Determinant Of Male Reproductive Success Research Articles

Recovery from heat-induced infertility-A study of reproductive tissue responses and fitness consequences in male Drosophila melanogaster.

The predicted temperature increase caused by climate change is a threat to biodiversity. Across animal taxa, male reproduction is often sensitive to elevated temperatures leading to fertility loss, and in more adverse scenarios, this can result in sterility when males reach their upper thermal fertility limit. Here, we investigate temperature-induced changes in reproductive tissues, fertility reduction, sterility, and the associated fitness loss during the subsequent recovery phase in male Drosophila melanogaster. We heat-stressed males during development and either allowed them to recover or not in early adulthood while measuring several determinants of male reproductive success. We found significant differences in recovery rate, organ sizes, sperm production, and other key reproductive traits among males from our different temperature treatments. Sperm maturation was impaired before reaching the upper thermal sterility threshold. While some effects were reversible, this did not compensate for the fitness loss due to damage imposed during development. Surprisingly, developmental heat stress was damaging to accessory gland growth, and female post-mating responses mediated by seminal fluid proteins were impaired regardless of the possibility of recovery. We suggest that sub-lethal thermal sterility and the subsequent fertility reduction are caused by a combination of inefficient functionality of both the accessory gland and testes.

Kangaroo Fathers Modulate Maternal Control of Offspring Sex but Not Postpartum Maternal Expenditure.

AbstractWhen sons and daughters have different fitness costs and benefits, selection may favor deviations from an even offspring sex ratio. Most theories on sex ratio manipulation focus on maternal strategies and sex-biased maternal expenditure. Recent studies report paternal influences on both offspring sex ratio and postpartum sex-biased maternal expenditure. We used long-term data on marked kangaroos to investigate whether and how paternal mass and skeletal size, both determinants of male reproductive success, influenced (a) offspring sex in interaction with maternal mass and (b) postpartum sex-biased maternal expenditure. When mothers were light, the probability of having a son increased with paternal mass. Heavy mothers showed the opposite trend. A similar result emerged when considering paternal size instead of mass. Postpartum maternal sex-specific expenditure was independent of paternal mass or size. Studies of offspring sex manipulation or maternal expenditure would benefit from an explicit consideration of paternal traits, as paternal and maternal effects can modulate each other.

Reproductive phenology and female mating frequency of the praying mantidTenodera angustipennisin western Japan

AbstractThe timing and frequency of female mating are important determinants of male reproductive success. Elucidating reproductive phenology is crucial to understand the evolution of mating behaviour and mating systems.Mate encounter rate is a key variable for understanding the evolutionary consequences of sexual cannibalism. However, remarkably little is known about female mating frequency in wild populations in mantids, charismatic insects that exhibit sexual cannibalism.The authors examined the reproductive phenology of a wild population of the sexually cannibalistic praying mantidTenodera angustipennis, and paid special attention to female mating frequency.Field surveys throughout two reproductive seasons were combined with survival model analysis to estimate the phenology of eclosion, adult sex ratio, female first mating, and oviposition, allowing quantification of time windows for reproductive maturation and female mating.Genetic paternity analysis using newly developed microsatellite markers revealed that females mated with two to six males on average before oviposition in the wild.The results provide a comprehensive record of the reproductive phenology and female mating frequency in a wild mantid population, and insight into the evolution of male mating behaviour under sperm competition and sexual cannibalism.

Identification of determinants of pollen donor fecundity using the hierarchical neighborhood model.

