Effects of Exogenous Testosterone on Parental Care Behaviours in Male Bluegill Sunfish (Lepomis macrochirus)

Androgens are known to mediate aggressive and defensive behaviour in many vertebrate species. However, high concentrations of androgens might also conflict with the expression of nurturing behaviours and therefore a trade‐off can exist between aggressive and nurturing behaviours during parental care. We explored the role of testosterone in paternal care in bluegill sunfish (Lepomis macrochirus), where males provide both sole defence of the young from predators and sole nurturing behaviour such as fanning of the eggs. At the onset of parental care, we manipulated testosterone levels in males using testosterone propionate implants. We then observed the frequency of nurturing and aggressive behaviours displayed by the males over 6 d of parental care. Testosterone‐implanted fish were more aggressive when presented with a brood predator, performing more bites, opercular flares and lateral displays than control males. Testosterone‐implanted males, however, were not less nurturing than control fish, performing similar levels of fanning and nest‐cleaning behaviours. Thus, our results support a positive relationship between testosterone and paternal aggression but no testosterone‐mediated trade‐off between paternal nurturing and aggression.     

Changes in male courtship intensity and androgen levels during brood cycling in the blenniid fish Rhabdoblennius nitidus

Androgens, for example testosterone, are major hormones that affect male courtship activity, territorial activity, sexual dimorphism, and reproductive tactics; they reach, and are maintained at, a sufficient level to express such sexual traits at the appropriate time for reproductive success. This study examined the effects of androgen levels (testosterone and 11-ketotestosterone) on male brood cycling with two distinct reproductive phases (i.e. courtship and parental phases) of a paternal brooding blenny Rhabdoblennius nitidus. Our study showed that time spent on courtship behaviour and androgen levels decreased with progress of brood cycling. In addition, time spent on courtship behaviour of males administered cyproterone acetate, an anti-androgen, was shorter than that of control males. These results indicate that the brood cycling is affected by the change in androgen levels. The study also showed that androgen levels decreased after acquisition of the eggs, irrespective of available spawning space in the nests. This result suggests that the presence of eggs themselves may be a trigger for the shift from the courtship phase to parental phase.     

Neither testosterone levels nor aggression decrease when the male Mongolian gerbil (Meriones unguiculatus) displays paternal behavior

The first studies that correlated mammalian paternal behavior and testosterone levels indicated that the concentration of this steroid hormone decreases when males exhibit paternal care. However, recent studies have also shown that testosterone levels do not decrease when males display paternal behavior. In this study, we measured testosterone levels in plasma throughout the reproductive cycle of the Mongolian gerbil. Testosterone concentrations were correlated with paternal care as well as aggression. We also examined whether there is a trade-off between paternal behavior and aggression in this mammal. Our results show that Mongolian gerbil testosterone levels do not decrease when the males give paternal care. Likewise, male Mongolian gerbils exhibit high levels of aggression while displaying paternal behavior, indicating that there is no trade-off between aggression and paternal behavior. More studies are needed to determine whether testosterone is involved in the regulation of paternal behavior in this rodent.     

Do Male Desert Gobies Compromise Offspring Care to Attract Additional Mating Opportunities?

Males often play a critical role in offspring care but the time and energy invested in looking after young can potentially limit their ability to seek out additional mating opportunities. Recent studies, however, suggest that a conflict between male parental effort and mating effort may not always be inevitable, especially if breeding occurs near the nest, or if parental behaviours are under sexual selection. Accordingly, we set out to experimentally investigate male care and courtship in the desert goby Chlamydogobius eremius, a nest-guarding fish with exclusive paternal care. Despite courtship occurring near the nest, we found that when egg-tending males were given the opportunity to attract additional females, they fanned their eggs less often, engaged in shorter fanning bouts, and spent more of their time outside their nests courting. Our findings highlight the importance of understanding the circumstances under which reproductive tradeoffs are expected to occur and how these, in turn, operate to influence male reproductive decisions.     

Steroid hormones and paternal care in the plainfin midshipman fish (Porichthys notatus)

The present study investigated the relationship between plasma steroid hormone levels and the expression ofpaternal behavior in the plainfin midshipman fish (Porichthys notatus), where males may simultaneously care for multiple clutches in different stages of development. Blood samples were collected from free-living parental males during that part of the breeding season when males may be found in various stages of parental care. Plasma 11-ketotestosterone levels were significantly higher in males with empty nests and nests containing only eggs than in males with nests containing embryos. All males with nests containing embryos had undetectable testosterone levels, whereas testosterone levels were detectable in many males with empty nests or nests containing only eggs. Estradiol levels were detectable in only a few males from nests with no eggs or nests containing only eggs. Cortisol levels were not correlated with stage of paternal care or with handling time. These results follow the frequently reported vertebrate pattern of declining androgen levels over the course of the breeding season or during the period of parental care. However, many male midshipman guarding nests containing only eggs had androgen levels similar to those of males whose nests contained no offspring. Thus the pattern of androgen levels exhibited by reproductively active parental male midshipman may reflect a compromise between investment in paternal care versus courtship and/or territoriality.     

