Male Reproductive Investment Research Articles

Crowd control: sex ratio affects sexually selected cuticular hydrocarbons in male Drosophila serrata.

Although it is advantageous for males to express costly sexually selected signals when females are present, they may also benefit from suppressing these signals to avoid costly interactions with rival males. Cuticular chemical profiles frequently function as insect sexual signals; however, few studies have asked whether males alter these signals in response to their social environment. In Drosophila serrata, an Australian fly, there is sexual selection for a multivariate combination of male cuticular hydrocarbons (CHCs). Here, we show that the ratio of females to males that an adult male experiences has a strong effect on his CHC expression, with female-biased adult sex ratios eliciting greater expression of CHC profiles associated with higher male mating success. Classical models predict that male reproductive investment should be highest when there is a small but nonzero number of rivals, but we found that males expressed the most attractive combination of CHCs when there were no rivals. We found that male CHCs were highly sensitive to adult sex ratio, with males expressing higher values of CHC profiles associated with greater mating success as the ratio of females to males increased. Moreover, sex ratio has a stronger effect on male CHC expression than adult density. Finally, we explore whether sex ratio affects the variance among a group of males in their CHC expression, as might be expected if individuals respond differently to a given social environment, but find little effect. Our results reveal that subtle differences in social environment can induce plasticity in male chemical signal expression.

Altitudinal variation in somatic condition and reproductive investment of male Yunnan pond frogs (Dianrana pleuraden)

Comparisons between populations that differ in resource availability and in environmental variables affecting the intensity of male–male competition allow insights into the mechanisms shaping reproductive allocation. Here, we studied inter-population variation in male investments in testis size and sperm length across four populations of the Yunnan pond frog (Dianrana pleuraden) along an altitudinal gradient in western China. Male body condition, relative testis size and sperm length did not increase with altitude despite an increasing male bias in the operational sex ratio (OSR) in high altitude was recorded. Our results were inconsistent with previous prediction that increasing latitude and/or altitude should lead to a declining male reproductive investment in anurans due to shortening breeding seasons and declining resource availability. We found a positive correlation between body condition and testes mass along the altitudinal gradient, which was indicative of a condition-dependent expression of testis size. By contrast, we recorded a non-significant correlation between testes mass and OSR, suggesting that male–male competition did not result in increasing levels of sperm competition. A non-significant correlation between sperm length and testis mass suggested that the intensity of sperm competition can account for the variation in sperm length.

Altitude underlies variation in the mating system, somatic condition, and investment in reproductive traits in male Asian grass frogs (Fejervarya limnocharis)

There is substantial comparative and growing experimental evidence that the competition for fertilization among sperm from different males can drive variation in male reproductive investments. However, less is known about the extent of natural variation in these investments relative to environmental variables affecting resource availability and mating system dynamics, which would allow insights into the mechanisms shaping reproductive allocation. Here, we studied interpopulation variation in male investments in testis size and sperm length across 25 populations of the Asian grass frog Fejervarya limnocharis along a 1550-km latitudinal and 1403-m altitudinal transect in China. We found relative testis mass and sperm length, male somatic condition, and the male/female sex ratio to increase with elevation but not latitude or longitude. Our results suggest that environmental variation may underlie local adaptations to reproductive investments among natural populations, mediated by differences in the availability of both resources and sexual partners (including the resulting male–male competition). These findings contrast with previous predictions that increasing latitude and/or elevation should lead to declining reproductive investments in male anurans due to shortening breeding seasons, declining resource availability, and lowering (rather than increasing) male/female sex ratios. We discuss these species differences in the context of differential resource allocation strategies, breeding ecology, and patterns of male–male competition. These differences show the need for future work on reproductive investments in anurans beyond the few model systems and for potential extension of the theoretical framework to species with different mating systems and strategies. Despite a broad theoretical framework of how environmental parameters can shape mating systems and these, in turn, drive the evolution of reproductive traits, there is limited empirical evidence from natural populations. We examined differences in the size of testes and sperm between males between natural populations along latitudinal and altitudinal transects. We found that at high elevation, males were relatively heavier and had longer sperm and disproportionately large testes, and the sex ratio was more male-biased. These interpopulation differences may reflect local adaptations to variation in the resource availability and temporal patterns of female availability, which affects the breeding synchrony, sperm demand, and male–male competition for mates and paternity. However, our results differ from previous studies of frogs, possibly due to different breeding ecology, which highlights the need for further work and potential extension of theoretical predictions to non-model anurans.

