No evidence for a trade‐off between sperm length and male premating weaponry

Male ornaments and armaments that mediate success in mate acquisition and ejaculate traits influencing competitive fertilization success are under intense sexual selection. However, relative investment in these pre‐ and post‐copulatory traits depends on the relative importance of either selection episode and on the energetic costs and fitness gains of investing in these traits. Theoretical and empirical work has improved our understanding of how precopulatory sexual traits and investments in sperm production covary in this context. It has recently also been suggested that male weapon size may trade off with sperm length as another post‐copulatory sexual trait, but the theoretical framework for this suggestion remains unclear. We evaluated the relationship between precopulatory armaments and sperm length, previously reported in ungulates, in five taxa as well as meta‐analytically. Within and between taxa, we found no evidence for a negative or positive relationship between sperm length and male traits that are important in male–male contest competition. It is important to consider pre‐ and post‐copulatory sexual selection together to understand fitness, and to study investments in different reproductive traits jointly rather than separately. A trade‐off between pre‐ and post‐copulatory sexual traits may not manifest itself in sperm length but rather in sperm number or function. Particularly in large‐bodied taxa such as ungulates, sperm number is more variable interspecifically and likely to be under more intense selection than sperm length. We discuss our and the previous results in this context.     

Do male secondary sexual characters signal ejaculate quality? A meta‐analysis

There are two reasons why researchers are interested in the phenotypic relationship between the expression of male secondary sexual characters (SSCs) and ‘ejaculate quality’ (defined as sperm/ejaculate traits that are widely assumed to increase female fertility and/or sperm competitiveness). First, if the relationship is positive then females could gain a direct benefit by choosing more attractive males for fertility assurance reasons (‘the phenotype‐linked fertility’ hypothesis). Second, there is much interest in the direction of the correlation between traits favoured by pre‐copulatory sexual selection (i.e. affecting mating success) and those favoured by post‐copulatory sexual selection (i.e. increasing sperm competitiveness). If the relationship is negative this could lead to the two forms of selection counteracting each other. Theory predicts that the direction of the relationship could be either positive or negative depending on the underlying genetic variance and covariance in each trait, the extent of variation among males in condition (resources available to allocate to reproductive traits), and variation among males in the cost or rate of mating. We conducted a meta‐analysis to determine the average relationship between the expression of behavioural and morphological male secondary sexual characters and four assays of ejaculate quality (sperm number, viability, swimming speed and size). Regardless of how the data were partitioned the mean relationship was consistently positive, but always statistically non‐significant. The only exception was that secondary sexual character expression was weakly but significantly positively correlated with sperm viability (r = 0.07, P < 0.05). There was no significant difference in the strength or direction of the relationship between behavioural and morphological SSCs, nor among relationships using the four ejaculate quality assays. The implications of our findings are discussed.     

Sperm competition and ejaculate economics

Sperm competition was identified in 1970 as a pervasive selective force in post‐copulatory sexual selection that occurs when the ejaculates of different males compete to fertilise a given set of ova. Since then, sperm competition has been much studied both empirically and theoretically. Because sperm competition often favours large ejaculates, an important challenge has been to understand the evolution of strategies through which males invest in sperm production and economise sperm allocation to maximise reproductive success under competitive conditions. Sperm competition mechanisms vary greatly, depending on many factors including the level of sperm competition, space constraints in the sperm competition arena, male mating roles, and female influences on sperm utilisation. Consequently, theoretical models of ejaculate economics are complex and varied, often with apparently conflicting predictions. The goal of this review is to synthesise the theoretical basis of ejaculate economics under sperm competition, aiming to provide empiricists with categorised model assumptions and predictions. We show that apparent contradictions between older and newer models can often be reconciled and there is considerable consensus in the predictions generated by different models. We also discuss qualitative empirical support for some of these predictions, and detail quantitative matches between predictions and observations that exist in the yellow dung fly. We argue that ejaculate economic theory represents a powerful heuristic to explain the diversity in ejaculate traits at multiple levels: across species, across males and within individual males. Future progress requires greater understanding of sperm competition mechanisms, quantification of trade‐offs between ejaculate allocation and numbers of matings gained, further knowledge of mechanisms of female sperm selection and their associated costs, further investigation of non‐sperm ejaculate effects, and theoretical integration of pre‐ and post‐copulatory episodes of sexual selection.     