Individual differences in male reproductive success drive genetic drift and natural selection, altering genetic variation and phenotypic trait distributions in future generations. Therefore, identifying the determinants of reproductive success is important for understanding the ecology and evolution of plants. Here, based on the spatially explicit mating model (the neighborhood model), we develop a hierarchical probability model that links co-dominant genotypes of offspring and candidate parents with phenotypic determinants of male reproductive success. The model accounts for pollen dispersal, genotyping errors as well as individual variation in selfing, pollen immigration, and differentiation of immigrant pollen pools. Unlike the classic neighborhood model approach, our approach is specially designed to account for excessive variation (overdispersion) in male fecundity. We implemented a Bayesian estimation method (the Windows computer program available at: https://www.ukw.edu.pl/pracownicy/plik/igor_chybicki/1806/) that, among others, allows for selecting phenotypic variables important for male fecundity and assessing the fraction of variance in fecundity (R2 ) explained by selected variables. Simulations showed that our method outperforms both the classic neighborhood model and the two-step approach, where fecundities and the effects of phenotypic variables are estimated separately. The analysis of two data examples showed that in wind-pollinated trees, male fecundity depends on both the amount of produced pollen and the ability to pollen spread. However, despite that the tree size was positively correlated with male fecundity, it explained only a fraction of the total variance in fecundity, indicating the presence of additional factors. Finally, case studies highlighted the importance of accounting for pollen dispersal in the estimation of fecundity determinants.

The impact of ageing on male reproductive success in Drosophila melanogaster

Male reproductive ageing has been mainly explained by a reduction in sperm quality with negative effects on offspring development and quality. In addition to sperm, males transfer seminal fluid proteins (Sfps) at mating; Sfps are important determinants of male reproductive success. Receipt of Sfps leads to female post-mating changes including physiological changes, and affects sperm competition dynamics. Using the fruit fly Drosophila melanogaster we studied ageing males' ability to induce female post-mating responses and determined the consequences of male ageing on their reproductive success. We aged males for up to 7weeks and assayed their ability to: i) gain a mating, ii) induce egg-laying and produce offspring, iii) prevent females from remating and iv) transfer sperm and elicit storage after a single mating. We found that with increasing age, males were less able to induce post-mating responses in their mates; moreover ageing had negative consequences for male success in competitive situations. Our findings indicate that with advancing age male flies transferred less effective ejaculates and that Sfp composition might change over a male's lifetime in quantity and/or quality, significantly affecting his reproductive success.

Factors influencing reproductive success in male white‐tailed deer

ABSTRACTPositive relationships between age, sexually selected traits, and male reproductive success have been reported for a number of polygynous ungulates; however, relatively little is known about the factors influencing male reproductive success in ungulate species whose mating system is characterized by tending‐bond behaviors. Broad interest in the genetic consequences of selective harvest supports a greater understanding of the role of these factors as determinants of male reproductive success in important game species (e.g., white‐tailed deer [Odocoileus virginianus]), that exhibit tending‐bond behaviors. We investigated male reproductive success in white‐tailed deer across a range of sex ratios and age structures using a known population of deer housed in a 175‐ha enclosure in central Alabama, USA. We measured age, annual antler size, and annual body size of male white‐tailed deer and assigned paternity to 143 known‐age offspring during 2007–2014. Reproductive success was attributed to a high proportion of males during each of the 6 breeding seasons. Our most supported model indicated that annual body size and antler size of the individual were positively associated with annual male breeding success. The effects of annual antler size were sensitive to changes in mean male age of the herd, with antler size having the greatest effect on male reproductive success under older male age structures. Young (≤1.5 yr) males reproduced most frequently when male age structure was youngest (which correlated with female‐biased sex ratios in this population). Our results suggest that male age structure and sex ratio played a key role in establishing patterns of male reproductive success in white‐tailed deer. Management practices that encourage balanced adult sex ratios and older male age structures (e.g., Quality Deer Management) may promote a highly competitive environment where sexually selected traits are of increased importance to male breeding success. However, the ability of managers to alter herd genetics in a positive or negative direction through selective harvest is limited in white‐tailed deer because of the high proportion of reproducing males. © 2016 The Wildlife Society.

Morphology-function relationships and repeatability in the sperm of Passer sparrows.