Reproductive strategy of the invasive sharpbelly,Hemiculter leucisculus(Basilewsky 1855), in Erhai Lake, China

This study describes the reproductive strategy of the sharpbelly Hemiculter leucisculus, an invasive and dominant species in Erhai Lake in China with the goal of understanding how reproductive strategy contributes to its environmental adaptability and invasive potential. Specimens (n = 3583) were collected monthly or bimonthly from July 2009 to June 2011 (min: 114-Feb, max: 883-Aug), using gill nets (inner/outer mesh = 30/110 mm, stretched mesh). Gonads were removed, weighed and preserved for further (histological) analyses. Oocyte size-frequency distribution was continuous and had advanced vitellogenic oocytes with postovulatory follicles present in spawning females, both suggesting that sharpbelly is a multiple spawner with adhesive eggs. Spawning extended from April to September, with the peak period from May to August. Standard lengths (SL, cm) at minimal observed maturity/L50/L99.9 values were 4.6/5.6/10.5 for females and 5.1/5.5/7.5 cm for males, respectively. Females were over-represented (P < 0.01) in SL-classes over 9 cm and males completely absent from the 13 to 19 cm SL-classes. Overall sex ratio was highly significantly (P < 0.01) biased towards females (♀ = 1518, ♂ = 685, ♀/♂ = 2.21), however this was reversed in the spawning stock (8.3–16 cm, ♀ = 58, ♂ = 142, ♂/♀ = 2.45, P < 0.01). Batch spawning, a long spawning period, high male investment in reproduction and adhesive eggs all represent local adaptations in reproductive strategy that, along with other environmental factors, contribute to the invasion success of sharpbelly in Erhai.

Altitudinal variation in male reproductive investment in a polyandrous frog species (Hyla gongshanensis jingdongensis)

Competition for fertilization in multi-male group spawning can drive variation in male reproductive investment (i.e., testis mass and sperm size). Inter-population comparisons of variation in energetic availability and allocation along geographical gradients allow insights into the mechanisms shaping the reproductive investments of animals. Although inter-population differences in female reproductive investment (i.e., clutch size and egg size) have been studied extensively across a wide range of taxa, little information on variation in reproductive investment in males is available. Here, we studied altitudinal variation in testis mass and sperm length among three populations in the Jingdong tree frog (Hyla gongshanensis jingdongensis), a polyandrous species, in Yunnan Province in China. The results showed that individuals exhibited smaller testes at higher altitudes while testes mass was positively correlated with body size, body condition and age. Longer sperm length was observed in the middle-altitude population. Moreover, we found that sperm number was positively correlated with testes mass and sperm length. Our correlational findings suggest that environmental constraints at high altitude select for less investment in testes and offspring number.

Rapid human-induced divergence of life-history strategies in Bahamian livebearing fishes (family Poeciliidae).

Human-induced rapid environmental change (HIREC) can have dramatic impacts on ecosystems, leading to rapid trait changes in some organisms and extinction in others. Such changes in traits signify that human actions can lead to cases of increased phenotypic diversity and consequently can strongly impact population-, community- and ecosystem-level dynamics. Here, we examine whether the ecological consequences of habitat fragmentation have led to changes in the life histories of three native species of mosquitofish (Gambusia spp.) inhabiting tidal creeks on six different Bahamian islands. We address two important questions: (i) How predictable and parallel are life-history changes in response to HIREC across islands and species, and (ii) what is the relative importance of shared (i.e. parallel) responses to fragmentation, differences between species or islands and species- or island-specific responses to fragmentation? Phenotypic differences between fragmentation regimes were as great or greater than differences between species or islands. While some adult life histories (lean weight and fat content) showed strong, shared responses to fragmentation, offspring-related life histories (embryo fat and fecundity) exhibited idiosyncratic, island-specific responses. While shared responses to fragmentation appeared largely driven by a reduction in piscivorous fish density, increased conspecific density and changes in salinity, we found some evidence that among-population variation in male reproductive investment and embryo fat content may have arisen via variation in conspecific density. Our results suggest that phenotypic responses to HIREC can be complex, with the predictability of response varying across traits. We therefore emphasize the need for more theoretical and empirical work to better understand the predictability of phenotypic responses to human-induced disturbances.

