Behavioral Ecology Advance Access originally published online on October 3, 2006
Behavioral Ecology 2007 18(1):47-52; doi:10.1093/beheco/arl049
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Phenotypic correlates of spermatozoon quality in the guppy, Poecilia reticulata
Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK
Address correspondence to A.M.J. Skinner. E-mail: amjskinner{at}fsmail.net.
Received 16 January 2006; revised 3 July 2006; accepted 13 August 2006.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The phenotype-linked fertility hypothesis suggests that a female can benefit directly from mate choice when the cues she uses indicate the quantity and/or quality of his spermatozoa. We tested the link between sperm quality and male body size and coloration in the resource-free mating system of the guppy, a tropical fish characterized by strong female choice. Larger males possessed larger testes and are therefore predicted to produce larger numbers of spermatozoa than smaller males. Larger male guppies also produced longer spermatozoa than smaller males. Degree of carotenoid coloration did not predict either the quantity or the quality of a male's spermatozoa. These results are consistent with a previous study that showed that female guppies in the study population prefer larger males to brightly colored males. The male-size directed increase in spermatozoon size may be the result of interplay between sperm competition and the coevolution of spermatozoon traits with the female reproductive tract.
Key words: male size, phenotype-linked fertility, Poecilia reticulata, sperm size, sperm velocity.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Much work on sexual selection has been concerned with understanding the evolution and maintenance of precopulatory (female) mate choice and in particular the possible benefits that females are likely to gain from such behavior (Andersson 1994
). Female choice has been said to evolve because it provides females with direct (material) and/or indirect (genetic) benefits (Kirkpatrick and Ryan 1991; Kokko et al. 2003). Direct benefits may include increased access to resources or a reduction in mating costs, whereas indirect benefits are said to accrue through the increased attractiveness or viability of a female's offspring when mated with a more attractive/fitter male (Kirkpatrick and Ryan 1991).
The guppy, Poecilia reticulata, is a live-bearing poeciliid fish native to Trinidad and Tobago and northern parts of South America and is widely used as a model organism in sexual selection studies due to the conspicuous color patterns and courtship displays that characterize males of this species (Houde 1997). The carotenoid colors are the male phenotypic component most consistently used by females during mate choice (reviewed in Houde 1997), but male size has also been demonstrated to be an important trait for female choice in some wild and feral populations (Reynolds and Gross 1992; Houde 1997; Watt et al. 2001).
The resource-free nature of the guppy mating system has led many to believe that precopulatory female choice of male guppies evolved primarily through the acquisition of indirect genetic benefits to a female's offspring (Houde 1997). However, although a number of studies have presented data that are consistent with the acquisition of genetic benefits, the potential role of direct benefits (e.g., reduced risks of infection and predation), and in particular direct fertility benefits, has not been fully evaluated (Houde 1997).
In birds, it has been suggested that females can gain direct fertility benefits from extrapair copulations if male functional fertility covaries with aspects of the male phenotype used by females in mate choice (Sheldon 1994). However, although little evidence among bird species supports this phenotype-linked fertility hypothesis (Sheldon 1994; Peters et al. 2004), there is growing evidence among fish species that a male's phenotype reflects his underlying fertility (Engen and Folstad 1999; Kortet et al. 2004; Måsvær et al. 2004). In the guppy, male phenotypic traits consistently used by female guppies during mate choice, such as the degree of carotenoid coloration, have been shown to correlate positively with both stripped (Pitcher and Evans 2001) and natural (Pilastro et al. 2002) ejaculate size, as well as with the share of paternity in sperm competition experiments (Evans et al. 2003). However, at present no study has tested empirically whether spermatozoon quality in the guppy is reflected in the male phenotype.