Sperm performance is likely to be an important determinant of male reproductive success, especially when females copulate with multiple males. Understanding sperm performance is therefore crucial to fully understand the evolution of male reproductive strategies. In this study, we examined the repeatability of sperm morphology and motility measures over three breeding seasons, and we studied relationships between sperm morphology and function. We conducted this study in wild-derived captive house sparrows (Passer domesticus) and Spanish sparrows (P. hispaniolensis). Results for the two species were similar. As predicted from results in other passerine species, total sperm length was highly repeatable across ejaculates, and repeatability for the length of other components was moderate. The repeatability of sperm swimming speed across ejaculates was lower, but statistically significant, suggesting that sperm velocity may be a relatively dynamic trait. Surprisingly, swimming speed did not correlate with the relative length of the midpiece, and it correlated negatively with the relative length of the flagellum and with total sperm length. This pattern is the opposite of what theory predicts and differs from what has been found in house sparrows before. Also contrary to previous work, we found no evidence that total sperm length correlates with sperm longevity. These results therefore highlight the need for a better understanding of relationships between sperm morphology and function in passerine birds.

Costs of mate-guarding in wild male long-tailed macaques (Macaca fascicularis): Physiological stress and aggression

Mate-guarding is an important determinant of male reproductive success in a number of species. However, it is known to potentially incur costs. The aim of the present study was to assess the effect of mate-guarding on male physiological stress and aggression in long-tailed macaques, a species in which males mate-guard females to a lesser extent than predicted by the Priority of Access model (PoA). The study was carried out during two mating periods on three groups of wild long-tailed macaques in Indonesia by combining behavioral observations with non-invasive measurements of fecal glucocorticoid (fGC) levels. Mate-guarding was associated with a general rise in male stress hormone levels but, from a certain threshold of mate-guarding onwards, increased vigilance time was associated with a decrease in stress hormone output. Mate-guarding also increased male-male aggression rate and male vigilance time. Overall, alpha males were more physiologically stressed than other males independently of mating competition. Increased glucocorticoid levels during mate-guarding are most likely adaptive since it may help males to mobilize extra-energy required for mate-guarding and ultimately maintain a balanced energetic status. However, repeated exposure to high levels of stress over an extended period is potentially deleterious to the immune system and thus may carry costs. This potential physiological cost together with the cost of increased aggression mate-guarding male face may limit the male’s ability to mate-guard females, explaining the deviance from the PoA model observed in long-tailed macaques. Comparing our results to previous findings we discuss how ecological factors, reproductive seasonality and rank achievement may modulate the extent to which costs of mate-guarding limit male monopolization abilities.

Mate-guarding constrains feeding activity but not energetic status of wild male long-tailed macaques (Macaca fascicularis)

Mate-guarding is an important determinant of male reproductive success in a number of species. Little is known however about the constraints of this behaviour, e.g. the associated energetic costs. We investigated these costs in long-tailed macaques where alpha males mate guard females to a lesser extent than predicted by the priority of access model. The study was carried out during two mating periods on three wild groups living in the Gunung Leuser National Park, Indonesia. We combined behavioural observations on males’ locomotion and feeding activity, GPS records of distance travelled and non-invasive measurements of urinary C-peptide (UCP), a physiological indicator of male energetic status. Mate-guarding led to a decrease in feeding time and fruit consumption suggesting a reduced intake of energy. At the same time, vertical locomotion was reduced, which potentially saved energy. These findings, together with the fact that we did not find an effect of mate-guarding on UCP levels, suggest that energy intake and expenditure was balanced during mate-guarding in our study males. Mate-guarding thus seems to not be energetically costly under all circumstances. Given that in strictly seasonal rhesus macaques, high-ranking males lose physical condition over the mating period, we hypothesise that the energetic costs of mate-guarding vary inter-specifically depending on the degree of seasonality and that males of non-strictly seasonal species might be better adapted to maintain balanced energetic condition year-round. Finally, our results illustrate the importance of combining behavioural assessments of both energy intake and expenditure with physiological measures when investigating energetic costs of behavioural strategies.

