Differences in prolactin levels between three alternative male reproductive tactics in striped mice (Rhabdomys pumilio)

In male fishes, birds and mammals, increased prolactin secretion is thought to play a role in species showing paternal behaviours. This hypothesis was investigated in the striped mouse (Rhabdomys pumilio). This paper compares serum prolactin levels in 71 free-living male striped mice following three different reproductive tactics: (i) paternal group-living breeders, (ii) alloparental philopatric group-living males, and (iii) roaming non-paternal solitary males. Prolactin levels of breeding males were significantly higher than that of roamers. Alloparental philopatric males had low prolactin levels, which concur with studies of cooperatively breeding mammals, but contrasts with studies of cooperatively breeding birds. Both breeding males and females showed a decrease in prolactin levels after the breeding season, but not alloparental philopatric males. Prolactin levels were correlated with neither corticosterone levels nor age. These results are in agreement with the hypothesis that prolactin is one proximate mechanism of male reproductive tactics, possibly regulating differences in male parental care.     

Changes in Paternal Responsiveness of Prairie Voles (Microtus ochrogaster) in Response to Olfactory Cues and Continuous Physical Contact with a Female

In mammals, paternal care is rarely displayed, and we know little about the mechanisms regulating this behavior. Prairie voles (Microtus ochrogaster) are ideal mammals for the study of paternal behavior because they are a monogamous, bi‐parental species that is easily raised in the laboratory. Paternal responsiveness occurs at moderate levels in sexually‐naive voles and is heightened following a short cohabitation period of 72 h with a female. To determine how increased levels of paternal care are maintained after the initial cohabitation period, we tested the paternal behavior of males that were housed in isolation, were in physical contact with a female, or were exposed to various olfactory cues. The results indicate that the absence of odor cues from a female did not diminish the male’s motivation to care for infants following the initial cohabitation period. In contrast, odor cues from a male appeared to negatively influence the male’s paternal tendencies. The data also show that males that had continuous physical contact with a female spent more time responding paternally and more time hovering over the young compared to males that were housed alone. Together, these results suggest that although paternal behavior is maximized in response to continuous physical contact with females, olfactory cues may not be necessary for the maintenance of heightened paternal behavior.     

`Little Chipmunk' Syndrome? Male Body Size and Dominance in Captive Yellow‐Pine Chipmunks (Tamias amoenus)

In mammals, large males are often assumed to have higher mating success because they have greater success at contest competition. This relationship is often used to explain the prevalence of male-biased sexual size dimorphism in mammals. However, in many small vertebrates, large individuals are not always dominant. Using staged dyadic encounters, we examined the relationship between male body size and social dominance in captive male yellow-pine chipmunks ( Tamias amoenus ), a species with female-biased sexual size dimorphism. The yellow-pine chipmunk has a mating system in which males participate in mating chases and dominant males may have an advantage in acquiring matings with oestrous females. Captive male chipmunks were aggressive in only 28% of 144 paired encounters; however, several lines of evidence indicated that smaller chipmunks were dominant over large chipmunks: (1) small males were dominant in more dyads than large males; (2) within dyads, dominant males were smaller than subordinate males; and (3) small males performed more aggressive behaviour than large males. These results are not consistent with the prediction that large males are typically dominant. If large chipmunks are able to gain matings with females because of qualities other than dominance (such as the ability to successfully find and/or chase receptive females), then the costs of aggression to large chipmunks may outweigh any potential benefits. Small males, but not large males, may improve their mating success by being aggressive.     

