Male Reproductive Behavior Research Articles

Sexual experience enhances Drosophila melanogaster male mating behavior and success.

Competition for mates is a wide-spread phenomenon affecting individual reproductive success. The ability of animals to adjust their behaviors in response to changing social environment is important and well documented. Drosophila melanogaster males compete with one another for matings with females and modify their reproductive behaviors based on prior social interactions. However, it remains to be determined how male social experience that culminates in mating with a female impacts subsequent male reproductive behaviors and mating success. Here we show that sexual experience enhances future mating success. Previously mated D. melanogaster males adjust their courtship behaviors and out-compete sexually inexperienced males for copulations. Interestingly, courtship experience alone is not sufficient in providing this competitive advantage, indicating that copulation plays a role in reinforcing this social learning. We also show that females use their sense of hearing to preferentially mate with experienced males when given a choice. Our results demonstrate the ability of previously mated males to learn from their positive sexual experiences and adjust their behaviors to gain a mating advantage. These experienced-based changes in behavior reveal strategies that animals likely use to increase their fecundity in natural competitive environments.

Heterosis in age‐specific selected populations of a seed beetle: Sex differences in longevity and reproductive behavior

We tested mutation accumulation hypothesis for the evolution of senescence using short-lived and long-lived populations of the seed-feeding beetle, Acanthoscelides obtectus (Say), obtained by selection on early- and late-life for many generations. The expected consequence of the mutation accumulation hypothesis is that in short-lived populations, where the force of natural selection is the strongest early in life, the late-life fitness traits should decline due to genetic drift which increases the frequency of mutations with deleterious effects in later adult stages. Since it is unlikely that identical deleterious mutations will increase in several independent populations, hybrid vigor for late-life fitness is expected in offspring obtained in crosses among populations selected for early-life fitness traits. We tested longevity of both sexes, female fecundity and male reproductive behavior for hybrid vigor by comparing hybrid and nonhybrid short-lived populations. Hybrid vigor was confirmed for male virility, mating speed and copulation duration, and longevity of both sexes at late ages. In contrast to males, the results on female fecundity in short-lived populations did not support mutation accumulation as a genetic mechanism for the evolution of this trait. Contrary to the prediction of this hypothesis, male mating ability indices and female fecundity in long-lived populations exhibited hybrid vigor at all assayed age classes. We demonstrate that nonhybrid long-lived populations diverged randomly regarding female and male reproductive fitness, indicating that sexually antagonistic selection, when accompanied with genetic drift for female fecundity and male virility, might be responsible for overriding natural selection in the independently evolving long-lived populations.

Emergency Contraception: What do Adolescent Males Know?

The high rate of adolescent unintended pregnancy has remained a significant public health concern. Adolescent male reproductive knowledge, attitudes and behavior has received very little research attention in comparison with their female counterparts, although they become sexually active at a younger age and have a higher incidence of sexual activity. Emergency contraception (EC) when used as recommended may reduce the risk of unintended pregnancy by 89-95%. Professional organizations including the American Academy of Pediatrics and the Society for Adolescent Health and Medicine, recommend that health care providers routinely offer information and counseling regarding EC to all patients, male and female.

Interplay of temperature and light influences wild guppy (Poecilia reticulata) daily reproductive activity

In this study we investigated the environmental regulation of daily reproductive activity of guppies (Poecilia reticulata). We observed male guppy reproductive behaviour for 17 days over three time periods (dawn, noon, and dusk) while recording natural variation in water temperature and light level. Water temperatures recorded during the experiments were highly variable (up to 7 °C per day), and there was a recurring pattern in daily variation for both light and temperature. Levels of activity were highest at dawn and similarly low during noon and dusk, but reproductive behaviour was recorded throughout the day. Mixed-effects models indicate that light and temperature affect reproductive behaviour differently at different times of the day, and can also have opposing effects. We suggest that the environmental heterogeneity of streams in Trinidad has led to a broad thermal tolerance, and has contributed to the high level of phenotypic plasticity in the guppy and its success as an invasive species. Furthermore, our results show that daily variation in temperature and its interaction with light should be considered in future studies of guppy reproductive behaviour. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 511–520.