The aim of this paper was to assess whether the phenotypic traits used by female guppies during precopulatory mate choice reflect the underlying quantity and, more importantly, quality of a male's spermatozoa. Spermatozoon quality, defined as the size and velocity of spermatozoa, was examined along with the males' standard length and relative area of carotenoid coloration. Spermatozoon size and motility have been shown to have important roles not only in the fertilization rates of single pair matings (Levitan 2000; Kime et al. 2001; Vladi
et al. 2002) but also in deciding the outcome of sperm competition during multimale matings across a range of taxa (Radwan 1996; Donoghue et al. 1999; Oppliger et al. 2003; Gage et al. 2004).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Experimental animals
Males (n = 65) in this study were descendants of a population of feral fish kept at the University of Leicester Botanical Gardens that originated from a group of 10 males and 10 females introduced to the gardens from Trinidad back in the late 1970s. All males were sexually mature, around 6 months old, and maintained in male-biased (approximately 3:1) mixed-sex aquaria, at 26 ± 1 °C with a 12:12 h light:dark lighting regime. Food consisting of freshly hatched brine shrimp and tropical flake food was provided ad libitum twice a day. Males were isolated from females 3 days prior to ejaculate stripping in order to ensure that spermatozoa reserves were replenished (Pilastro and Bisazza 1999
).
Ejaculate stripping
The ejaculate stripping procedure was as described in Matthews et al. (1997) with 2 exceptions. First, males were anesthetized with a 0.09% solution of 2-phenoxyethanol. Second, the ejaculate was stripped into a drop of guppy saline solution (207 mM NaCl, 5.4 mM KCl, 1.3 mM CaCl2, 0.49 mM MgCl2, 0.41 mM MgSO4, 10 mM Tris (Cl), pH 7.5; Gardiner 1978) placed near the base of the gonopodium. This drop of saline helped draw the spermatozoa away from the body of the fish and also reduced their adhesion to the receptacle on which the fish was being stripped. Male standard length (distance between the tip of the snout and the end of the tail root or caudal peduncle) was also measured during this procedure using manual calipers accurate to 0.02 mm. Spermatozoa were obtained from 57 of the 65 males used in this study.
Assessment of spermatozoon motility
The spermatozoa of the guppy are produced in the form of unencapsulated sperm aggregations known as spermatozeugmata (Constantz 1984). On insemination into the female reproductive tract, the spermatozeugmata show a rapid (approximately 60 s) dissociation into free-swimming spermatozoa, and within 15 min, these spermatozoa migrate to the ovarian cavity (Hamlett WC, Greven H, and Schindler J, unpublished data). The fertilization dynamics of the guppy are poorly understood. The eggs appear to be fertilized over a 2- to 8-day period following parturition of the previous brood (Turner 1937; Thibault and Schultz 1978), but the fate of inseminated spermatozoa during this fertilization period is not known. It is possible that they are temporarily stored until eggs are ready to be fertilized, either within an anterodorsally located region known as the "seminal receptacle" or in narrow invaginations of the ovarian epithelia, called "delles," which penetrate down toward each egg (Jalabert and Billard 1969; Kobayashi and Iwamatsu 2002). It is not clear, however, how the spermatozoa then penetrate through the delle epithelia layers to meet the egg surface (Kobayashi and Iwamatsu 2002).
The speed at which a male's spermatozoa initially dissociate may be important in deciding which spermatozoa reach the delles first and therefore have the best chance of fertilizing an egg. Similarly, the rate at which a male's spermatozoa move following arrival in the delles may further influence their chances of maintaining their position in the delles prior to penetrating the epithelia and reaching the egg surface. Spermatozoon motility measurements were therefore carried out for 15 min from the point of initial activation to mimic the time period during which naturally inseminated spermatozoa are likely to reach and take up position in the delles. Spermatozoon motility was quantified during the first 60 s of activity (the period of initial dissociation described above, hereafter called ID motility) and again 15 min later (the period of ovarian migration described above, hereafter called OM motility).
Spermatozoa were activated using a solution of 150 mM KCl containing dried skimmed milk powder (Marvel, Birmingham, UK; 150 mg per 10 ml of 150 mM KCl). To prevent adhesion of the spermatozoa, glass slides and coverslips were wiped with a water repellent solution (Rain-X, Pennzoil Quaker State Ltd., Bishop's Stortford, UK). The addition of 4 wax "pillars" approximately 0.5 mm thick to the slide prevented a coverslip squashing the spermatozeugma prior to activation.