Mortality costs of sexual selection and parental care in natural populations of birds

Abstract Is the cost of reproduction different between males and females? On the one hand, males typically compete intensely for mates, thus sexual selection theory predicts higher cost of reproduction for males in species with intense male‐male competition. On the other hand, care provisioning such as incubating the eggs and raising young may also be costly, thus parental care theory predicts higher mortality for the care‐giving sex, which is often the female. We tested both hypotheses of reproductive costs using phylogenetic comparative analyses of sex‐specific adult mortality rates of 194 bird species across 41 families. First, we show that evolutionary increases in male‐male competition were associated with male‐biased mortalities. This relationship is consistent between two measures of mating competition: social mating system and testis size. Second, as predicted by the parental cost hypothesis, females have significantly higher adult mortalities (mean ± SE, 0.364 ± 0.01) than males (0.328 ± 0.01). However, the mortality cost of parental care was only detectable in males, when the influence of mating competition was statistically controlled. Taken together, our results challenge the traditional explanation of female‐biased avian mortalities, because evolutionary changes in female care were unrelated to changes in mortality bias. The interspecific variation in avian mortality bias, as we show here, is driven by males, specifically via the costs of both mating competition and parental care. We also discuss alternative hypotheses for why most birds exhibit female‐biased mortalities, whereas in mammals male‐biased mortalities predominate.     

Exogenous testosterone inhibits several forms of male parental behavior and stimulates song in a monogamous songbird: the blue-headed vireo (Vireo solitarius)

Natural variation in circulating testosterone is thought to play a role in creating inter- and intraspecific variation in paternal care in birds. Experimental elevation of plasma testosterone in males has reduced rates of male care in many species. However, a small number of studies suggest that male care is not inhibited by testosterone when there appears to be strong selection for male care. Both genetic monogamy and male incubation are thought to be the result of selection for biparental care, yet the sensitivity of male care to inhibition by T had not been examined in a species with both characteristics. Male blue-headed vireos have been shown to be strictly monogamous and provide extensive parental care, including incubation. Males received subcutaneous implants of testosterone, flutamide (an anti-androgen), or empty controls. Consistent with previous studies, testosterone treatment decreased the relative contribution to incubation by males and increased the average duration that the nest was left unattended during incubation, relative to control and flutamide treatments. The relative and absolute rates of feeding offspring and nest sanitation by T-treated males also decreased relative to controls. Flutamide-treated males incubated eggs and brooded young more than testosterone-treated males, with control males performing at intermediate values. Testosterone-treated males sang more often and at higher rates, and flutamide-treated males sang less often, than controls. These results demonstrate that even in a strictly monogamous songbird with biparental incubation, all forms of paternal care remain sensitive to elevated plasma testosterone, suggesting a shift from parental effort to mating effort.     

Free-Ranging Male Koalas Use Size-Related Variation in Formant Frequencies to Assess Rival Males

Although the use of formant frequencies in nonhuman animal vocal communication systems has received considerable recent interest, only a few studies have examined the importance of these acoustic cues to body size during intra-sexual competition between males. Here we used playback experiments to present free-ranging male koalas with re-synthesised bellow vocalisations in which the formants were shifted to simulate either a large or a small adult male. We found that male looking responses did not differ according to the size variant condition played back. In contrast, male koalas produced longer bellows and spent more time bellowing when they were presented with playbacks simulating larger rivals. In addition, males were significantly slower to respond to this class of playback stimuli than they were to bellows simulating small males. Our results indicate that male koalas invest more effort into their vocal responses when they are presented with bellows that have lower formants indicative of larger rivals, but also show that males are slower to engage in vocal exchanges with larger males that represent more dangerous rivals. By demonstrating that male koalas use formants to assess rivals during the breeding season we have provided evidence that male-male competition constitutes an important selection pressure for broadcasting and attending to size-related formant information in this species. Further empirical studies should investigate the extent to which the use of formants during intra-sexual competition is widespread throughout mammals.     

A theoretical study on the evolution of male parental care and female multiple mating: effects of female mate choice and male care bias

Male parental care and female multiple mating are seen in many species in spite of the cost they entail. Moreover, they even coexist in some species though polyandry, by reducing paternity confidence of caregiving males, seems to hinder the evolution of paternal care. Previous studies have investigated the coevolutionary process of paternal care and polyandry under various simplifying assumptions, including random mating and random provision of male care. We extend these models to examine possible effects of female mate choice and male care bias, assuming that (a) monandrous females mate preferentially with caregiving males while polyandrous females compromise their preference in order to mate with multiple males and (b) caregiving males tend to direct their care to offspring of monandrous females. Our models suggest that both the female preference and the male bias always favor caregiving males while they may not always facilitate the evolution of monandry.     