Traumatic Insemination in Terrestrial Arthropods

Traumatic insemination is a bizarre form of mating practiced by some invertebrates in which males use hypodermic genitalia to penetrate their partner's body wall during copulation, frequently bypassing the female genital tract and ejaculating into their blood system. The requirements for traumatic insemination to evolve are stringent, yet surprisingly it has arisen multiple times within invertebrates. In terrestrial arthropods traumatic insemination is most prevalent in the true bug infraorder Cimicomorpha, where it has evolved independently at least three times. Traumatic insemination is thought to occur in the Strepsiptera and has recently been recorded in fruit fly and spider lineages. We review the putative selective pressures that may have led to the evolution of traumatic insemination across these lineages, as well as the pressures that continue to drive divergence in male and female reproductive morphology and behavior. Traumatic insemination mechanisms and attributes are compared across independent lineages.

Quantitative Ethogram of Male Reproductive Behavior in the South European Toothcarp Aphanius fasciatus

This work provides an ethogram of male reproductive behavior in the most widespread Mediterranean killifish, the South European toothcarp Aphanius fasciatus. The ethogram was obtained by video-recording the behavior of breeding groups under aquarium conditions. The behavioral analysis revealed the existence of seven behavioral states, with the expression of different forms of male-male competition: single and multiple courtship, single and multiple spawning, aggression, homosexual courtship, and post-mating cannibalism. These behaviors were organized into sequences that followed a first-order Markov chain. Single courtship was the most prevalent behavior, but more than one male, from two to five, could participate simultaneously in courtship and spawning. Results suggested that the breeding system is based on mate monopolization, with high levels of sperm competition and parasitic spawning. Results are discussed in light of the current literature on alternative mating tactics and male-male competition in teleost fishes.

Reproductive behavior of the male rose bitterling Rhodeus ocellatus as influenced by the operational sex ratio

Abstract Background Game theory predicts that as the operational sex ratio (OSR; the ratio of sexually active males to fertilizable females) increases, reproductive males may adopt alternative reproductive behaviors. Empirical studies indicated that alternative behaviors may differ for different species. In the present study, we investigated the influence of different male-biased OSRs on male reproductive behaviors shown by a freshwater fish, the rose bitterling Rhodeus ocellatus. Results Six levels of the OSR (1:1, 2:1, 3:1, 5:1, 7:1, and 9:1) were established, and male leading, aggression, and preoviposition ejaculation behaviors were recorded. Our experiments showed that at low OSRs, the leading behavior of male rose bitterling increased with an increasing OSR, reaching a maximum at an OSR of 3:1, and then decreased as the OSR further increased. In contrast, aggression and preoviposition ejaculation behavior continually increased with an increasing OSR. Notably, males possibly lost their territorial position to other males and became sneakers when facing more rivals. Conclusions These observations suggest that at lower OSRs, male rose bitterling mainly rely on leading behavior, while at higher OSRs, they increasingly adopt aggression and preoviposition ejaculation. Therefore, for the rose bitterling, (1) decreased leading behavior and (2) increased aggression and preoviposition ejaculation are two alternative responses in the face of an increasing OSR, which is a more straightforward strategy for facing an increased risk of sperm competition than that adopted by its congener, the European bitterling.

A Novel Method for Induction of Pairing inXenopusby Addition of Steroids into the Water

The African clawed frog, Xenopus laevis, is widely used in biological studies. Ovulation of Xenopus is normally induced by the injection of human chorionic gonadotropin (hCG) into the dorsal lymph sac of fully-grown female frogs. Previously, we reported a novel method for inducing Xenopus ovulation by adding a mixture of steroids into the surrounding water. In the present study, we demonstrate how to induce reproductive behavior in male frogs using the same methodology. The types and concentrations of steroids were evaluated, and the efficiency of the selected steroid for the induction of ejaculation was examined. New procedures were also examined for inducing mating by mixing both females and males activated by steroids. In male frogs, testosterone was effective for the induction of physiological changes, accumulation of melanin in the hands and induction of amplexus. Time course experiments revealed that eight hours were sufficient to induce male reproductive behavior and ovulation in females. Finally, we established an efficient means of inducing pairing in frogs that involved pre-treatment of frogs with salt solution followed by testosterone for males and a mixture of estradiol and progesterone for females. Although the numbers of oocytes obtained were relatively fewer than those resulting from hCG injection, the fertilization rate of eggs ovulated using the new treatment method was similar to that with eggs obtained by hCG-injection, and juveniles developed normally. In conclusion, we have developed a novel method to induce pairing in frogs without the need for injections.