Experimental food supplementation reveals habitat-dependent male reproductive investment in a migratory bird.

Environmental factors can shape reproductive investment strategies and influence the variance in male mating success. Environmental effects on extrapair paternity have traditionally been ascribed to aspects of the social environment, such as breeding density and synchrony. However, social factors are often confounded with habitat quality and are challenging to disentangle. We used both natural variation in habitat quality and a food supplementation experiment to separate the effects of food availability-one key aspect of habitat quality-on extrapair paternity (EPP) and reproductive success in the black-throated blue warbler, Setophaga caerulescens. High natural food availability was associated with higher within-pair paternity (WPP) and fledging two broods late in the breeding season, but lower EPP. Food-supplemented males had higher WPP leading to higher reproductive success relative to controls, and when in low-quality habitat, food-supplemented males were more likely to fledge two broods but less likely to gain EPP. Our results demonstrate that food availability affects trade-offs in reproductive activities. When food constraints are reduced, males invest in WPP at the expense of EPP. These findings imply that environmental change could alter how individuals allocate their resources and affect the selective environment that drives variation in male mating success.

Exploring simultaneous allocation to mating effort, sperm production, and body growth in male guppies

In several species, males increase their mating and sperm investment in the presence of unfamiliar females, the so-called Coolidge effect. Such an elevated reproductive effort is expected to be associated with a decreased investment in other costly traits, such as somatic growth and maintenance. How precopulatory, postcopulatory, and somatic investments interact one with each other, however, has been rarely evaluated simultaneously. We used the guppy (Poecilia reticulata), a polyandrous livebearing fish with alternative male mating tactics, to compare these 3 investments between males whose encounter rate with unfamiliar females was experimentally maintained at either high (high mate encounter rate [HER]) or low rate (low mate encounter rate [LER]) for 4 months. At the end of this period, HER males showed an increased sperm production as compared with their LER counterparts. This increment was accompanied with a reduction in the time spent following the female and by a shift from costly courtship displays to gonopodial thrusting, a less expensive coercive mating tactic. This effect may indicate a trade-off between these 2 components of male reproductive investment or may reflect a change in male optimal reproductive strategy associated with different mate encounter rate. In contrast, body growth was positively correlated with the increase in sperm production, and did not differ between experimental groups. Collectively, these results suggest that males did not vary their overall reproductive investment in response to their encounter rate with unfamiliar females, but differed significantly in the amount of resources available individually.

Developmental stress increases reproductive success in male zebra finches.

There is increasing evidence that exposure to stress during development can have sustained effects on animal phenotype and performance across life-history stages. For example, developmental stress has been shown to decrease the quality of sexually selected traits (e.g. bird song), and therefore is thought to decrease reproductive success. However, animals exposed to developmental stress may compensate for poor quality sexually selected traits by pursuing alternative reproductive tactics. Here, we examine the effects of developmental stress on adult male reproductive investment and success in the zebra finch (Taeniopygia guttata). We tested the hypothesis that males exposed to developmental stress sire fewer offspring through extra-pair copulations (EPCs), but invest more in parental care. To test this hypothesis, we fed nestlings corticosterone (CORT; the dominant avian stress hormone) during the nestling period and measured their adult reproductive success using common garden breeding experiments. We found that nestlings reared by CORT-fed fathers received more parental care compared with nestlings reared by control fathers. Consequently, males fed CORT during development reared nestlings in better condition compared with control males. Contrary to the prediction that developmental stress decreases male reproductive success, we found that CORT-fed males also sired more offspring and were less likely to rear non-genetic offspring compared with control males, and thus had greater overall reproductive success. These data are the first to demonstrate that developmental stress can have a positive effect on fitness via changes in reproductive success and provide support for an adaptive role of developmental stress in shaping animal phenotype.