小型田鼠:研究单配制进化与调控的模型

哺乳动物的单配制通常被认为是社会性单配制,它不是单纯地由性行为来决定,而是由诸多因素,包括长期的pair bond、夫妻双方共同抚育后代、免近亲交配以及雌雄两性相似等来决定的。在这篇综述中,我们论述了如何以啮齿类田鼠属(Microtus)为模型,通过比较研究来帮助我们理解社会性单配制的进化以及其神经调控机制。对田鼠属的研究不仅证实了单配制起源于艰苦的生存条件的假说,而且还证实了雌性性选择可能有利于维持单配制。不仅如此,哺乳动物单配制的进化还需要雄性的prosocial行为的不断强化。例如,亲近行为可以促进pairbond的形成并强化雄性对后代的哺育行为,而这种强化则来源于神经多肽催产素(OT)和加压素(AVP)与类固醇类激素的相互作用。催产素和加压素调控pairbond和双亲哺育行为的表达,而单配制和多配制田鼠的催产素和加压素受体在脑内的分布有显的不同。比较研究揭示了小型田鼠单配制的调控机制,而种内差异和行为上的可塑性则有助于我们进一步理解这种机制。比如,在某些条件下,多配制的草原田鼠(Microtus pennsylvanicu)的雄性个体具有哺育后代的行为。尽管草原田鼠的加压素Vla受体在脑内的分布与其他多配制的田鼠相似,但是如果脑室注射加压素,仍可以诱发其哺育后代的行为。同样是单配制的橙腹田鼠(Microtus ochrogaster),生活在：Illnois的显示出高水平的prosocial行为,而生活在Kansas的则表现出较低水平的社会性行为。即使两个种群的催产素或加压素Vla受体在脑内的分布相同,它们的雌激素受体表达水平显不同,这在雄性个体表现尤其明显。与Kansas的雄性个体相比,在终纹床核(bed rucleus of the stria tenninalis)和杏仁核中区(medial amygdala)这两个调控亲近行为和攻击行为的脑区,Illinois的雄性个体的α雌激素受体的水平要低得多。这些研究表明对雌激素的低敏感程度有利于高水平地表达prosocial行为并降低特定类型的攻击行为。     

Social status and cortisol levels in singing rock hyraxes

Many mammals use acoustic signals to communicate with conspecifics. Rock hyraxes (Procavia capensis) are social mammals whose vocal communication is usually restricted to quiet sounds used between nearby individuals. Loud repetitive warning trills are an exception. In our study site, a third of the adult male hyraxes also produces a rich, complex and loud vocalization we term 'singing'. In this study, we examine whether singers, which are more conspicuous by the act of singing, have higher cortisol (i.e. basal stress; C) levels than non-singers, and whether there is an association between social status and stress hormones in male hyraxes. We show that 'singing' males are different from the general adult male population in that their C levels are higher than those of silent males. Only in singers, C levels are associated with social rank, with dominants showing the highest levels. Singers are also on average older and more dominant than most other sexually mature non-singing males. Further, they copulate more than non-singers, suggesting that singing males may have higher reproductive success. Our results support the ‘stress of domination’ hypothesis and indicate that in the rock hyrax singing may reflect high competitive ability, designating singers as a distinct class of males, unique in their personal attributes and behavior.     

Male care in primates: does it ever reflect paternity?

Female mammals have internal fertilization, long gestation, and lactation. These basic facts of reproductive biology have important social consequences. Internal fertilization (accompanied by sperm competition) forces males either to face considerable uncertainty about paternity or to invest heavily in mate guarding. Long gestation increases the benefits of mate desertion for males. And because only females lactate, males have relatively less to contribute to rearing the young. Hence, it is not surprising that male mammals rarely assist their mates in caring for their young: Direct infant care by males occurs in fewer than 5 percent of all mammalian species.^1,2 In fact, many mammalian mothers attack males, even possible father of their offspring.³     

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.     

