paternity in mosquitofish (Gambusia spp.) (Chesser et al. 1984; Robbins et al. 1987; Greene and Brown 1991; Zane et al. 1999), guppies (Poecilia reticulata) (Haskins et al. 1961; Kelly et al. 1999; Neff and Pitcher 2002), sailfin mollies (Poecilia latipinna) (Travis et al. 1990; Trexler et al. 1997), platys (Xiphophorus maculatus and Xiphophorus variatus) (Borowsky and Kallman 1976; Borowsky and Khouri 1976), swordtails (Xiphophorus multilineatus) (Luo et al. 2005), topminnows (Poeciliopsis monacha) (Leslie and Vrijenhoek 1977), and killifish (Heterandria formosa) (Soucy and Travis 2003).
The green swordtail, Xiphophorus helleri, was first recognized as a candidate species for investigating sperm competition 2 decades before Parker (1970) first alerted biologists to the evolutionary implications of sperm competition in his review of the insects. These live-bearing poeciliid fish, native to southern Mexico but distributed widely in feral populations (Courtenay and Meffe 1989), have resource-free mating systems and have become a model system in the study of precopulatory intra- and intersexual selection (Basolo 1990; Morris 1998; Rosenthal et al. 2001; Johnson and Basolo 2003; Benson and Basolo 2006; Fisher and Rosenthal 2007; Walling et al. 2007). Clark (1950) was the first to develop the method of artificial insemination in live-bearing fishes using X. helleri, commenting with remarkable foresight that the "experimental investigation of the problem of sperm competition could be greatly facilitated in these viviparous fishes by a method for controlled inseminations." Since Clark's (1950) pioneering work, artificial insemination has been developed in poeciliid fishes (Lodi 1981; Evans et al. 2003) and has been used to investigate postcopulatory sexual selection while controlling the influence of precopulatory interactions between males and females (Evans et al. 2003). Despite their early promise, however, green swordtails have never been studied in the context of postcopulatory sexual selection, and there are currently no published data on the occurrence of polyandry in the laboratory or in natural populations. This study aims to facilitate future studies on postcopulatory sexual selection in X. helleri by estimating the natural rates of polyandry in a wild population. We use microsatellite markers to genotype the offspring produced by wild-caught females and genetic parentage analyses to estimate the number of sires in each brood.
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Materials and Methods |
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Population Sampling
A population of X. helleri was sampled in March 2006 from the Irwin River, south of Geraldton, Western Australia (S29 13.066', E115 16.008'). Feral populations of X. helleri were first reported in Australia in the early 1960s (Lever 1996). The first published record of X. helleri from the Irwin River was in 2001 (Morgan and Gill 2001). They are widespread throughout the river system (Morgan and Gill 2004) and occur in high densities (LW Simmons, JP Evans, personal observation). Fish were caught with a 1-person seine, and females were transported to the laboratory where they were housed individually in separate 5-l containers (containing airstone and weed) until they gave birth to their first brood. To ensure that all offspring were the result of matings in the wild, rather than in transit, we only considered broods produced within 20 days of collection (gestation is ca., 26–30 days). The offspring were collected immediately and frozen. A fin clip of each female was also taken and frozen for microsatellite analysis.
Microsatellite Analysis
DNA was extracted from adult fin clips of the females and from the whole offspring using a rapid salt extraction method (Simmons et al. 2006). The samples were screened using 5 microsatellite markers, 4 developed specifically for X. helleri (Yue and Orban 2004) and 1 developed in Xiphophorus montezumae (Seckinger et al. 2002). To allow for the different annealing temperatures, 3 polymerase chain reactions (PCRs) were carried out. The first contained 1 x PCR buffer (10 mM Tris–HCl pH 8.3, 50 mM KCl) (Invitrogen, Mount Waverley, Victoria), 1.5 mM MgCl2 (Invitrogen), 200 µM of each deoxynucleoside triphosphate (Invitrogen), 250 nM of Xhe 02 forward primer labeled with 6-Fam (Geneworks, Hindmarsh, South Australia) and Xhe 03 forward primer labeled with Ned (Applied Biosystems, Scoresby, Victoria), the labeled primer diluted 1:10 with unlabeled primer, 250 nM of Xhe 02 and Xhe 03 reverse primers, 0.5 units of Platinum Taq polymerase (Invitrogen), and 1–10 ng DNA. PCR amplification was performed with cycling conditions as follows: 94 °C for 3 min, then 30 cycles of 94 °C for 35 s, 55 °C for 35 s, and 72 °C for 75 s, and finally 72 °C for 30 min. The second PCR was similar, but with Xhe 15 forward primer labeled with Pet (Applied Biosystems), Xhe 01 forward primer labeled with 6-Fam (Geneworks) and an annealing temperature of 60 °C. The third PCR was also similar, with KonT38 forward primer labeled with PET (Applied Biosystems) and an annealing temperature of 48 °C. The products from each PCR (1.5 µl) were combined and analyzed on an ABI3730 Sequencer, sized using Genescan-500 LIZ internal size standard, and genotyped using Genemapper software (version 3.7).