The cost of trying: weak interspecific correlations among life-history components in male ungulates

Life-history trade-offs are well known in female mammals, but have seldom been quantified for males in polygynous species. I compared age-specific mass, weapon size, survival, and reproductive success of males in eight species of ungulates, and found weak interspecific correlations among life-history traits. Young males tended to have higher reproductive success in rapidly-growing than in slow-growing species, and in species where horns or antlers reached near-asymptotic size over the first few years of life. There was no clear interspecific trade-off between early reproduction and early survival. Reproductive senescence was evident in most species. Generation length, calculated as the mean age of fathers, was negatively correlated with the reproductive success of young males and positively with life expectancy of 3-year-olds, but not with early mortality. The main determinant of male reproductive success in polygynous ungulates is the ability to prevail against competing males. Consequently, the number and age structure of competitors should strongly affect an individual’s ability to reproduce, making classic trade-offs among life-history traits very context-dependent. Most fitness costs of reproduction in male ungulates likely arise from energy expenditure and injuries sustained while attempting to mate. Individual costs may be weakly correlated with fitness returns.

Sexual selection and the differential effect of polyandry.

In principle, widespread polyandry (female promiscuity) creates potential for sexual selection in males both before and after copulation. However, the way polyandry affects pre- and postcopulatory episodes of sexual selection remains little understood. Resolving this fundamental question has been difficult because it requires extensive information on mating behavior as well as paternity for the whole male population. Here we show that in replicate seminatural groups of red junglefowl, Gallus gallus, polyandry eroded variance in male mating success, which simultaneously weakened the overall intensity of sexual selection but increased the relative strength of postcopulatory episodes. We further illustrate the differential effect of polyandry on pre- and postcopulatory sexual selection by considering the case of male social status, a key determinant of male reproductive success in this species. In low-polyandry groups, however, status was strongly sexually selected before copulation because dominants mated with more females. In high-polyandry groups, sexual selection for status was weakened and largely restricted after copulation because dominants defended paternity by mating repeatedly with the same female. These results reveal polyandry as a potent and dynamic modulator of sexual selection episodes.

Male reproductive senescence as a potential source of sexual conflict in a beetle

The link between senescence and reproductive success is a contentious yet crucial issue to our understanding of mate choice, sexual conflict, and the evolution of ageing. By imposing direct (i.e., male fertility) or indirect (i.e., zygote viability) reproductive costs to females, male senescence may lead to sexual conflict at different levels. For example, ageing may affect male ability to deliver sperm, thus setting the scene for sexual conflict over mating, and/or may affect the quality of individual sperm cells, generating the potential for sexual conflict over fertilizing strategies. We addressed these issues by studying the mating behavior, reproductive fitness, and fertilization patterns of females mated to young versus old males in a beetle (Tenebrio molitor). Our results show that male senescence imposes direct fertility costs on females and that females mated to old males produce offspring of lower quality (i.e., smaller) than those mated to young males. Compared with females mated to young males, females mated to old males were less receptive and decreased their allocation to spermatophore guarding (a crucial determinant of male reproductive success in this species), increasing the risk of sperm competition by other males. In contrast, old males increased their own investment in spermatophore guarding, which suggests the existence of antagonistic selection over sperm competition strategies. These findings lend support to the recent notion that ageing may act as an evolutionary source of sexual conflict. [Behav Ecol]

Sexual dimorphism and growth trade‐offs in Blue Tit Cyanistes caeruleus nestlings

The outcome of sibling competition for food is often determined by variation in body size within the brood and involves trade‐offs; traits that enhance competitive ability within the nest may be developed at the expense of traits that enable effective flight at fledging, or vice versa. We quantified growth of skeletal, body mass and feather traits in male and female Blue Tit Cyanistes caeruleus nestlings. Males were significantly heavier, had longer tarsi and tended to have greater head–bill lengths than females, whereas females were similar to males in wing flight feather growth. These differences in growth may result from sexual differences in selection of the traits. Females are likely to prioritize feather growth to facilitate synchronized fledging with the rest of the brood, and to enhance escape from predators. We suggest that males are heavier and develop longer tarsi because body size is an important determinant of male reproductive success.