Behavioural insensitivity to supplementary testosterone during the parental phase in the chestnut-collared longspur,Calcarius ornatus

In seasonally breeding male birds that show paternal care, plasma testosterone (T) peaks in the early spring coincident with territory establishment and pair bonding. Once nests are initiated, T declines precipitously and remains low as nestlings hatch and males become parental. A growing body of evidence suggests there is a trade-off between a male's level of T and his expression of paternal care: high T enhances sexual behaviour but reduces paternal care. Male chestnut-collared longspurs show high levels of paternal care. They feed and brood young, act as nest sentries and aggressively defend the nest against predators. We experimentally altered males' plasma levels of T such that the early spring T peak was extended through the parental phase. T enhanced song behaviour typical of the sexual phase and decreased nest sentry behaviour during incubation, but did not reduce brooding or feeding of nestlings. Thus, males responded behaviourally to T during incubation, but, unlike most other temperate-breeding birds studied, did not respond to T after eggs hatched. Based on these data and similar results in an Arctic passerine, we suggest that the pattern of males' reduced responsiveness to T during the nestling phase may reflect the relative importance of male care to nest success in this species, or a phylogenetic constraint common to the genusCalcarius . Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free-living males with high testosterone are more immunocompetent

The immunocompetence handicap hypothesis proposes that the immunosuppressive effect of testosterone enforces honesty of sexual signalling via a physiological trade-off between signal intensity and immunocompetence. However, evidence that testosterone is immunosuppressive is scant, particularly in birds. I studied the correlation between immunocompetence and testosterone in superb fairy-wrens (Malurus cyaneus), a species with intense intersexual selection. Males are seasonally dichromatic and testosterone increases during the moult from dull brown eclipse plumage into bright nuptial plumage. I determined the primary antibody response to immunization with sheep red blood cells (SRBCs) in (i) control and testosterone-implanted males in captivity, and (ii) a cross-section of free-living males with basal and elevated testosterone (in eclipse plumage, moulting and in nuptial plumage). Experimental treatment with testosterone decreased the likelihood of an antibody response to SRBCs in captive birds. In contrast, free-living males which had acquired the nuptial plumage and had naturally elevated testosterone were more likely to respond to SRBCs than males in eclipse plumage with basal testosterone levels. The association between higher immunocompetence and higher immunosuppressive testosterone could arise if both are positively correlated with male phenotypic quality In addition, the association could result if males compensate for potential immunosuppression by enhancing their humoral immune responses, particularly since high testosterone is linked to other demanding activities such as moulting and courtship displays.     

Should advertising parental care be honest?

Species with paternal care show less exaggerated sexual ornamentation than those in which males do not care, although direct benefits from paternal care can vastly exceed the indirect benefits of mate choice. Whether condition-dependent handicaps can signal parenting ability is controversial. The good-parent process predicts the evolution of honest signals of parental investment, whereas the differential-allocation model suggests a trade-off between the attractiveness of a mate and his care-provisioning. I show that both alternatives can arise from optimal allocations to advertisement, parental investment and future reproductive value of the male, and that the male''s marginal fitness gain from multiple matings determines which option should apply. The marginal gain is diminishing if opportunities for polygyny or extra-pair copulations are limited. Advertisement is then expected to be modest and honest, indicating genetic quality and condition-dependent parental investment simultaneously. Increasing marginal gains are likely to be related to cases where genetic quality has a significant influence on offspring fitness. This alternative leads to differential allocation with stronger advertisement, more frequent extra-pair copulations, and diminished male care. Reliability is also reduced if allocation benefits have thresholds, e.g. if there is a minimum body condition required for survival, or if females use a polygyny-threshold strategy of mate choice.     