Environmental Effects on Male Reproductive Success and Parental Care in the Florida Flagfish Jordanella floridae

Models of optimal parental care predict that parental investment should depend on offspring value or the effect parental care has on offspring benefits. Few studies have examined the effect of external factors that influence offspring survival and the cost of care. In this study on the Florida flagfish (Jordanella floridae), a species with male parental care, we examined whether environmentally induced changes in care result from changes in egg requirements or in parental costs. We manipulated salinity and temperature, as these factors are known to affect the metabolic rate in both eggs and parents. We predicted that if the change in care behavior is determined by costs to the male then it should be paralleled by changes in non‐egg‐directed behavior. Conversely, if egg‐directed behavior changes independently of other behavior it would suggest that behavior is determined primarily by egg requirements. In addition we examined patterns of mating success under the assumption that if male care is affected by environmental factors then female preferences may change accordingly. Males decreased egg‐directed behavior (fanning and cleaning of eggs) at high salinity. Non‐egg‐directed behavior was unaffected by salinity. Temperature had no effects on behavior. Thus, we conclude that changes in egg demands are primarily responsible for the observed results. Successful males were bigger and more aggressive. This suggests that male dominance was an important determinant of male mating success. Unsuccessful males showed significantly more variation in number of red stripes with respect to salinity than successful males. Unsuccessful males may be less able to regulate color expression under varying environmental conditions, in which case color may be an indicator of male quality. We replicated the experiment early and late in the season. Males did not change their effort in care over the season. However, care (fanning) in the absence of eggs increased towards the end of the season. Since pre‐mating fanning was positively correlated to a male’s eventual mating success we conclude that males increased their effort to attract mates late in the season.     

A comparative study of parental care between two rodent species: implications for the mating system of the mound-building mouse Mus spicilegus

Paternal care is uncommon in mammals where males are more often involved in sexual competition than in providing care for their own offspring. However some species present some form of paternal care and, most of the time, this phenomenon is associated with a monogamous mating system. Mice of the genus Mus, such as the house mouse Mus musculus domesticus, are commonly considered to be polygamous-polygynous species. In Mus spicilegus, the mound-building mouse, previous results on female sexual preferences have suggested the existence of pair bonding more compatible with a monogamous mating system than with a polygamous one. We therefore tested the hypothesis that male M. spicilegus present a higher level of paternal care than males of the polygynous house mouse. Results showed that male M. spicilegus spent significantly more time covering the young during the first week after birth than male M. m. domesticus, particularly when the female was exploring, and retrieved stray pups significantly more frequently and more rapidly than male M. m. domesticus. There were practically no differences between the females of these two species. M. spicilegus parents also more significantly alternated their protection of the pups than M. m. domesticus parents. We discuss the evolution of paternal care in M. spicilegus in relation to monogamy.     

Low Testosterone Correlates with Delayed Development in Male Orangutans

Male orangutans (Pongo spp.) display an unusual characteristic for mammals in that some adult males advance quickly to full secondary sexual development while others can remain in an adolescent-like form for a decade or more past the age of sexual maturity. Remarkably little is understood about how and why differences in developmental timing occur. While fully-developed males are known to produce higher androgen levels than arrested males, the longer-term role of steroid hormones in male life history variation has not been examined. We examined variation in testosterone and cortisol production among 18 fully-developed (“flanged”) male orangutans in U.S. captive facilities. Our study revealed that while testosterone levels did not vary significantly according to current age, housing condition, and species origin, males that had undergone precocious development had higher testosterone levels than males that had experienced developmental arrest. While androgen variation had previously been viewed as a state-dependent characteristic of male developmental status, our study reveals that differences in the physiology of early and late developing males are detectable long past the developmental transition and may instead be trait-level characteristics associated with a male’s life history strategy. Further studies are needed to determine how early in life differences in testosterone levels emerge and what consequences this variation may have for male behavioral strategies.     

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.     