Colourful male guppies produce faster and more viable sperm

In guppies (Poecilia reticulata) precopulatory sexual selection (via female choice) and post-copulatory selection (via sperm competition) both favour males with relatively high levels of carotenoid (orange) pigmentation, suggesting that colourful males produce more competitive ejaculates. Here we test whether there is a positive association between male orange pigmentation and sperm quality. Our analysis of sperm quality focused on sperm swimming speeds (using CASA: computer-assisted sperm analysis to estimate three parameters of sperm velocity in vitro), sperm viability (proportion of live sperm per stripped ejaculate) and sperm lengths. We found that males with relatively large areas of orange pigmentation had significantly faster and more viable sperm than their less ornamented counterparts, suggesting a possible link between dietary carotenoid intake and sperm quality. By contrast, we found no relationship between sperm length (head length and total sperm length) and male phenotype. These findings, in conjunction with previous work showing that highly ornamented male guppies sire higher quality offspring, suggest that female preference for colourful males and sperm competition work in concert to favour intrinsically higher quality males.     

The copulatory plug delays ejaculation by rival males and affects sperm competition outcome in house mice

Females of many species mate with multiple males (polyandry), resulting in male–male competition extending to post‐copulation (sperm competition). Males adapt to such post‐copulatory sexual selection by altering features of their ejaculate that increase its competitiveness and/or by decreasing the risk of sperm competition through female manipulation or interference with rival male behaviour. At ejaculation, males of many species deposit copulatory plugs, which are commonly interpreted as a male adaptation to post‐copulatory competition and are thought to reduce or delay female remating. Here, we used a vertebrate model species, the house mouse, to study the consequences of copulatory plugs for post‐copulatory competition. We experimentally manipulated plugs after a female's first mating and investigated the consequences for rival male behaviour and paternity outcome. We found that even intact copulatory plugs were ineffective at preventing female remating, but that plugs influenced the rival male copulatory behaviour. Rivals facing intact copulatory plugs performed more but shorter copulations and ejaculated later than when the plug had been fully or partially removed. This suggests that the copulatory plug represents a considerable physical barrier to rival males. The paternity share of first males increased with a longer delay between the first and second males' ejaculations, indicative of fitness consequences of copulatory plugs. However, when males provided little copulatory stimulation, the incidence of pregnancy failure increased, representing a potential benefit of intense and repeated copulation besides plug removal. We discuss the potential mechanisms of how plugs influence sperm competition outcome and consequences for male copulatory behaviour.     

Impaired sperm quality,delayed mating but no costs for offspring fitness in crickets winning a fight

The outcome of male–male contest competition is known to affect male mating success and is believed to confer fitness benefits to females through preference for dominant males. However, by mating with contest winners, females can incur significant costs spanning from decreased fecundity to negative effects on offspring. Hence, identifying costs and benefits of male dominance on female fitness is crucial to unravel the potential for a conflict of interests between the sexes. Here, we investigated males' pre‐ and post‐copulatory reproductive investment and its effect on female fitness after a single contest a using the field cricket Gryllus bimaculatus. We allowed males to fight and immediately measured their mating behaviour, sperm quality and offspring viability. We found that males experiencing a fight, independently of the outcome, delayed matings, but their courtship effort was not affected. However, winners produced sperm of lower quality (viability) compared to losers and to males that did not experience fighting. Results suggest a trade‐off in resource allocation between pre‐ and post‐mating episodes of sexual selection. Despite lower ejaculate quality, we found no fitness costs (fecundity and viability of offspring) for females mated to winners. Overall, our findings highlight the importance of considering fighting ability when assessing male reproductive success, as winners may be impaired in their competitiveness at a post‐mating level.     

Evolutionary change in testes tissue composition among experimental populations of house mice

Theory assumes that postcopulatory sexual selection favors increased investment in testes size because greater numbers of sperm within the ejaculate increase the chance of success in sperm competition, and larger testes are able to produce more sperm. However, changes in the organization of the testes tissue may also affect sperm production rates. Indeed, recent comparative analyses suggest that sperm competition selects for greater proportions of sperm‐producing tissue within the testes. Here, we explicitly test this hypothesis using the powerful technique of experimental evolution. We allowed house mice (Mus domesticus) to evolve via monogamy or polygamy in six replicate populations across 24 generations. We then used histology and image analysis to quantify the proportion of sperm‐producing tissue (seminiferous tubules) within the testes of males. Our results show that males that had evolved with sperm competition had testes with a higher proportion of seminiferous tubules compared with males that had evolved under monogamy. Previously, it had been shown that males from the polygamous populations produced greater numbers of sperm in the absence of changes in testes size. We thus provide evidence that sperm competition selects for an increase in the density of sperm‐producing tissue, and consequently increased testicular efficiency.     