Life History Trade-Offs and Behavioral Sensitivity to Testosterone: An Experimental Test When Female Aggression and Maternal Care Co-Occur

Research on male animals suggests that the hormone testosterone plays a central role in mediating the trade-off between mating effort and parental effort. However, the direct links between testosterone, intrasexual aggression and parental care are remarkably mixed across species. Previous attempts to reconcile these patterns suggest that selection favors behavioral insensitivity to testosterone when paternal care is essential to reproductive success and when breeding seasons are especially short. Females also secrete testosterone, though the degree to which similar testosterone-mediated trade-offs occur in females is much less clear. Here, I ask whether testosterone mediates trade-offs between aggression and incubation in females, and whether patterns of female sensitivity to testosterone relate to female life history, as is often the case in males. I experimentally elevated testosterone in free-living, incubating female tree swallows (Tachycineta bicolor), a songbird with a short breeding season during which female incubation and intrasexual aggression are both essential to female reproductive success. Testosterone-treated females showed significantly elevated aggression, reduced incubation temperatures, and reduced hatching success, relative to controls. Thus, prolonged testosterone elevation during incubation was detrimental to reproductive success, but females nonetheless showed behavioral sensitivity to testosterone. These findings suggest that the relative importance of both mating effort and parental effort may be central to understanding patterns of behavioral sensitivity in both sexes.     

Patterns of Parental Investment and Sexual Selection in Teleost Fishes: Do They Support Bateman's Principles?

Bateman demonstrated differences in variance for fertility andmating success between the sexes, with males usually havinga greater variance than females. Thus in general, male reproductivesuccess increases with number of mates acquired. These resultshave been referred to as "Bateman's principles" and taken togetherwith other parameters (e.g., relative parental investment) havebeen proposed to estimate a component of sexual selection. Forthis review I examine patterns of parental care and sexual selectionin teleost fishes (substrate brooding and with internal fertilization).I present data for the pumpkinseed sunfish Lepomis gibbosus,in which I estimated cost of paternal care and compared directmeasures of the intensity of selection on possible sexuallyselected traits to measures of sexual selection based on Bateman'sprinciples. Despite high levels of paternal care in substrate brooding fishes,sexual selection tends to act more strongly on males than onfemales, which suggests that maternal investment is higher thanpaternal investment and that parental care does not limit thereproductive rate for males. In pumpkinseed sunfish, selectionfavors parents with high levels of defense that may excludepredators more effectively and, as suggested by Bateman's measures,alternative reproductive strategies may decrease the opportunityfor sexual selection within the parental strategy. In teleostfishes with internal fertilization, patterns of parental investmentand intensity of sexual selection seem to support Bateman'sprinciples, but further studies using these systems and thesemeasures of selection will improve the understanding of factorsaffecting the intensity of sexual selection and its relationto mating systems.     

Testosterone affects reproductive success by influencing extra-pair fertilizations in male dark-eyed juncos (Aves: Junco hyemalis)

Monogamous male birds typically allocate less effort to courtship and more to parental behaviour than males of polygynous species. The seasonal pattern of testosterone (T) secretion varies accordingly. Monogamous males exhibit a spring peak in plasma T followed by lower levels during the parental phase, while males of polygynous species continue to court females and maintain T at higher levels. To determine whether testosterone underlies the trade-off between mating and parental effort, we treated male dark-eyed juncos (Junco hyemalis) with exogenous T and compared the reproductive success (RS) of T-treated males (T-males) to that of controls. T-males had lower apparent annual RS than controls, probably because elevated T reduced parental care. Nevertheless, annual genetic RS of the treatment groups was similar because (i) T-males suffered fewer losses in genetic RS due to extra-pair fertilizations (EPFs), and (ii) T-males gained more genetic RS through their own EPFs. This is the first hormonal manipulation of an avian phenotype shown to have influenced male RS through EPFs. Together with other studies, it suggests that testosterone may have mediated the evolution of inter- and intraspecific differences in allocation of reproductive effort to mate attraction and parental care.     

Facultative paternal investment in the polyphenic beetle Onthophagus taurus: the role of male morphology and social context

Members of a population often differ significantly in theirparental investment. Such variation is generally believed tohave important consequences for mating system evolution andhas been suggested to play an important role in the evolutionof some secondary sexual traits and displays. Recent studiessuggest that individuals are able to adjust the intensity and kindof parental investment they provide according to the breedingconditions they encounter. As a consequence, between-individualvariation in parental investment may depend more on externalconditions than previously thought for these taxa. This mayhave important implications for current perspectives on therole of differential parental investment in the evolution andmaintenance of certain mating systems and sexual selection regimes.Here I quantify patterns of variation in paternal investmentas a function of social conditions in a species of beetle thatis dimorphic for male horn morphology. I demonstrate that undercertain conditions (namely, the absence of other males), paternalassistance covaries with male morphology, with horned males investingsubstantially more time in assisting females than hornless males.I also show that the magnitude of differences in paternal investmentbetween male morphs varies in response to external conditions.In the presence of other males, paternal assistance was negligiblefor both male morphs, who instead invested substantially andequally in mate-securing behaviors. I use my findings to discussthe significance of variation in paternal assistance for onthophaginemating systems and evaluate ideas proposed to explain the evolutionof alternative morphologies in the genus Onthophagus.     