The electron microscopic analysis of synaptonemal complexes in male hybrids]

Cytogenetic studies of sterile male F1 hybrids may be helpful for the understanding of genetic bases of Haldane's Rule. The main purpose of this review is to provide several explanations for various meiotic abnormalities associated with impaired fertility. Results of cytogenetic studies of gametogenesis in vertebrates (mainly mammals) performed using electron microscopy lead to the conclusion that abnormal morphology of synaptonemal complexes is one of the main factors underlying sterility of hybrid males in mammals. Various abnormalities of synaptonemal complexes have been described in male hybrids of primates (lemur), small rodents (hybrids of laboratory mice with wild mice, as well as voles, mole-voles, hamsters, rats, and gerbils), and carnivores (silver fox, mustelids), as well as in the shrew, cattle hybrids, buffalo, and fish.     

The unexpected but understandable dynamics of mating,paternity and paternal care in the ocellated wrasse

Although theory generally predicts that males should reduce paternal care in response to cues that predict increased sperm competition and decreased paternity, empirical patterns are equivocal. Some studies have found the predicted decrease in male care with increased sperm competition, while even more studies report no effect of paternity or sperm competition on male care. Here, we report the first example, to our knowledge, of paternal care increasing with the risk and intensity of sperm competition, in the ocellated wrasse (Symphodus ocellatus). Theory also predicts that if paternal care varies and is important to female fitness, female choice among males and male indicators traits of expected paternal care should evolve. Despite a non-random distribution of mating success among nests, we found no evidence for female choice among parental males. Finally, we document the highest published levels of extra-pair paternity for a species with exclusive and obligate male care: genetic paternity analyses revealed cuckoldry at 100 per cent of nests and 28 per cent of all offspring were not sired by the male caring for them. While not predicted by any existing theory, these unexpected reproductive patterns become understandable if we consider how male and female mating and parental care interact simultaneously in this and probably many other species.     

Female preference for dominant males in the Mexican mojarra cichlid fish,Cichlasoma istlanum

It is widely assumed that female preference and male competition operate simultaneously during sexual selection. Dominance is likely an honest indicator of male quality, and females can identify and choose the dominant male to reproduce with individuals with greater competitive abilities, thus improving the quality and competitiveness of their offspring. In this context, few studies have investigated female preference in relation to male fighting ability. The Mexican mojarra, Cichlasoma istlanum, is a cichlid species native to the Balsas River basin. It is territorial during reproduction and provides parental care. Males commonly engage in territorial defence, whereas females care directly for offspring. This study examined whether females prefer dominant males that exhibit more aggressive behaviour. The authors conducted experiments using groups of two males and one female to test competitive ability in males and female preference. They also quantified the time during which the female associated with the dominant male and the subordinate male after observing the outcome of a fight between the two males. They found that Mexican mojarra females preferred dominant males and that the time females spent associating with males was positively related with their aggressive behaviours during competition. These results indicate that dominant males were more attractive than subordinate males to female Mexican mojarra. The relationship between female preference and male dominance in the Mexican mojarra demonstrates the importance of male competitive ability for future parental care in reproduction.     

The evolution of postpairing male mate choice

An increasing number of empirical studies in animals have demonstrated male mate choice. However, little is known about the evolution of postpairing male choice, specifically which occurs by differential allocation of male parental care in response to female signals. We use a population genetic model to examine whether such postpairing male mate choice can evolve when males face a trade‐off between parental care and extra‐pair copulations (EPCs). Specifically, we assume that males allocate more effort to providing parental care when mated to preferred (signaling) females, but they are then unable to allocate additional effort to seek EPCs. We find that both male preference and female signaling can evolve in this situation, under certain conditions. First, this evolution requires a relatively large difference in parental investment between males mated to preferred versus nonpreferred females. Second, whether male choice and female signaling alleles become fixed in a population versus cycle in their frequencies depends on the additional fecundity benefits from EPCs that are gained by choosy males. Third, less costly female signals enable both signaling and choice alleles to evolve under more relaxed conditions. Our results also provide a new insight into the evolution of sexual conflict over parental care.