Song and Sperm in Crickets: A Trade‐off between Pre‐ and Post‐copulatory Traits or Phenotype‐Linked Fertility?

When females mate multiply (polyandry) both pre‐ and post‐copulatory sexual selection can occur. Sperm competition theory predicts there should be a trade‐off between investment in attracting mates and investment in ejaculate quality. In contrast, the phenotype‐linked fertility hypothesis predicts a positive relationship should exist between investment in attracting mates and investment in ejaculate quality. Given the need to understand how pre‐ and post‐copulatory sexual selection interacts, we investigated the relationship between secondary sexual traits and ejaculate quality using the European house cricket, Acheta domesticus. Although we found no direct relationship between cricket secondary sexual signals and ejaculate quality, variation in ejaculate quality was dependent on male body weight and mating latency: the lightest males produced twice as many sperm as the heaviest males but took longer to mate with females. Our findings are consistent with current theoretical models of sperm competition. Given light males may have lower mating success than heavy males because females take longer to mate with them in no‐choice tests, light males may be exhibiting an alternative reproductive tactic by providing females with more living sperm. Together, our findings suggest that the fitness of heavy males may depend on pre‐copulatory sexual selection, while the fitness of light males may depend on post‐copulatory fertilization success.     

Methyl eugenol effects on Bactrocera dorsalis male total body protein,reproductive organs and ejaculate

Methyl eugenol (ME) and inclusion of protein into the adult diet increase the mating competitiveness of the Oriental fruit fly, Bactrocera dorsalis (Hendel). Exposing males to ME or protein is a promising post‐teneral treatment for males being released in the sterile insect technique (SIT). However, the effect of this post‐teneral treatment on male reproductive organs or the male ejaculate is unknown. During mating, males transfer sperm and accessory gland products (AGPs) to females and these compounds are reported to modulate female sexual inhibition. We studied the impact of male exposure to ME and a yeast hydrolysate (YH) diet on the protein reserves of males, male reproductive organ size, and the male ejaculate through sperm and AGPs. We show that males exposed to ME regardless of access to YH accumulated a greater amount of whole body protein. Males fed on YH also had increased total body protein and had bigger reproductive organs than YH‐deprived males, but no apparent effect of ME exposure was observed on reproductive organ size. Females stored less sperm when mated with males fed on YH and ME compared to males not fed on ME. YH and ME had no effect on male AGPs. Females injected with AGPs of males fed on YH and exposed to ME were just as likely to mate as females injected with AGPs of non‐treated males. However, females injected with AGPs of males exposed to ME mated faster than females injected with AGPs of non‐exposed males. We conclude that while exposure to ME increases male copulatory success and protein reserves in the male body, there seem to be some potential trade‐offs such as lower sperm stored by females. We discuss our results in terms of pre‐release protocols that may be used for B. dorsalis in SIT application.     

Assessing the potential for post‐ejaculatory female choice in a polyandrous beach‐spawning fish

In species with limited opportunities for pre‐ejaculatory sexual selection (behavioural components), post‐ejaculatory mechanisms may provide opportunities for mate choice after gametes have been released. Recent evidence from a range of taxa has revealed that cryptic female choice (i.e., female‐mediated differential fertilization bias), through chemical cues released with or from eggs, can differentially regulate the swimming characteristics of sperm from various males and ultimately determine male fertilization success under sperm competition. We assessed the potential role that such female‐modulated chemical cues play in influencing sperm swimming characteristics in beach‐spawning capelin (Mallotus villosus), an externally fertilizing fish that mates as couples (one male and one female) or threesomes (two males and one female) with presumably limited opportunities for pre‐ejaculatory sexual selection. We assayed sperm swimming characteristics under varying doses and donor origins of egg cues and also examined the possibility of assortative mating based on body size. We found mating groups were not associated by size, larger males did not produce better quality ejaculates, and egg cues (regardless of dosage or donor identity) did not influence sperm swimming characteristics. Our findings suggest that intersexual pre‐ejaculatory sexual selection and cryptic female choice mediated by female chemical cues are poorly developed in capelin, possibly due to unique natural selection constraints on reproduction.     