The intrinsically dynamic nature of mating patterns and sexual selection

Selection processes are influenced by both biotic and abiotic variables, most of which seasonally fluctuate. Therefore, selection may also vary temporally. Specifically, sexual selection, an integral component of natural selection, will inevitably exhibit temporal variation but the scale at which these changes occur are still not well understood. In this study, performed on a wild population of the sex-role reversed black striped pipefish Syngnathus abaster (Risso, 1827), we contrast variables such as male reproductive success, mating success, female investment, mate choice and operational sex ratio between two periods, either near the onset or end of the breeding season. Sexual selection is stronger early in the breeding season. Male reproductive and mating success are significantly affected by male size during the onset of the breeding season but not during the end. Moreover, we found that larger females reproduce mainly during the onset while smaller females had increased chances of reproducing towards the end. As our sampling was performed in two consecutive years, it could be argued that our results stem primarily from between-year variation. Nevertheless, variation in demographic parameters from the onset to the end of the breeding season is similar to that observed in past sampling events. Hence, we suggest that the change in mating patterns within the breeding season derives from seasonal fluctuations in several abiotic (e.g., temperature) and biotic variables (e.g., operational sex ratio), rendering the expression of selective forces, such as sexual selection, inherently dynamic.

Male-female relatedness and patterns of male reproductive investment in guppies.

Inbreeding can cause reductions in fitness, driving the evolution of pre- and postcopulatory inbreeding avoidance mechanisms. There is now considerable evidence for such processes in females, but few studies have focused on males, particularly in the context of postcopulatory inbreeding avoidance. Here, we address this topic by exposing male guppies (Poecilia reticulata) to either full-sibling or unrelated females and determining whether they adjust investment in courtship and ejaculates. Our results revealed that males reduce their courtship but concomitantly exhibit short-term increases in ejaculate quality when paired with siblings. In conjunction with prior work reporting cryptic female preferences for unrelated sperm, our present findings reveal possible sexually antagonistic counter-adaptations that may offset postcopulatory inbreeding avoidance by females.

The Effects of Perceived Mating Opportunities on Patterns of Reproductive Investment by Male Guppies

Males pay considerable reproductive costs in acquiring mates (precopulatory sexual selection) and in producing ejaculates that are effective at fertilising eggs in the presence of competing ejaculates (postcopulatory sexual selection). Given these costs, males must balance their reproductive investment in a given mating to optimise their future reproductive potential. Males are therefore expected to invest in reproduction prudently according to the likelihood of obtaining future matings. In this study we tested this prediction by determining whether male reproductive investment varies with expected future mating opportunities, which were experimentally manipulated by visually exposing male guppies (Poecilia reticulata) to high or low numbers of females in the absence of competing males. Our experiment did not reveal consistent effects of perceived future mating opportunity on either precopulatory (male mate choice and mating behaviour) or postcopulatory (sperm quality and quantity) investment. However, we did find that male size and female availability interacted to influence mating behaviour; large males visually deprived of females during the treatment phase became more choosy and showed greater interest in their preferred female than those given continuous visual access to females. Overall, our results suggest males tailor pre- rather than postcopulatory traits according to local female availability, but critically, these effects depend on male size.

Is Fatter Sexier? Reproductive Strategies of Male Squirrel Monkeys (Saimiri sciureus)

Sexually dimorphic traits can evolve through male–male competition or female choice. Squirrel monkeys (genus Saimiri) live in large multimale, multifemale groups and are seasonal breeders with concealed ovulation. In several species of the genus, females are dominant to males. Males show weight gain preceding and during the mating season, which produces a “fattened” appearance in the upper arms, shoulders, and torso. Although much is known about the physiology of fattening, the evolutionary function(s) of this sexually dimorphic trait, including possible benefits and costs, remain(s) unknown. This unusual reproductive physiology of males is suggestive of sexual selection. Here I present data on wild Saimiri sciureus studied in Brazil to describe male reproductive investment in the species and to examine the hypothesis that male fattening is a product of sexual selection. I observed at least nine adult males via focal animal sampling and ad libitum observations during four mating seasons and during an additional 10 nonbreeding season months for comparison. Compared to less robust males, fatter males spent significantly more time near females and less time alone. These males also spent more time engaged in sociosexual activities and less time feeding/foraging, suggesting a trade-off between maintenance and reproductive behaviors. The 2-mo mating season accounted for 62% of all male–male agonism observed over one 12-mo period. These results are suggestive of male–male competition for females. However, males did not coerce females to mate and females often rejected males; this pattern suggests female choice. It is possible that male fattening in Saimiri is a product of both intra- and intersexual selection. Males experience intense reproductive costs related to agonism with other males, and related to time and energy invested in the pursuit of females. Although fattening may mitigate some of these costs by aiding in male–male competition and in female preference, this phenomenon is likely not without physiological costs to adult males.