Social interaction facilitates reproduction in male German cockroaches, Blattella germanica

Sociality can be beneficial for individuals because it may increase access to resources, provide greater protection from predators and create opportunities for mating. In some species, social conditions and experience also influence the physiology and behavioural responses of individuals. Although social facilitation of sexual maturation is poorly understood in insects, the German cockroach has served as an important model system for this phenomenon as group-housed females mature faster than solitary females. However, social modulation of male reproduction has not been investigated in this or any other nonpolyphenic insect species. We investigated the relative effects of social interactions and isolation on endocrine, reproductive and behavioural events during sexual maturation of B. germanica males. Results show that social interactions significantly facilitate juvenile hormone biosynthesis as well as protein production by the accessory reproductive glands, whereas isolation suppresses these processes. Other processes, such as accumulation of cuticular hydrocarbons, maturation of the male's courtship readiness and his readiness to copulate, appear to be relatively independent of social experience. However, both courtship and copulation latencies declined with age more in socially paired males than in isolated males. Our study is the first to reveal that social interactions have a profound effect on certain aspects of male reproductive physiology and behaviour in an insect species that does not exhibit phase or developmental polyphenism . • Social interactions affect male cockroach reproductive physiology and behaviour. • Group living facilitates juvenile hormone biosynthesis in adult males. • Group living facilitates protein production in adult male accessory reproductive glands. • Social conditions influence male sexual maturation. • Some events during sexual maturation are independent of male social experience.

SPERM COMPETITIVE ABILITY EVOLVES IN RESPONSE TO EXPERIMENTAL ALTERATION OF OPERATIONAL SEX RATIO

In naturally polygamous organisms such as Drosophila, sperm competitive ability is one of the most important components of male fitness and is expected to evolve in response to varying degrees of male-male competition. Several studies have documented the existence of ample genetic variation in sperm competitive ability of males. However, many experimental evolution studies have found sperm competitive ability to be unresponsive to selection. Even direct selection for increased sperm competitive ability has failed to yield any measurable changes. Here we report the evolution of sperm competitive ability (sperm defense-P1, offense-P2) in a set of replicate populations of Drosophila melanogaster subjected to altered levels of male-male competition (generated by varying the operational sex ratio) for 55-60 generations. Males from populations with female-biased operational sex ratio evolved reduced P1 and P2, without any measurable change in the male reproductive behavior. Males in the male-biased regime evolved increased P1, but there was no significant change in P2. Increase in P1 was associated with an increase in copulation duration, possibly indicating greater ejaculate investment by these males. This study is one of the few to provide empirical evidence for the evolution of sperm competitive ability of males under different levels of male-male competition.

Epidemiology and fitness effects of wood mouse herpesvirus in a natural host population

Rodent gammaherpesviruses have become important models for understanding human herpesvirus diseases. In particular, interactions between murid herpesvirus 4 and Mus musculus (a non-natural host species) have been extensively studied under controlled laboratory conditions. However, several fundamental aspects of murine gammaherpesvirus biology are not well understood, including how these viruses are transmitted from host to host, and their impacts on host fitness under natural conditions. Here, we investigate the epidemiology of a gammaherpesvirus in free-living wood mice (Apodemus sylvaticus) and bank voles (Myodes glareolus) in a 2-year longitudinal study. Wood mouse herpesvirus (WMHV) was the only herpesvirus detected and occurred frequently in wood mice and also less commonly in bank voles. Strikingly, WMHV infection probability was highest in reproductively active, heavy male mice. Infection risk also showed a repeatable seasonal pattern, peaking in spring and declining through the summer. We show that this seasonal decline can be at least partly attributed to reduced recapture of WMHV-infected adults. These results suggest that male reproductive behaviours could provide an important natural route of transmission for these viruses. They also suggest that gammaherpesvirus infection may have significant detrimental effects in wild hosts, questioning the view that these viruses have limited impacts in natural, co-evolved host species.