Estimating the Number of Sires
For each of the females collected, their offspring (9–24 offspring per female) were genotyped and the number of fathers was estimated in 3 ways: allele counting, GERUD (version 2.0) (Jones 2005), and PARENTAGE (Emery et al. 2001). For allele counting, this involved identifying the maternal alleles and disregarding them. Homozygotes at a particular locus were assumed to have 1 maternal and 1 paternal allele, and heterozygotes with the same genotype as the mother were taken to have one contributing paternal allele. Alleles were then counted, and the number from the locus with the most nonmaternal alleles was taken as an estimate of the number of paternal alleles present. This number was then divided by 2 (each potential father could donate 2 different alleles) to give a conservative estimate of the number of fathers present.
Next, we used PARENTAGE (Emery et al. 2001) to infer the probable number of fathers of each family using population allele frequencies, and initial probabilities based on what we already knew about the parentage of the offspring. Each maternal genotype was specified, and initial probabilities for the number of possible fathers, based on the number of offspring present in each family, were set. The maternity share was set with a low probability of there being more than one mother (gamma distribution with a shape parameter of 1 and a mean of 0.25). The paternity share was set using a gamma distribution with a shape parameter of 1 and a mean of 0.005. To allow for a mutation rate that agrees with levels observed for microsatellite markers (Weber and Wong 1993), a mutation rate was set using a gamma distribution with a shape parameter of 2 and a mean of 0.001. This allowed for 95% of the mutation rates to lie between 0.00014 and 0.0028 mutations per generation. We ran 5000 iterations for each family (using a burn-in of 5000 and a thinning interval of 400).
Finally, we used the software program GERUD (version 2.0) (Jones 2005), which is more sophisticated than allele counting because it uses multiple loci simultaneously. After removing the maternal alleles from offspring genotypes, the program then simulates all possible paternal genotypes and calculates the combinations of these genotypes that yield the fewest possible males that could have contributed to the offspring genotypes observed.
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Characterizations of the microsatellite markers in this population of X. helleri are provided in Table 1. Across the 5 microsatellite loci, the population shows no evidence of inbreeding (mean inbreeding coefficient did not differ from zero; FIS = –0.003 ± 0.096, t4 = –0.03, P = 0.979) and no significant deviation from Hardy–Weinberg equilibrium (
2 = 14.76, degrees of freedom = 10, P = 0.141). Heterozygosity was moderate (mean observed heterozygosity, 0.541 ± 0.097), close to that reported from a natural population of X. multilineatus (0.573; Luo et al. 2005) and broadly within the range found among natural populations of other poeciliid fishes: for H. formosa average hetereozygosity across microsatellite loci ranged from 0.557 to 0.821 (Soucy and Travis 2003), for P. reticulata from 0.445 to 0.888 (Kelly et al. 1999), and for 2 natural populations of Gambusia holbrooki heterozygosity was 0.679 and 0.663 (Zane et al. 1999). Thus, the population genetics of this feral population of X. helleri appear similar to populations of poeciliid fishes in their natural range.
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Our genetic analyses revealed multiple paternity in the majority of broods that were sampled. Results from the allele counting method provided conservative estimates of the number of sires present in each brood, which in the 14 families analyzed yielded a mean (±standard error) of 1.57 ± 0.10 (Table 2). For the PARENTAGE analyses, the modal number of sires ranged from 1 to 4 with a mean of 2.1 ± 0.3 and the mean number of fathers also ranged from 1 to 4 with a slightly higher mean of 2.3 ± 0.3 (Table 2). The GERUD method yielded identical results to the allele counting method (Table 2). For 5 of the females, the 3 estimates for number of fathers were identical. For the remaining females, the estimates tended to be higher than the other methods in all but one case (S25). With PARENTAGE, Pmode values indicate the probability of obtaining the observed modal number out of 5000 iterations. For the estimates that do agree with the other calculation methods, the mean Pmode was 0.89 ± 0.04 compared with a mean Pmode of 0.60 ± 0.07 for the estimates that disagree with the other methods. This suggests that the higher estimates returned by PARENTAGE for these females may be unreliable.
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GERUD provides a reconstruction of potential sire genotypes and an estimation of the number of offspring fathered by each sire. For each father combination, we calculated the paternity skew as the sum of the squared proportions of offspring sired (Starr 1984). All mixed paternity broods were sired by just 2 males and with random sperm mixing skew should equal 0.5. Thus, for 2 broods (S9 and S22), there was no evidence of paternity skew, whereas for the remaining broods, the 95% confidence intervals for skew did not include 0.5, indicating that paternity was significantly skewed toward one of the fathers (Table 2).