Spermatozoon motility was recorded on a standard VHS video recorder connected to a Hitachi CCD black and white video camera (Model KP-M1E/K) and an Olympus BX41 negative phase contrast microscope with a X20 negative phase objective. All recordings of motility were carried out at 26 ± 1 °C in order to mimic the body temperature of females in which normal spermatozoa motility would occur and to limit any temperature-mediated changes in spermatozoon motility.
To record ID motility, 10 µl of the activation solution was added to a pretreated glass slide along with an individual spermatozeugma isolated from the guppy saline solution using a pulled and fire-polished glass micropipette (Brand microhaematocrit tubes, Na-hep, 75 mm long) and covered with a coverslip. Filming started once spermatozoa were observed to leave the spermatozeugma and continued for 90 s. Where possible, 3 spermatozeugmata were filmed for each male.
OM motility was recorded by adding 4 spermatozeugmata to a 0.5-ml microfuge tube containing 40 µl of the activation solution. After 15 min, the tube was gently agitated to ensure a homogenous mix of the spermatozoa in the solution without damaging them. A 10-µl sample of the agitated mixture was then removed and added to a pretreated glass slide and filming was started immediately and motility recorded over a 30-s period. Again, where possible 3 replicates were filmed for each male.
Quantifying spermatozoon motility
Spermatozoon motility was quantified using the Hobson Sperm Tracker package (Hobson Tracking Systems Ltd, Sheffield, UK). Kime et al. (2001) recommend that the 3 most useful parameters for assessing spermatozoon motility in fish are 1) the curvilinear velocity (VCL – average velocity [µms–1] measured over the whole track), 2) the straight-line velocity (VSL – average velocity [µms–1] measured over a straight line from the start to the end of the track), and 3) the linearity (LIN – average value of the ratio VSL/VCL [%], which estimates the proximity of the cell's track to a straight line). We found strong correlations among these parameters at each time point, and therefore, only the VSL was used in the subsequent analyses.
ID motility analysis was quantified for 60 s out of the 90-s recording sequences to capture a representative sample of the variation during the dissociation period. OM motility analysis was restricted to the first 15 s of the 30-s recorded period because spermatozeugmata had fully dissociated at this time point.
Assessment of spermatozoon size
Free spermatozoa were obtained by dissociating 10–20 spermatozeugmata from each male in 100–200 µl of activation solution and fixing them in a 5% formalin solution after 15 min. A 5-µl sample of the fixed spermatozoa was placed onto a standard glass slide with a coverslip and left to dry for 10 min. The sample was viewed at 400x magnification using a Leitz Laborlux S microscope, and only spermatozoa that appeared intact without broken flagella or distorted heads/midpieces were selected for analysis. Images of these spermatozoa were captured using an attached Spot CCD camera (Insight QE Model 4.2, Diagnostic Instruments Inc., Sterling Heights, MI) connected to the Leica IM50 image manager software package (Version 1.2, Leica Microsystems AG, Glattbrugg, Switzerland) and measured using the Scion image analysis software (www.scioncorp.com).
We measured the length (µm) of the head, midpiece, and flagellum of the spermatozoa, as well as the areas (µm2) of the head and midpiece region. Twenty spermatozoa were measured for each male (n = 54), except in the case of 3 males where only 19, 19, and 13 spermatozoa were measured, respectively (total of 1131 spermatozoa measured).
Assessment of male phenotype
Approximately 1 month following the ejaculate-stripping procedure, males were euthanased via overanesthetization and body mass (MB) and testes mass (MT) were measured (wet masses accurate to 0.1 mg). Testes mass was used as a surrogate of the size of a male's spermatozoa reserves because the need to use large numbers of spermatozeugmata for other purposes meant that total stripped ejaculate could not be quantified. Still images of each male's right lateral view were also captured using a Vista CCD camera (Model NCL5132DSP) attached to a standard VHS video recorder. Due to fish losses, and the use of some males in another study, body mass and testes mass measurements were obtained from only 37 of the original 57 males.