Understanding reversals in the relative strength of sexual selection on males and females: a role for sperm competition?

Sperm competition affects sexual selection intensity on males, but models suggest it cannot affect the relative intensity of sexual selection on males compared to females. However, if sperm competition depresses the payoff for male multiple mating, it could affect the relative intensity of sexual selection and even cause sexual selection to be more intense on females than males (reversal of typical pattern). To evaluate how sperm competition, energy availability, and parental investment affect the intensity of sexual selection on each sex, I constructed a simulation model using the relationship between fecundity and number of mates to estimate sexual selection gradients. Unlike earlier models, I include a trade-off between paternal investment and sperm competition ability. The amount of energy available for reproduction affects the sexual selection gradient for each sex. Reversals in the sex experiencing stronger sexual selection do occur when additional paternal investment reduces a male's ability to compete for fertilizations within females. The shape of the distribution of mates for each sex (determined by mate competition) is also important. Output from the model is qualitatively similar to empirical data from insects with paternal investment. This model challenges previous thinking about the role of sperm competition in sex-role reversal.     

鸟类的父本行为及其内分泌调控机制研究进展

飞翔能力帮助鸟类极大地扩展了生存空间,使其能够迅速移动来应对各种局部环境的变化。然而,个体发育早期,不具备这样的能力,使其极不适应环境,需要大量的亲本照顾。不同于哺乳类动物主要依赖母本行为,雄性鸟类表现出了大量的父本行为,诸如筑巢行为、孵卵行为和育雏行为等。针对这一系列行为及其调控机制,本文进行了归纳:1)筑巢行为常常伴随着雄性的求偶行为,睾酮对两种行为均有促进作用,加压素也促进筑巢行为。2)孵卵行为可以传递热量,保护和帮助子代发育;同时会刺激泌乳素释放,而泌乳素又会进一步促进孵卵行为;此时的睾酮水平下降。3)育雏行为与雏鸟的发育速度有关,晚成鸟需要更多的父本照顾;与孵卵行为的调控相似,泌乳素升高,睾酮降低;孕酮也参与调控父本行为。4)环境压力通过影响皮质酮和泌乳素水平的变化,调节鸟类的父本行为。综上,在鸟类父本行为形成和表现过程中,睾酮和泌乳素先后发挥着主要的调控作用,并且受到环境压力的影响。然而,在神经内分泌水平上,研究非常缺乏,需要加强。     

Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies

Polyandry, where females mate with multiple males, means that a male''s reproductive success will depend both on his ability to acquire mates and the ability of his sperm to compete effectively for fertilizations. But, how do males partition their reproductive investment between these two episodes of selection? Theory predicts that increases in ejaculate investment will come at a cost to investment in other reproductive traits. Although evidence revealing such trade-offs is accumulating, we know little about their genetic basis. Here, I report patterns of genetic (co)variation for a range of traits subject to pre- and post-copulatory sexual selection in the guppy Poecilia reticulata, a promiscuous livebearing fish in which males alternate between courtship and sneak matings to obtain copulations. The analyses of genetic variation and covariation for these behaviours revealed a strong genetic predisposition for one tactic over the other. Both mating tactics were also strongly genetically integrated with the level of sexual ornamentation and ejaculate quality. Males that predominantly performed sneak matings were less ornamented but had faster swimming sperm than those that predominantly used courtship. These patterns of genetic variation and covariation reveal potential evolutionary constraints on the direction of selection of pre- and post-copulatory traits, and support sperm competition theory by revealing a trade-off between sexual attractiveness and investment in ejaculates.     

Testosterone response to courtship predicts future paternal behavior in the California mouse, Peromyscus californicus

In the monogamous and biparental California mouse (Peromyscus californicus), paternal care is critical for maximal offspring survival. Animals form pair bonds and do not engage in extrapair matings, and thus female evaluation of paternal quality during courtship is likely to be advantageous. We hypothesized that male endocrine or behavioral response to courtship interactions would be predictive of future paternal behavior. To test this hypothesis, we formed 20 pairs of California mice, and evaluated their behavior during the first hour of courtship interactions and again following the birth of young. We also collected blood from males at baseline, 1 hr after pairing, 3 weeks paired, and when young were 4 days old to measure testosterone (T). We found that male T-response to courtship interactions predicted future paternal behavior, specifically the amount of time he huddled over young when challenged by the temporary removal of his mate. Males that mounted T increases at courtship also approached pups more quickly during this challenge than males who had a significant decrease in T at courtship. Proximity of the male and female during courtship predicted paternal huddling during a 1-hr observation, and a multiple regression analysis revealed that courtship behavior was also predictive of birth latency. We speculate that male T-response to a female in P. californicus is an honest indicator of paternal quality, and if detectable by females could provide a basis for evaluation during mate choice.     