The effects of male social environment on sperm phenotype and genome integrity

Sperm function and quality are primary determinants of male reproductive performance and hence fitness. The presence of rival males has been shown to affect ejaculate and sperm traits in a wide range of taxa. However, male physiological conditions may not only affect sperm phenotypic traits but also their genetic and epigenetic signatures, affecting the fitness of the resulting offspring. We investigated the effects of male‐male competition on sperm quality using TUNEL assays and geometric morphometrics in the zebrafish, Danio rerio. We found that the sperm produced by males exposed to high male–male competition had smaller heads but larger midpiece and flagellum than sperm produced by males under low competition. Head and flagella also appeared less sensitive to the osmotic stress induced by activation with water. In addition, more sperm showed signals of DNA damage in ejaculates of males under high competition. These findings suggest that the presence of a rival male may have positive effects on sperm phenotypic traits but negative effects on sperm DNA integrity. Overall, males facing the presence of rival males may produce faster swimming and more competitive sperm but this may come at a cost for the next generation.     

Male age and its association with reproductive traits in captive and wild house sparrows

Evolutionary theory predicts that females seek extra‐pair fertilizations from high‐quality males. In socially monogamous bird species, it is often old males that are most successful in extra‐pair fertilizations. Adaptive models of female extra‐pair mate choice suggest that old males may produce offspring of higher genetic quality than young males because they have proven their survivability. However, old males are also more likely to show signs of reproductive senescence, such as reduced sperm quality. To better understand why old males account for a disproportionally large number of extra‐pair offspring and what the consequences of mating with old males are, we compared several sperm traits of both captive and wild house sparrows, Passer domesticus. Sperm morphological traits and cloacal protuberance volume (a proxy for sperm load) of old and young males did not differ substantially. However, old males delivered almost three times more sperm to the female's egg than young males. We discuss the possibility of a post‐copulatory advantage for old over young males and the consequences for females mated with old males.     

The evolution of gonad expenditure and gonadosomatic index (GSI) in male and female broadcast‐spawning invertebrates

Sedentary broadcast‐spawning marine invertebrates, which release both eggs and sperm into the water for fertilization, are of special interest for sexual selection studies. They provide unique insight into the early stages of the evolutionary succession leading to the often‐intense operation of both pre‐ and post‐mating sexual selection in mobile gonochorists. Since they are sessile or only weakly mobile, adults can interact only to a limited extent with other adults and with their own fertilized offspring. They are consequently subject mainly to selection on gamete production and gamete success, and so high gonad expenditure is expected in both sexes. We review literature on gonadosomatic index (GSI; the proportion of body tissue devoted to gamete production) of gonochoristic broadcast spawners, which we use as a proxy for gonad expenditure. We show that such taxa most often have a high GSI that is approximately equal in both sexes. When GSI is asymmetric, female GSI usually exceeds male GSI, at least in echinoderms (the majority of species recorded). Intriguingly, though, higher male GSI also occurs in some species and appears more common than female‐biased GSI in certain orders of gastropod molluscs. Our limited data also suggest that higher male GSI may be the prevalent pattern in sperm casters (where only males release gametes). We explore how selection might have shaped these patterns using game theoretic models for gonad expenditure that consider possible trade‐offs with (i) somatic maintenance or (ii) growth, while also considering sperm competition, sperm limitation, and polyspermy. Our models of the trade‐off between somatic tissue (which increases survival) and gonad (which increases reproductive success) predict that GSI should be equal for the two sexes when sperm competition is intense, as is probably common in broadcast spawners due to synchronous spawning in aggregations. Higher female GSI occurs under low sperm competition. Sperm limitation appears unlikely to alter these conclusions qualitatively, but can also act as a force to keep male GSI high, and close to that of females. Polyspermy can act to reduce male GSI. Higher male than female GSI is predicted to be less common (as observed in the data), but can occur when ova/ovaries are sufficiently more resource‐intensive to produce than sperm/testes, for which some evidence exists. We also show that sex‐specific trade‐offs between gonads and growth can generate different life‐history strategies for males and females, with males beginning reproduction earlier. This could lead to apparently higher male GSI in empirical studies if immature females are included in calculations of mean GSI. The existence of higher male GSI nonetheless remains somewhat problematic and requires further investigation. When sperm limitation is low, we suggest that the natural logarithm of the male/female GSI ratio may be a suitable index for sperm competition level in broadcast spawners, and that this may also be considered as an index for internally fertilizing taxa.     