Finally, we assessed the power of the microsatellite markers to detect mixed paternity broods using the software provided by Neff and Pitcher (2002). Given the allele frequencies for the microsatellite loci in Table 1, the average number of offspring sampled for each female with 2 fathers (17) and an average paternity skew of 0.73, the power to detect 2 fathers was 0.68, and the power to detect 3 fathers was 0.88.
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Discussion |
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Our molecular genetic analyses revealed clear and consistent evidence for polyandry in wild-caught female green swordtails, adding to an increasing number of studies reporting estimates for polyandry in natural populations of fishes (Avise et al. 2002; Soucy and Travis 2003; Hain and Neff 2007), insects (Bretman and Tregenza 2005; Simmons et al. 2007; Song et al. 2007), mammals (Burton 2002; Holleley et al. 2006; Gottelli et al. 2007), and birds (Griffith et al. 2002). Our estimate of the rate of mixed paternity broods in this feral population of X. helleri ranged from 0.57 (from allele counting and GERUD) to 0.71 (from PARENTAGE). Given the relatively low power of the microsatellite loci for detecting 2 fathers, our data will have underestimated the true rate of mixed paternity broods in this population. Based on the calculated probability of detecting 2 fathers, the actual frequency of multiple mated females is likely to be as high as 0.84–1.00 (Neff and Pitcher 2002). Rates of mixed paternity broods vary widely among poeciliid fishes (reviewed in Soucy and Travis 2003), including species of Xiphophorus where recorded rates range from 0.33 in X. multilineatus (Luo et al. 2005) to 0.42 in X. variatus (Borowsky and Khouri 1976) and 0.66 in X. maculatus (Borowsky and Kallman 1976). Our global estimate (from all 3 analyses) of the number of sires contributing to the parentage of wild-caught broods (1.74 ± 0.73) is also consistent with the numbers of sires reported from mixed paternity broods from a range of poeciliid fishes (Soucy and Travis 2003).
Our data provide information about genetic mating frequency—the number of fathers contributing toward the parentage of broods—rather than the actual number of mating partners. This is because not all mating partners will necessarily achieve genetic representation in the sperm stores of multiply mated females. Indeed, skewed paternity toward a subset of multiply mated males has been reported in laboratory studies of guppies (Becher and Magurran 2004) and a natural population of the swordtail X. multilineatus (Luo et al. 2005). Our data suggest that the same is true for X. helleri, with paternity being skewed toward a single male in all but 2 of the broods we examined. The average skew of 0.73 across our sample of X. helleri was remarkably similar to the 0.70 reported for X. multilineatus (Luo et al. 2005). Under laboratory conditions, double-mated female guppies rarely produce broods that are sired in equal proportions by both putative sires, and paternity distributions exhibit bimodality and some degree of last-male precedence (Evans and Magurran 2001; Pitcher et al. 2003). In guppies at least, such effects are likely to be influenced by differences in sperm quality between rival males (Evans et al. 2003; Locatello et al. 2006; Pitcher et al. 2007) but are also almost certainly due to female-mediated processes that bias sperm transfer or sperm retention in favor of certain males (Pilastro et al. 2004). As a consequence of such sexually selected processes, our field data for genetic mating frequency are likely to underestimate actual levels of polyandry in the wild.
As in other poeciliids, female swordtails are capable of storing sperm for several months within the ovary and gonoduct (Constantz 1989; Potter and Kramer 2000). Our estimates of genetic mating frequency may therefore include fertilizations due to stored sperm from previous reproductive cycles. Although sperm storage will clearly elevate realized levels of multiple paternity, previous work on other poeciliids shows that fresh sperm have a competitive advantage over previously stored sperm (Hildemann and Wagner 1954). The genetic representation of fertilizations due to stored sperm is therefore likely to be minimal, although this has yet to be demonstrated in X. helleri.
In conclusion, we show that there is the opportunity for postcopulatory sexual selection to occur in X. helleri. In other poeciliid fishes, studies of sperm competition have been facilitated by the development of artificial insemination techniques, which offer unparalleled experimental control over staged double matings to test sperm competition theory (Lodi 1981; Evans et al. 2003). Although Clark (1950) was instrumental in developing this technique in X. helleri, with particular reference to its applicability for sperm competition studies (see Introduction), to date there has been no published account of its use in this context with green swordtails. We anticipate that our field data should stimulate such studies by providing baseline data on the prevalence of polyandry and thus a conservative estimate of the proportion of females mating with more than 1 male (sperm competition risk; Parker 1998) and the number of males that contribute to paternity for polyandrous females (intensity of sperm competition; Parker 1998) in a free-living population.
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This work was funded by grants from the Australian Research Council to LWS and JPE, and by a West Australian Centres of Excellence in Science and Innovation Program to LWS.
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Acknowledgments |
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We thank Cameron Duggin for assistance with fish husbandry.
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Footnotes |
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Corresponding Editor: Steve Karl
Received December 10, 2007
Accepted May 22, 2008
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