Rhythmic male reproductive behavior controls timing of courtship and mating in Laupala cerasina

In many organisms, mating behavior occurs at a particular time of day, which may be important for avoiding mate competition or interspecific mating. Crickets of the Hawaiian genus Laupala exhibit an unusually protracted courtship in which males produce a series of nuptial gifts prior to the species-typical time of mating. Mating time is one of several rhythmic behaviors that have diverged among closely related Laupala species, which exhibit an extremely high speciation rate. Mating rhythm may reflect direct selection on male and/or female sexual receptivity or the pleiotropic consequence of selection on other rhythmic behaviors. To examine the role of sexual rhythmicity in Laupala cerasina, we characterized the time boundaries or “circadian gate” of courtship and mating, as well as female phonotactic response to male song. We also examined which sex is responsible for mating rhythmicity by phase-shifting males relative to the female photophase. Our results demonstrate that mating behavior is gated by the end of the light phase. Time limits to female mating receptivity were not observed and thus male rhythm alone appears to be responsible for the timing of mating. Furthermore, when courtship is initiated later in the day, males produce fewer nuptial gifts and increase nuptial gift production rate while delaying mating, suggesting that the number of gifts a female receives is important to male reproductive success.

Perceived environmental threats as a factor in reproductive behavior: an examination of American youth

This study presents a test of general life history theory by estimating the association between perceived environmental threat (PET) and reproductive outcomes among American youth. Data for the study came from the National Longitudinal Survey of Youth 1997–2009, which consists of a nationally representative sample of youth. Analyses were based on a subsample of N=4748 respondents who were aged 12–14 years in 1997; reported having no biological children in 1997; and, for females, were not pregnant at the time of the 1997 interview. PET was measured using 11 questionnaire items that asked respondents about experiences with violent assaults from peers, witnessing violent assaults, and nonviolent crime victimization. First childbirth occurred earlier among respondents who reported higher PET in 1997. Average fertility during the study period was also higher among respondents with higher PET. Male and female respondents' reproductive behaviors were similarly associated with PET. However, only among female respondents was the association between PET and fertility moderated by the quality of the household environment.

Brain circuit imprints of developmental 17α-Ethinylestradiol exposure in guppies (Poecilia reticulata): Persistent effects on anxiety but not on reproductive behaviour

The effects of endocrine disruptors may vary with the timing of exposure. The physiological implications of adult exposure are present during and shortly after exposure while embryonic exposure can imprint changes manifested in adulthood. In this study, guppy (Poecilia reticulata) embryos were exposed to 2 and 20ng/L of 17α-ethinylestradiol during development via the mother and reared in clean water from gestation until 6months of age. As adults, fish exposed to 20ng/L during development showed significantly altered behaviour in the Novel Tank test, where anxiety is determined as the tendency to remain at the bottom upon introduction into an unfamiliar tank. 17α-ethinylestradiol treatment increased the latency time before swimming to the upper half of the tank and decreased the number of transitions to the upper half. In control females the basal stress behaviour responses were significantly higher than in males, as indicated by longer latency period and fewer and shorter visits to the upper half, supporting the importance of gonadal hormones for the behaviour. The anxiety increased, however, with treatment in both sexes, suggesting that the observed response is not entirely due to feminisation of the males. Shoaling behaviour, analysed as tendency to leave a shoal of littermates, was neither sex-differentiated nor changed by treatment. Also male reproductive behaviour, brain aromatase activity and testes histology, previously shown to respond to oestrogen exposure in adult guppy, were unaffected by the developmental treatment. This suggests that the stress system in the guppy is very sensitive to 17α-ethinylestradiol, which possibly causes an early organisational imprint on the brain circuit that regulates stress reactions.