Influence of male courtship intensity and male–male competition on paternity distribution in Hermann's tortoise,Testudo hermanni hermanni (Chelonia: Testudinidae)

Honest‐advertisement models of sexual selection suggest that condition‐dependent male secondary sexual characters could function as reliable signals of male quality, enabling females to discriminate among potential partners, both in the pre‐ and post‐copulatory phases. In this context, many studies have revealed the importance of promiscuous mating systems and female sperm storage in determining the occurrence of such a model of sexual selection. By contrast, few studies have investigated the presence and extent of post‐copulatory female choice in chelonian species. The present study aimed to investigate the effect of male size, male–male competition, and courtship intensity on paternity distribution in Testudo hermanni hermanni, combining behavioural and genetic data. We created experimental groups composed of two males of different sizes and three or four randomly selected females. Observations conducted during social interactions between males revealed that a hierarchy, unrelated to male size, was soon established: Alpha males were more aggressive towards competitors and courted females more intensively. Alpha males also achieved a higher mounting success than Beta males. Paternity analysis performed on hatchlings produced from experimental females revealed that male reproductive success was not correlated with male–female size ratio. Finally, despite the higher mounting success of Alpha males, paternity analysis revealed that male reproductive success did not differ between Alpha and Beta males. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 656–667.     

Positive correlations between pre‐ and post‐copulatory sexual traits in warblers

Theoretical models predict that investment in pre‐copulatory and post‐copulatory sexually selected traits should trade‐off. At the macroevolutionary scale, the majority of studies to date have focused on male weaponry as the target of pre‐copulatory sexual selection, but the trade‐off should equally apply to traits used to attract females, such as bird song and plumage. We studied the Old World leaf warblers (Phylloscopidae), a group of socially monogamous songbirds that experience relatively high levels of sperm competition. We examined the relationships between song duration and number of elements in the song with sperm length across 21 species, and between the same song variables and combined testes mass in a subset of these species (n = 10). Across species, these song variables and testes mass/sperm length were generally positively correlated, albeit not statistically significantly so or with borderline significance. In contrast to theory, we found no evidence for negative associations between pre‐ and post‐copulatory traits. We argue that this is a consequence of males of some species investing more into overall fertilization success (i.e. the sum of pre‐ and post‐copulatory sexual selection) than males of other species, and high fertilization success is achieved through investment into both mate attraction and sperm competition.     

Sperm morphology and evidence for sperm competition among parrots

Sperm competition is an important component of post‐copulatory sexual selection that has shaped the evolution of sperm morphology. Previous studies have reported that sperm competition has a concurrently directional and stabilizing effect on sperm size. For example, bird species that show higher levels of extrapair paternity and larger testes (proxies for the intensity of sperm competition) have longer sperm and lower coefficients of variation in sperm length, both within and between males. For this reason, these sperm traits have been proposed as indexes to estimate the level of sperm competition in species for which other measures are not available. The relationship between sperm competition and sperm morphology has been explored mostly for bird species that breed in temperate zones, with the main focus on passerine birds. We measured sperm morphology in 62 parrot species that breed mainly in the tropics and related variation in sperm length to life‐history traits potentially indicative of the level of sperm competition. We showed that sperm length negatively correlated with the within‐male coefficient of variation in sperm length and positively with testes mass. We also showed that sperm is longer in sexually dichromatic and in gregarious species. Our results support the general validity of the hypothesis that sperm competition drives variation in sperm morphology. Our analyses suggest that post‐copulatory sexual selection is also important in tropical species, with more intense sperm competition among sexually dichromatic species and among species that breed at higher densities.     

Developmental temperature affects the expression of ejaculatory traits and the outcome of sperm competition in Callosobruchus maculatus