Some pollinators are more equal than others: Factors influencing pollen loads and seed set capacity of two actively and passively pollinating fig wasps

The nursery pollination system of fig trees (Ficus) results in the plants providing resources for pollinator fig wasp larvae as part of their male reproductive investment, with selection determining relative investment into pollinating wasps and the pollen they carry. The small size of Ficus pollen suggests that the quantities of pollen transported by individual wasps often limits male reproductive success. We assessed variation in fig wasp pollen loads and its influence on seed production in actively pollinated (Ficus montana) and passively pollinated (Ficus carica) dioecious fig trees.The ratios of number of male flowers on number of female flowers in a glasshouse-maintained F. montana population were highly variable. When fig wasps were introduced into receptive female figs, the resulting seed numbers were strongly linked to the numbers of pollinators that had been seeking access to pollen, relative to the number of anthers in their natal figs. In F. carica estimates of the amounts of pollen produced per fig and the quantities of pollen carried by emerging fig wasps suggest that less than 10% of the pollen is transported. Pollinators of F. carica that emerged earlier from figs carried more pollen, and also generated more seeds when introduced into receptive female figs.We show here that all pollinators are not equally valuable and producing more pollinators is not necessarily a good option in terms of Ficus male fitness. Previous results on F. montana figs showed that only around half of the flowers where pollinators lay eggs produced adult offspring. The amount of pollen collected by young female fig wasps may be a major determinant of their reproductive success.

Increase in Male Reproductive Success and Female Reproductive Investment in Invasive Populations of the Harlequin Ladybird Harmonia axyridis

Reproductive strategy affects population dynamics and genetic parameters that can, in turn, affect evolutionary processes during the course of biological invasion. Life-history traits associated with reproductive strategy are therefore potentially good candidates for rapid evolutionary shifts during invasions. In a series of mating trials, we examined mixed groups of four males from invasive and native populations of the harlequin ladybird Harmonia axyridis mating freely during 48 hours with one female of either type. We recorded the identity of the first male to copulate and after the 48 h-period, we examined female fecundity and share of paternity, using molecular markers. We found that invasive populations have a different profile of male and female reproductive output. Males from invasive populations are more likely to mate first and gain a higher proportion of offspring with both invasive and native females. Females from invasive populations reproduce sooner, lay more eggs, and have offspring sired by a larger number of fathers than females from native populations. We found no evidence of direct inbreeding avoidance behaviour in both invasive and native females. This study highlights the importance of investigating evolutionary changes in reproductive strategy and associated traits during biological invasions.

Carotenoid supplementation during adulthood, but not development, decreases testis size in mallards

Nutritional constraints on reproduction are well-characterized in female animals, but rarely have particular nutrients been linked to male reproductive investments. Carotenoid pigments promote egg-laying and fertility in several animals, and are displayed externally within secondary sex traits by males of many colorful species to attract mates, but it is unclear if or how carotenoids affect male primary sex traits. We manipulated carotenoid availability in the diet of male mallards (Anas platyrhynchos) during both development and adulthood to determine effects on size and carotenoid content of the testes. We found that developmental carotenoid manipulations did not affect testis size or carotenoid concentration, but that increased carotenoid dietary levels at adulthood resulted in more carotenoid-rich, but smaller, testes. This latter result was surprising, given positive correlations in mammals between testicle size and carotenoid concentration. We also found negative correlations between testis size and carotenoid concentration for individual ducks, regardless of dietary treatment. These results suggest that carotenoid deposition into testis tissue can reduce investment in gonad size (and thus overall sperm count), although the functional consequences of this relationship remain to be tested.