Protracted Reproductive Seasonality in the Male Giant Panda (Ailuropoda melanoleuca) Reflected by Patterns in Androgen Profiles, Ejaculate Characteristics, and Selected Behaviors1

The female giant panda (Ailuropoda melanoleuca) experiences a brief (24-72 h) seasonal estrus, occurring once annually in spring (February-May). Our aim was to determine the existence and temporal profile of reproductive seasonality in the male of this species. The study was facilitated by 3 yr of access to eight giant panda males living in a large breeding center in China. Seasonal periods for the male were defined on the basis of female reproductive activity as prebreeding, breeding (early, peak, late), and nonbreeding seasons. Testes size, fecal androgen excretion, ejaculated sperm density, and frequency of reproductive behaviors (i.e., locomotion, scent marking, vocalizations) increased (P < 0.05) from the prebreeding period (October 1-January 31) to the early breeding season (February 1-March 21). Testes volume and sperm concentration were maximal from March 22 through April 15, a period coinciding with maximal female breeding activity. The occurrence of male reproductive behaviors and fecal androgen concentrations began declining during peak breeding and continued from April 16 through May 31 (late breeding period), returning to nadir throughout the nonbreeding interval (June 1-September 30). Reproductive quiescence throughout the latter period was associated with basal testes size/volume and aspermic ejaculates. Our results reveal that testes morphometry, fecal androgen excretion, seminal quality, and certain behaviors integrated together clearly demonstrate reproductive seasonality in the male giant panda. The coordinated increases in testes size, androgen production, sperm density, and sexual behaviors occur over a protracted interval, likely to prepare for and then accommodate a brief, unpredictable female estrus.

Impairments in aromatase expression, reproductive behavior, and sperm quality of male fish exposed to 17β‐estradiol

Growing evidence shows that environmental estrogen can reach levels that are high enough to exert adverse reproductive effects on wild fish populations. The authors report different parameters of male reproductive behavior, brain, and gonadal aromatase expression, as well as sperm quality in an internally fertilizing fish species (Jenynsia multidentata, Jenyns) exposed to environmentally relevant concentrations of 17β-estradiol (E(2) ). Adult males were exposed to 0, 50, 100, and 250 ng/L E(2) over 28 d. The authors' findings demonstrate that E(2) exposure resulted in a very clear increase in brain aromatase transcript abundance at all assayed concentrations compared with control; however, no effects on gonadal aromatase expression were observed. Behavioral measures revealed increased sexual activity at 50 ng/L but not 100 or 250 ng/L E(2) . In contrast to the molecular and behavioral responses, the condition factor, gonadosomatic index, and sperm quality were unaltered by E(2) exposure. The results from the present work suggest that E(2) affects some aspects of the reproductive biology of J. multidentata. These modifications in the reproductive biology caused by exposure to E(2) could potentially lead to long-term effects at population levels that may not always be immediately evident. To the best of the authors' knowledge, this is the first report on the combined effect of E(2) on aromatase expression, sexual behavior, and sperm parameters in fish.

Sexual experience affects reproductive behavior and preoptic androgen receptors in male mice

Reproductive behavior in male rodents is made up of anticipatory and consummatory elements which are regulated in the brain by sensory systems, reward circuits and hormone signaling. Gonadal steroids play a key role in the regulation of male sexual behavior via steroid receptors in the hypothalamus and preoptic area. Typical patterns of male reproductive behavior have been characterized, however these are not fixed but are modulated by adult experience. We assessed the effects of repeated sexual experience on male reproductive behavior of C57BL/6 mice; including measures of olfactory investigation of females, mounting, intromission and ejaculation. The effects of sexual experience on the number of cells expressing either androgen receptor (AR) or estrogen receptor alpha (ERα) in the primary brain nuclei regulating male sexual behavior was also measured. Sexually experienced male mice engaged in less sniffing of females before initiating sexual behavior and exhibited shorter latencies to mount and intromit, increased frequency of intromission, and increased duration of intromission relative to mounting. No changes in numbers of ERα-positive cells were observed, however sexually experienced males had increased numbers of AR-positive cells in the medial preoptic area (MPOA); the primary regulatory nucleus for male sexual behavior. These results indicate that sexual experience results in a qualitative change in male reproductive behavior in mice that is associated with increased testosterone sensitivity in the MPOA and that this nucleus may play a key integrative role in mediating the effects of sexual experience on male behavior.