Still images of each male's lateral view were digitized through an imagenation frame grabber card (Model PXC200A) using the PXCBASIC software provided. Images were analyzed, and the extent of the carotenoid-colored regions of the total lateral body area (excluding fins) were quantified using the Scion image analysis software described previously. Calibration of measurements (in mm2) was carried out using the standard length measurements recorded earlier. To control for any effects of body size, the absolute extent of the carotenoid-colored regions of the body was converted to relative extents by dividing the absolute values by the total lateral body area (excluding fins). The image obtained from one male was of insufficient quality to be able to accurately quantify the degree of carotenoid coloration, and so measurements were made from the remaining 36 males only.
Statistical analysis
All data were checked for normality (Kolmogorov–Smirnov test). As a result, relative body area measures for the carotenoid-colored regions of each male were arcsine square root transformed to increase their approximation to a normal distribution. Comparisons between males for both the size of spermatozoon components and the speed of spermatozoon motility were conducted using nonparametric Kruskal–Wallis tests due to heterogeneity of variance. In addition, the significance of correlation analyses was adjusted for the effects of multiple comparisons using the sequential Bonferroni correction (Rice 1989). All statistical analyses were conducted using SPSS version 11.0.1. Descriptive values where reported are mean ± standard deviation.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Spermatozoon motility parameters
Spermatozoon motility estimates for ID and OM motilities were available for 35 males and 26 males, respectively. This was due to low numbers of spermatozeugmata and the lack of intact spermatozeugmata in the stripped ejaculates of some males.
VSL averaged 94.47 ± 22.84 and 38.54 ± 12.67 µms–1 for the ID and OM motility, respectively. More variation occurred between males than within males for this motility parameter at both time points (ID: H = 53.25, degrees of freedom [df] = 32, P = 0.011; OM: H = 55.01, df = 24, P < 0.001), and so the mean estimates for each male at each time point were used in the subsequent analyses.
Spermatozoon size parameters
Males differed significantly in the mean size of all spermatozoon measures (Table 1). Males with a longer flagellum had significantly shorter midpieces (Table 2; r = –0.48, n = 57, P < 0.001), but midpiece area was significantly larger in males with larger VSL for OM motility (r = 0.58, n = 26, P = 0.002).
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Male phenotype
Male mean length was 17.39 ± 1.67 mm (range 13.38–20.31 mm; n = 57), and mean MB was 82.01 ± 20.82 mg (n = 37). Mean MT of the 37 males measured was 3.51 ± 1.76 mg with a mean gonadosomatic index [GSI: (MT/MB) x 100] of 4.28 ± 1.89. Larger males had larger absolute testes mass than small males (Figure 1). There was, however, no significant difference in GSI between different sized males (r = 0.060, n = 37, P = 0.72).
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Carotenoid-colored patches covered a mean 14.41 ± 4.80% of a male's total body area, but the relative extent of these patches was unrelated to male standard length (r = 0.27, n = 36, P = 0.11) or MT (r = 0.020, n = 36, P = 0.91). VSL was unrelated to male standard length (ID: r = 0.048, n = 35, P = 0.79; OM: r = 0.040, n = 26, P = 0.85) and relative carotenoid area (ID: r = –0.18, n = 28, P = 0.35; OM: r = 0.004, n = 21, P = 0.99).
Correlation analyses were used to investigate whether male phenotypic traits (standard length, relative carotenoid area) were good indicators of the size of each spermatozoon component. There were no significant correlations between the relative size of the carotenoid regions and any of the spermatozoon components measured. However, male standard length correlated positively with both the length of the flagellum (Table 3; r = 0.37, n = 57, P = 0.005) and the total length of the spermatozoon (Figure 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Male size was found to be a good predictor of both the potential size of a male's spermatozoa reserves and also the length of the spermatozoa contained within those reserves, with larger males producing larger numbers and longer spermatozoa than smaller males. There was no relationship between either the potential size or the quality of the spermatozoa reserves and the relative size of a male's carotenoid-colored area. Male size therefore better predicted a male's potential fertility than carotenoid coloration, consistent with the evidence that females in this population show preferences for large males rather than brightly colored males (Watt et al. 2001
).