Male Reproductive Senescence Causes Potential for Sexual Conflict over Mating

The realization that senescence, age-dependent declines in survival and reproductive performance, pervades natural populations has brought its evolutionary significance into sharper focus. However, reproductive senescence remains poorly understood because it is difficult to separate male and female mechanisms underpinning reproductive success. We experimentally investigated male reproductive senescence in feral fowl, Gallus gallus domesticus, where socially dominant males monopolize access to females and the ejaculates of multiple males compete for fertilization. We detected the signal of senescence on multiple determinants of male reproductive success. The effect of age on status was dependent upon the intensity of intrasexual competition: old males were less likely to dominate male-biased groups where competition is intense but were as likely as young males to dominate female-biased groups. Mating and fertilization success declined sharply with male age largely as a result of population-level patterns. These age-dependent declines translated into sexually antagonistic payoffs: old males fertilized more eggs when they were dominant, but this resulted in females suffering a drastic reduction in fertility. Thus, male senescence causes potential for sexual conflict over mating, and the intensity of this conflict is modulated socially, by the probability of old males dominating reproductive opportunities.

Male mate choice: why sequential choice can make its evolution difficult

Male reproductive success is typically mate limited, which implies that males should rarely be choosy. On the other hand, females often vary greatly in their fecundity or other determinants of male reproductive success. There are two coexisting threads in the current literature on male mate choice: a number of studies emphasize that male mate choice has been underappreciated in the past, while another set reminds us that it nevertheless evolves less easily than female choice. Here we show that when mate choice is sequential rather than simultaneous (which is often the case for the mate-limited sex), male mate choice may fail to evolve even if there is large variation among fitness prospects offered by various females, and when mating is very costly. Our model is inspired by the mating system of the sexually cannibalistic praying mantid Pseudomantis albofimbriata. Males of this species do not stop approaching females that have turned to face them even though this female behaviour greatly increases the risk of being cannibalized. We show that low mate availability can override the effect of all other factors that select for male mate choice: rejecting a current mating opportunity in the hope of better future opportunities is then not easily selected for. We conclude that studies of mate choice should examine why individuals refuse to take advantage of every opportunity, instead of merely focusing on the fact that some opportunities are better than others. Our results also call for more rigorous empirical tests of mate choice.

PRONOUNCED WITHIN-INDIVIDUAL PLASTICITY IN SPERM MORPHOMETRY ACROSS SOCIAL ENVIRONMENTS

Sperm morphometry (i.e., size and shape) and function are important determinants of male reproductive success and are thought to be under stabilizing selection. However, recent studies suggest that sperm morphometry can be a phenotypically plastic trait, which can be adjusted to varying conditions. We tested whether different behavioral strategies in aggression between aggressive red and nonaggressive black males of the color polymorphic Gouldian finch (Erythrura gouldiae) can influence sperm morphometry. We show pronounced within-individual phenotypic plasticity in sperm morphometry of male Gouldian finches in three different social environments. Both red and black males placed in intermediate to high competitive environments (high frequency of red males) increased the relative length of their sperm midpiece. By contrast, red males placed in low to intermediate competitive environments (higher frequency of black males) increased the length of the sperm flagellum. Significant changes in stress and sex steroid hormone levels (in response to the competitive environment) appear to influence sperm traits in red but not in black males, suggesting that changes in hormonal levels are not solely responsible for the observed changes in sperm morphometry. These findings imply that males can adjust sperm morphometry across social environments.

Determinants of male reproductive success in American black bears

We determined annual male reproductive success in black bears (Ursus americanus) using DNA and field data from two populations in New Mexico. We identified the likely father for 78 of 120 genotyped cubs born during 1994–2000 and calculated reproductive success for 102 males known or presumed present within designated mating regions. Age was a strong determinant of reproductive success. The observed peak in reproductive success occurred at roughly the same intermediate age (10 years) as milder peaks in body size characteristics (11–12 years) and frequency of bear-inflicted wounds (13 years), suggesting body size and fighting might be important for mating. Success was negatively associated with the distance between home range centers of males and mothers. Success of young males (<7 years old) was also negatively associated with mature male (≥7 years old) density, and increasing density shifted the peak age of reproduction higher. The dispersed distribution of females likely limited the capacity of large mature males to dominate reproduction; therefore, success was determined by a complex set of variables.