Devoted fathers or selfish lovers? Conflict between mating effort and parental care in a harem‐defending arachnid

When there is a temporal trade‐off between mating effort and parental care, theoretical models predict that intense sexual selection on males leads to reduced paternal care. Thus, high‐quality males should invest more in mating effort because they have higher chances of acquiring mates, whereas low‐quality males should bias their investment towards parental care. Once paternal care has evolved, offspring value should also influence males’ decisions to invest in offspring attendance. Here, we performed a manipulation under field conditions to investigate the factors that influence male allocation in either mating effort or parental care. We predicted that facultative paternal care in the harem‐holding harvestman Serracutisoma proximum would be negatively influenced by male attractiveness and positively influenced by offspring value. We found that attractive males were less likely to engage in egg attendance and that the higher the perceived paternity, the higher the caring frequency. Finally, egg mortality was not related to caring frequency by males, but predation pressure was much lower than that recorded in previous studies with the same population. Thus, the benefits of facultative male care may be conditional to temporal variation in the intensity of egg predation. In conclusion, males adjust their investment in either territory defence or egg attendance according to their recent mating history and perceived paternity. Our findings suggest that exclusive paternal care can evolve from facultative paternal care only if the trade‐off between mating effort and parental care is circumvented.     

Circulating androgens are influenced by parental nest defense in a wild teleost fish

While social interactions influence vertebrate endocrine regulation, the dynamics of regulation in relation to specific behaviors have not been clearly elucidated. In the current study, we investigated whether androgens (testosterone) or glucocorticoids (cortisol) play a functional role in aggressive offspring defense behavior in wild smallmouth bass (Micropterus dolomieu), a teleost fish with sole paternal care. We measured circulating testosterone and cortisol concentrations in plasma samples taken from parental males following a simulated nest intrusion by a common nest predator, the bluegill sunfish (Lepomis macrochirus). To understand whether endocrine regulation changes across the parental care period, we looked both at males guarding fresh eggs and at males guarding hatched embryos. Plasma testosterone levels increased in males subjected to a simulated nest intrusion when compared to sham controls. Testosterone concentrations in males guarding embryos were lower than in males guarding fresh eggs, but circulating testosterone was positively correlated with the level of aggression towards the nest predator at both offspring development stages. However, there was no increase in cortisol levels following a simulated nest intrusion, and no relationship between cortisol and any measured parameter. These results suggest that androgens play an important role in promoting aggressive nest defense behavior in teleost fish.     

Vigorously courting male sticklebacks are poor fathers

Male threespine sticklebacks (Gasterosteus aculeatus) that are unsuccessful at hatching eggs may provide insufficient parental care or have unhealthy or unfertilized eggs. In this study, most males that were unsuccessful at hatching eggs appeared to be poor fathers because they depleted their energy reserves by vigorously courting females and by maintaining intense nuptial coloration during courtship and parental care, leading to reduced fanning of the eggs. Unsuccessful males differed from successful males by investing more in obtaining a clutch of eggs and less in the eggs once they had them, suggesting a trade-off between investing in courtship and investing in paternal care. Received: 14 August 1998 / Received in revised form: 26 August 1999 / Accepted: 6 September 1999     

Care of young, aggressiveness, and secretion of testosterone in male rodents: A correlation analysis

To test the current hypotheses on the relationship between the mating system, reproductive strategy, aggression, and secretion of testosterone, a comparative study of interactions in pair encounters, the level of parental care, and the gonadal testosterone level in males was performed in six rodent species (Clethrionomys rutilus, Meriones meridianus, Microtus arvalis, Lagurus lagurus, Lasiopodomys mandarinus, and Meriones unguiculatus) with different types of spatial-and-ethological population structures (SEPSs). It is shown that this dependence is absent in species with promiscuous mating and dominance hierarchy among males (C. rutilus and M. meridianus, SEPS type II). A trade-off, or negative correlation, was found in M. arvalis—a species with weak pair bonds and male competition for receptive females (SEPS type III). In species with persistent pair bonds and structured family groups (L. mandarinus and M. unguiculatus, SEPS type IV), no inverse relationship between the secretion of testosterone and paternal behavior was found either. Moreover, in male L. mandarinus androgens appear to stimulate paternal care.