The outcome of post‐copulatory sexual selection is determined by a complex set of interactions between the primary reproductive traits of two or more males and their interactions with the reproductive traits of the female. Recently, a number of studies have shown the primary reproductive traits of both males and females express phenotypic plasticity in response to the thermal environment experienced during ontogeny. However, how plasticity in these traits affects the dynamics of sperm competition remains largely unknown. Here, we demonstrate plasticity in testes size, sperm size and sperm number in response to developmental temperature in the bruchid beetle Callosobruchus maculatus. Males reared at the highest temperature eclosed at the smallest body size and had the smallest absolute and relative testes size. Males reared at both the high‐ and low‐temperature extremes produced both fewer and smaller sperm than males reared at intermediate temperatures. In the absence of sperm competition, developmental temperature had no effect on male fertility. However, under conditions of sperm competition, males reared at either temperature extreme were less competitive in terms of sperm offence (P₂), whereas those reared at the lowest temperature were less competitive in terms of sperm defence (P₁). This suggests the developmental pathways that regulate the phenotypic expression of these ejaculatory traits are subject to both natural and sexual selection: natural selection in the pre‐ejaculatory environment and sexual selection in the post‐ejaculatory environment. In nature, thermal heterogeneity during development is commonplace. Therefore, we suggest the interplay between ecology and development represents an important, yet hitherto underestimated component of male fitness via post‐copulatory sexual selection.     

Female Remating Behavior in a Lekking Moth

In polyandrous species, male reproductive success will at least partly be determined by males' success in sperm competition. To understand the potential for post‐mating sexual selection, it is therefore important to assess the extent of female remating. In the lekking moth Achroia grisella, male mating success is strongly determined by female choice based on the attractiveness of male ultrasonic songs. Although observations have indicated that some females will remate, only little is known about the level of sperm competition. In many species, females are more likely to remate if their first mating involved an already mated male than if the first male was virgin. Potentially, this is because mated males are less well able to provide an adequate sperm supply, nutrients, or substances inhibiting female remating. This phenomenon will effectively reduce the strength of pre‐copulatory sexual selection because attractive males with high mating success will be more susceptible to sperm competition. We therefore performed an experiment designed both to provide a more precise estimate of female remating probability and simultaneously to test the hypothesis that female remating is influenced by male mating history. Overall, approximately one of five females remated with a second male. Yet, although females mated to non‐virgin males were somewhat more prone to remate, the effect of male mating history was not significant. The results revealed, however, that heavier females were more likely to remate. Furthermore, we found that females' second copulations were longer, suggesting that, in accordance with theory, males may invest more sperm in situations with an elevated risk of sperm competition.     

Condition‐dependent ejaculate production affects male mating behavior in the common bedbug Cimex lectularius

Food availability in the environment is often low and variable, constraining organisms in their resource allocation to different life‐history traits. For example, variation in food availability is likely to induce condition‐dependent investment in reproduction. Further, diet has been shown to affect ejaculate size, composition and quality. How these effects translate into male reproductive success or change male mating behavior is still largely unknown. Here, we concentrated on the effect of meal size on ejaculate production, male reproductive success and mating behavior in the common bedbug Cimex lectularius. We analyzed the production of sperm and seminal fluid within three different feeding regimes in six different populations. Males receiving large meals produced significantly more sperm and seminal fluid than males receiving small meals or no meals at all. While such condition‐dependent ejaculate production did not affect the number of offspring produced after a single mating, food‐restricted males could perform significantly fewer matings than fully fed males. Therefore, in a multiple mating context food‐restricted males paid a fitness cost and might have to adjust their mating strategy according to the ejaculate available to them. Our results indicate that meal size has no direct effect on ejaculate quality, but food availability forces a condition‐dependent mating rate on males. Environmental variation translating into variation in male reproductive traits reveals that natural selection can interact with sexual selection and shape reproductive traits. As males can modulate their ejaculate size depending on the mating situation, future studies are needed to elucidate whether environmental variation affecting the amount of ejaculate available might induce different mating strategies.     

Relationship between pre‐ and post‐copulatory traits in Salvator rufescens (Squamata: Teiidae)

Understanding pre‐ and post‐copulatory mechanisms of sexual selection can provide insights into the evolution of male reproductive strategies. The phenotype‐linked fertility hypothesis postulates that male sperm quality and secondary sexual characteristics will positively co‐vary, whereas the sperm competition hypothesis predicts a negative association between those traits. Male reproductive traits often show variation throughout the reproductive period, suggesting that the relationship between pre‐ and post‐copulatory sexual selection may vary temporally. Here, we evaluated the relationship between secondary sexual character and sperm traits and its temporal variation in Salvator rufescens, a south American lizard. We observed a negative relationship between jaw muscle and principal piece length of sperm and a variation in the relationship between pre‐ and post‐copulatory traits throughout the reproductive period. Collectively, our results evidenced a trade‐off between pre‐ and post‐copulatory traits and a strong seasonal flexibility of male reproductive strategies in this lizard species.