Male body size and breeding tubercles are both linked to intrasexual dominance and reproductive success in the minnow

Male dominance hierarchies are usually linked to relative body size and to weapon size, that is, to determinants of fighting ability. Secondary sexual characters that are not directly used as weapons could still be linked to dominance if they reveal determination or overall health and vigour and hence, indirectly, fighting ability. We studied the mating behaviour of the minnow, Phoxinus phoxinus, a cyprinid fish in which males develop breeding tubercles during the spawning season. The function of these breeding tubercles is still not clear. Using microsatellite markers, we determined male reproductive success under controlled conditions. The minnows were territorial and quickly established a dominance hierarchy at the beginning of the spawning season. Dominance was strongly and positively linked to fertilization success. Although body size and number of breeding tubercles were not significantly correlated in our sample, both large males and males with many breeding tubercles were more dominant and achieved higher fertilization success than small males or males with few tubercles. We found multimale fertilization in most clutches, suggesting that sperm competition is important in this species. Females showed behaviour that may be linked to spawning decision, that is, male dominance might not be the only determinant of male reproductive success in minnows.

EXPERIMENTAL MANIPULATION OF SEXUAL SELECTION PROMOTES GREATER MALE MATING CAPACITY BUT DOES NOT ALTER SPERM INVESTMENT

Sexual selection theory makes clear predictions regarding male spermatogenic investment. To test these predictions we used experimental sexual selection in Drosophila pseudoobscura, a sperm heteromorphic species in which males produce both fertile and sterile sperm, the latter of which may function in postmating competition. Specifically, we determined whether the number and size of both sperm types, as well as relative testis mass and accessory gland size, increased with increased sperm competition risk and whether any fitness benefits could accrue from such changes. We found no effect of sexual selection history on either the number or size of either sperm morph, or on relative testis mass. However, males experiencing a greater opportunity for sexual selection evolved the largest accessory glands, had the greatest mating capacity, and sired the most progeny. These findings suggest that sterile sperm are not direct targets of sexual selection and that accessory gland size, rather than testis mass, appears to be an important determinant of male reproductive success. We briefly review the data from experimental sexual selection studies and find that testis mass may not be a frequent target of postcopulatory sexual selection and, even when it is, the resulting changes do not always improve fitness.

Sperm quantity and size variation in un-irradiated and irradiated males of the malaria mosquito Anopheles arabiensis Patton

Anopheles mosquitoes are important candidates for genetic control strategies. However, little is known about sperm quality and quantity as determinants of male reproductive success. In this study, sperm quantity and length variation were assessed in testes of un-irradiated and irradiated Anopheles arabiensis. Male reproductive organs were dissected for sperm and an estimate of the total number of spermatozoa was made. Sperm lengths were measured using imaging software. The effects of irradiation were evaluated for males exposed in the pupal or adult stage to a full (120 Gy) or partially sterilising dose (70 Gy). Sperm length variation in the laboratory strain was compared to the distribution observed in wild males. We also determined the size distribution of sperm lengths in spermathecae of inseminated females compared to those observed in male testes. Sperm quantity increased with age, and 12-day-old males had significantly more sperm in their testes (8214 ± 467) than males aged 3 days (5022 ± 375). Mosquitoes irradiated in the pupal stage had significantly fewer sperm (2982 ± 125) than un-irradiated males (4950 ± 848) although for adult stage irradiation similar amounts of sperm were observed compared to un-irradiated males. Sperm length variation was detected with sperm lengths ranging between <50 and 500 μm. There were no differences in sperm length distribution compared to wild males. Sperm length distributions were similar to those reported for the closely related sibling species An. gambiae s.s. There was no major effect of irradiation on the distribution of sperm lengths in the testes, with the exception that pupal irradiation resulted in a significant increase in sperm numbers in the category of 100–200 μm. Sperm length distributions in spermathecae were different to those measured directly from sperm in the testes and harboured less cells of the smaller (<100–200 μm), and more cells of the larger category (300–400 μm). The finding that testes of pupal irradiated males produce fewer and smaller sperm in comparison to un-irradiated and adult irradiated testes are discussed in the context of genetic control strategies, in particular the Sterile Insect Technique (SIT).