The number of spermatozoa in the stripped ejaculate of the guppy has been shown previously to correlate with a number of aspects of male phenotype, including body size (Kuckuck and Greven 1997; Pilastro and Bisazza 1999; Pitcher and Evans 2001). Mature fish testes consist mainly of spermatozoon cells (Billard 1986), and so it is generally assumed that testes mass will be a good indicator of the number of spermatozoa produced, as has been shown in a number of fish species (Marconato and Shapiro 1996; Zbinden et al. 2001) including the guppy (Haubruge et al. 2000). Relative testes mass (measured here as GSI) is predicted to increase with sperm competition risk and/or intensity (Parker 1998), and comparative studies have demonstrated this across species of fish (Stockley et al. 1997), birds (Birkhead 1998), and mammals (Gomendio et al. 1998). In the present study, however, the lack of a correlation between male standard length and GSI implies that sperm competition intensity does not differ across the range of male sizes studied and is therefore unlikely to explain the male-size directed increases in either spermatozoa number or size.
Spermatozoon size is predicted to evolve around narrow optima under the influence of natural selection and/or sexual selection and can be best explained by the marginal value theorem (Parker 1993). For example, in the moth Plodia interpunctella, when nutritional resources are limited, males maintain spermatozoon size but alter spermatozoa numbers, suggesting the former spermatozoon trait is more critical to fitness (Gage and Cook 1994). Similarly, sperm competition theory predicts that under increasing levels of sperm competition risk/intensity, the size of spermatozoa will remain the same but the number of spermatozoa will increase (Parker 1993). However, spermatozoon size can either increase or decrease under increasing levels of sperm competition depending on the mode of fertilization and how spermatozoon size affects spermatozoon longevity (Parker 1998). Although comparative studies across species have demonstrated both positive (birds, Briskie et al. 1997; frogs, Byrne et al. 2003; butterflies, Gage 1994; mammals, Gomendio and Roldan 1991; moths, Morrow and Gage 2000) and negative (fish, Stockley et al. 1997) effects of increasing sperm competition on spermatozoon size, within species there has generally been less evidence of any sperm competition effect (Simmons et al. 1999; LaMunyon and Ward 2002).
The female reproductive tract may also have important influences on the size of a male's spermatozoa, particularly under sperm competition (Briskie and Montgomerie 1992; Morrow and Gage 2000; Miller and Pitnick 2002; Pitnick et al. 2003). For instance, the dimensions of a female's reproductive tract are likely to influence whether large spermatozoa are competitively advantaged (through increased swimming speed; Gomendio and Roldan 1991) or disadvantaged (through reduced longevity; Gomendio and Roldan 1993), relative to smaller spermatozoa. Furthermore, increasing the size of the spermatozoon storage vessel (seminal receptacle) in female fruit flies, Drosophila melanogaster, can lead to an increase in the size of a male's spermatozoa through postcopulatory female choice favoring large spermatozoa (Miller and Pitnick 2002). It is possible that a similar mechanism maintains the male-size directed increase in spermatozoon size observed in this study.
Large male guppies produce offspring with faster growth rates in at least one guppy population (Reynolds and Gross 1992). If large male guppies also possess larger spermatozoa, as suggested here, and these are competitively advantaged, then female preference for large males is likely to also select for an increase in spermatozoon size. Larger males will produce larger females, which will in turn select for males with larger spermatozoa. However, for this mechanism to operate, 2 assumptions must be met. First, larger males must produce larger spermatozoa. Second, larger spermatozoa must be at a competitive advantage when competing against smaller spermatozoa.