Dissociated functional pathways for appetitive and consummatory reproductive behaviors in male Syrian hamsters

In many species, including Syrian hamsters, the generation of male reproductive behavior depends critically on the perception of female odor cues from conspecifics in the environment. The behavioral response to these odors is mediated by a network of steroid-sensitive ventral forebrain nuclei including the medial amygdala (MA), posterior bed nucleus of the stria terminalis (BNST) and medial preoptic area (MPOA). Previous studies have demonstrated that each of these three nuclei is required for appropriate sexual behavior and that MA preferentially sends female odor information directly to BNST and MPOA. It is unknown, however, how the functional connections between MA and BNST and/or MPOA are organized to generate different aspects of reproductive behavior. Therefore, the following experiments used the asymmetrical pathway lesion technique to test the role of the functional connections between MA and BNST and/or MPOA in odor preference and copulatory behaviors. Lesions that functionally disconnected MA from MPOA eliminated copulatory behavior but did not affect odor preference. In contrast, lesions that functionally disconnected MA from BNST eliminated preference for volatile female odors but did not affect preference for directly contacted odors or copulatory behavior. These results therefore demonstrate a double dissociation in the functional connections required for attraction to volatile sexual odors and copulation and, more broadly, suggest that appetitive and consummatory reproductive behaviors are mediated by distinct neural pathways.

“Nice guys finish last”: Influence of mate choice on reproductive success in Long–Evans rats

The present study was designed to determine if male physiology and male reproductive behavior predict reproductive success in Long–Evans rats. Mating behavior was observed in sexually naïve, naturally cycling female rats during behavioral estrous that were given the opportunity to mate with two males simultaneously. DNA analysis of offspring born following these mating encounters was used to identify the paternity of each pup. In order to assess the effect of mate choice during these mating encounters on reproductive success, one male rat in each pair was categorized as the preferred mate if the female spent more time (>50%) with him during the mating test of the present study. Furthermore, each male in the pairs was categorized as “attractive” or “non-attractive” by computing the number of females that preferred each male across many mating tests. Similar to results reported in Lovell et al. (2007), during 76% of these mating tests the same male rat in each pair was preferred by different female rats. Overall attractiveness of individual male rats predicted reproductive success in the present study. Interestingly, “attractive” males sired significantly FEWER pups than “non-attractive” males. Neither behavioral (e.g., latency to first sexual stimulation, number of sexual stimulations) nor physiological measures (e.g., body weight, urinary testosterone levels) of male rats predicted their reproductive success. In conclusion, the present results indicate that certain features of some males are more attractive to females, but attractive males are at a reproductive disadvantage (as measured by the number of pups sired). Although basal urinary testosterone levels did not differ between males that sired the majority of pups in a litter and males that sired few or none of the pups in a litter, aggression and/or other physiological measures of fertility (e.g., penile reflexes) may differ between males that are attractive to females and those that have a reproductive advantage.

Unravelling complex associations between testosterone and parasite infection in the wild

Summary1. Testosterone has emerged as an important mechanism linking variation in male reproductive behaviour to parasite infection in vertebrates, and there are numerous pathways by which testosterone can influence infection risk, particularly in free‐living animals.2. The immunocompetence handicap hypothesis posits that the positive effects of testosterone on sexual signalling and behaviour are traded off with negative effects on immune function. While this obligate trade‐off may sometimes explain the association between testosterone and parasite infection, testosterone–parasite relationships may also be mediated by correlated changes in stress, condition and exposure to parasites.3. In this study, we explored associations between testosterone and reproductive behaviour, immune function and parasitism in free‐living Grant’s gazelle (Nanger granti). In particular, we examined how stress (glucocorticoids), behaviour and condition might mediate associations between testosterone, immunity and parasitism.4. We found that variation in endogenous testosterone in male gazelle was correlated with mating behaviour in terms of sexual signal intensity (horn size) and resource‐holding potential (territoriality). We also showed that these same levels of testosterone were associated with immunity and parasite infection, but associations between testosterone, immunity and parasitism were complex. Testosterone was negatively associated with adaptive immunity, but positively associated with innate immunity. Relationships between testosterone and parasitism varied for different parasites.5. Our results suggest that the effects of testosterone on male immunity are not universally suppressive and that immunoenhancement may also occur. In addition, testosterone–parasite relationships vary depending on the parasite, most likely due to the opposing effects of testosterone on different aspects of immunity and indirect effects on parasite exposure mediated by changes in behaviour.