Larval competition causes the difference in male ejaculate expenditure in Callosobruchus maculatus

AbstractThe seed beetle Callosobruchus maculatus larvae exhibit two types of resource competition: scramble, in which a resource is shared, and contest, in which the resource is monopolized. This difference in larval behavior results in different adult densities. Under contest competition, adult density remains constant regardless of larval density, but under scramble competition, adult density increases with larval density. This in turn affects mating frequency during adulthood, and thus, the intensity of sexual selection operating on males. In this study, we examined the relationship between larval competition types and male reproductive investment in mating. We assessed the male ejaculate expenditure per mating across geographic strains of C. maculatus. The male investment (ejaculate expenditure) increased with the degree of scramble competition and decreased with the degree of contest competition. We therefore suggest that males experience different selective pressures depending on the type of larval competition: scramble type males are selected for increased reproductive investment.

Exposure to sperm competition risk improves survival of virgin males

Sperm competition between the ejaculates of multiple males for the fertilization of a given set of ova is taxonomically widespread. Males have evolved remarkable adaptations to increase their reproductive success under postcopulatory sexual selection, which in many species includes the ability to modify behaviour and ejaculate characteristics plastically to match the perceived level of sperm competition. Males of the model species Drosophila melanogaster increase mating duration and modify seminal fluid composition in response to short-term changes in sperm competition risk. If these responses increase a male's total investment in reproduction, he must either trade-off this cost against other life-history traits or suffer reduced survival. We tested whether mounting a plastic sperm competition response bears an instantaneous survival cost, and instead found that male D. melanogaster exposed to a high risk of sperm competition survive 12 per cent longer than those at low risk, equating to a 49 per cent reduction in the hourly hazard of death. This striking effect was found only among virgins: the high cost of mating in this species eliminates any such benefit among non-virgin males. Our results suggest that the improvement in survival found among virgins may be a product of males' tactical responses to sperm competition.

Age‐Related Male Reproductive Investment in Courtship Display and Nuptial Gifts in a Moth, Ostrinia scapulalis

AbstractDue to a trade‐off between current and future reproduction, costly reproductive investments should be increased towards the end of a lifespan when the probability of reproduction becomes low (terminal investment hypothesis). We investigated age‐related changes in male reproductive investment towards courtship display and the spermatophore in three age classes (young, middle‐aged and old) of a monandrous moth, Ostrinia scapulalis. As predicted, old males had higher mating success than young and middle‐aged males in no‐choice tests. Moreover, two‐choice tests revealed that middle‐aged males had a higher success rate than young males because of their higher courtship frequency rather than any female preference for them. It was found that old males produced a larger spermatophore than young and middle‐aged males, suggesting greater reproductive effort. The protein content of spermatophores also tended to increase with male age. Despite the age‐related variation in spermatophore size and protein content, age did not affect female fecundity or longevity. A decrease in the number of sperm in the older males might counteract the nutritional benefit of larger spermatophores. Alternatively, fitness components other than longevity and fecundity may be influenced by male age.

Strategic male mate choice minimizes ejaculate consumption

Reproduction can be costly for males, particularly when they provide nutrient-rich ejaculates in the form of spermatophores or secondary ejaculatory components. These costs may further increase if females reject or consume a male’s ejaculate rather than using it for egg fertilization. Males should, therefore, attempt to minimize these costs to maximize their reproductive payoffs. We examined male reproductive investment toward virgin females in the Southern Bottletail Squid, Sepiadarium austrinum. Specifically, we assessed whether the presence of unfertilized eggs inside females influenced male reproductive investment, whether females removed spermatophores postcopulation, and what phenotypic characteristics influenced spermatophore removal. We found that males were more likely to attempt mating with females that were proportionally larger, but mated for longer and were more likely to transfer spermatophores to egg-carrying females. Females consistently ate spermatophores transferred by males, with the smallest females eating the most. However, males did not vary spermatophore investment according to female size or the associated risk of spermatophore consumption.