Theory suggests that longer spermatozoa will produce larger propulsive forces and swim faster (Katz and Drobnis 1990), though supporting empirical data are lacking (but see Gomendio and Roldan 1991; Casselman and Montgomerie 2004). Evidence from a range of taxa suggests, however, that both the size (Radwan 1996; Oppliger et al. 2003) and motility (Donoghue et al. 1999; Gage et al. 2004) of spermatozoa can influence their relative success during sperm competition, with larger/faster swimming spermatozoa outcompeting their smaller/slower competitors.
The assumption that larger males produce longer spermatozoa is harder to justify. The available evidence suggests that spermatozoon size is not condition dependent (Gage and Cook 1994; Hellriegel and Blanckenhorn 2002), and so it is unlikely that larger male guppies are simply in better condition. Because guppies exhibit XY sex determination with males as the heterogametic sex (Volff and Schartl 2001), spermatozoon size could be sex linked, as suggested for other species (Ward 2000; Morrow and Gage 2001; Simmons and Kotiaho 2002). Furthermore, body size in guppies shows significant father–son heritability (Reynolds and Gross 1992), and heritability estimates are sufficiently high to suggest Y-linked inheritance (Nakajima and Taniguchi 2002). Perhaps, genes conferring males with large spermatozoa are closely associated with or are the same genes on the Y chromosome that control male body size. Female preference for large male size could therefore indirectly select for males with large spermatozoon size, particularly if such spermatozoa are competitively advantaged.
We found no correlations between spermatozoon quality or quantity and the relative area of carotenoid coloration, implying that this coloration is a poor indicator of a male's potential fertility. This result is somewhat surprising given the consistent preference shown by female guppies for carotenoid coloration (Houde 1997). Guppy color patterns have evolved under the conflicting forces of natural (predation) selection and sexual selection, with males from high-predation environments evolving fewer and smaller color spots (Houde 1997). In addition, carotenoid availability in the environment is thought to further limit the expression of carotenoid-based color patches (Grether et al. 1999). Athough carotenoids in the diet do not affect the area of carotenoid coloration in guppies, they do affect the color saturation, or chroma, of these colors (Grether 2000). Furthermore, the chroma of carotenoid-colored regions is also an important component used during mate choice in the guppy (Kodric-Brown 1989). It is possible, therefore, that we might have found different results had we measured the chroma of carotenoid patches.
Previous work on the study population has, however, found no female preference for either the relative area of carotenoid-colored patches or their chroma (Watt et al. 2001). Grether (2000) suggested that the indicator value of carotenoid ornaments should be higher in environments with limited carotenoid availability because increases in carotenoid uptake can produce considerable increases in the chroma of carotenoid-based ornaments. In contrast, in environments with high carotenoid availability, an increase in carotenoid uptake leads to little change in the chroma of carotenoid-based ornaments (Grether 2000). It is therefore possible that the population used in this study has sufficiently high carotenoid availability to render the carotenoid ornament of little value in conveying information to females. No data are available on carotenoid availability in this population to test this idea.
The results discussed here suggest a potential direct fertility benefit to female choice of male size in the present study population, a fact hitherto unknown in this resource-free mating system. Females in the study population prefer larger males to brightly colored males (Watt et al. 2001), and here we show that male size was a better predictor of both the potential size of spermatozoa reserves and the total length of spermatozoa contained within those reserves, than the degree of carotenoid coloration. The idea that a male's phenotype may reflect the underlying quality of his spermatozoa has important implications for the mating system of the guppy because it provides a potential mechanism by which females can ensure their offspring are sired by the male of their choice (i.e., if males favored during precopulatory mate choice are also favored during postcopulatory sperm competition). Given that sexual selection theory suggests that direct selection on female mating preferences is a relatively greater force than indirect selection (Kirkpatrick and Barton 1997; Kokko et al. 2003), we believe that direct fertility benefits in the guppy deserve further attention before we can fully understand the evolution of this model mating system.
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ACKNOWLEDGEMENTS |
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We thank Terry Burke and Klaus Reinhardt for helpful and constructive comments on an earlier draft of this manuscript. We would also like to thank Tim Birkhead for the loan of equipment and valuable advice. All work was conducted under Home Office License PPL40/2520 and supported by a University of Sheffield studentship awarded to A.M.J.S.
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