Experimentally-elevated testosterone, female parental care, and reproductive success in a songbird, the Dark-eyed Junco (Junco hyemalis)

In male dark-eyed juncos (Junco hyemalis), experimentally elevated testosterone (T) decreases male parental care and offspring survival, but results in higher overall fitness through greater mating success. To help address the ensuing question of what prevents selection from favoring higher levels of T in male juncos, we manipulated T in female juncos. A previous study demonstrated no effect of experimentally elevated T on female incubation behavior, suggesting that female parental behavior might be insensitive to T. In this study we asked whether experimentally elevated T mediates other female parental behaviors and whether variation in T-mediated parental behavior might influence reproductive success. We videotaped free-living control- and T-females during nesting to quantify brooding behavior when young were 3 days old and provisioning behavior when young were 6 days old. Nest defense was measured by quantifying responses to a mounted predator placed near the nest. Reproductive success was assessed via fecundity, nestling quality, and nest survival. T-females spent less time than control females brooding but did not differ in provisioning rate. T-females performed fewer dives at the predator mount and, unlike controls, failed to increase defense as nesting progressed. T-females also had lower daily nest survival and lower nest success (odds of producing at least one fledgling). We conclude that some aspects of female parental behavior are sensitive to experimentally elevated T while others are not and consider the implications for the evolution of T-mediated characters in both sexes.     

Adult male replacement and subsequent infant care by male and siblings in socially monogamous owl monkeys (<Emphasis Type="Italic">Aotus azarai</Emphasis>)

Owl monkeys (Aotus azarai) are small, territorial, socially monogamous primates that show intense infant care by the adult male in the group. It has been hypothesized that male care may be adaptive because it increases offspring survival and/or reduces the metabolic costs to the female of raising the offspring. Alternatively, males may provide care even when they are not related to the infants to increase future reproductive opportunities. We describe changes in infant care patterns that took place after the eviction of the resident male by a solitary male in an owl monkey population in the Argentinean Chaco. The resident male and mother provided all infant care during the first month of life of the infant, until the male was evicted. During the three-day male replacement event, care of the infant was shared among the mother, a four-year-old sister, and a one-year-old brother. The new male began contributing to infant care soon after entering the group, carrying, and interacting socially with the infant in much the same way as any male regularly does. However, despite receiving biparental care from both the original and new resident males, the infant disappeared at the age of four months and was presumed dead. These are the first reports of care by sibling and by non-putative fathers in wild owl monkeys. Given the significant amount of time that new pairs of owl monkeys spend before reproducing, it is possible that male care in owl monkeys functions as mating effort as much as or more than parenting effort.     

Proteomics profiling of epidermal mucus secretion of a cichlid (Symphysodon aequifasciata) demonstrating parental care behavior

The discus fish (Symphysodon aequifasciata) is a cichlid demonstrating advanced mode of parental care towards fry. Both male and female fish utilized epidermal mucus secreted from specialized epidermal cells to feed developing fry. We utilized proteomics to compare protein profile from parental and nonparental fish. Gel analysis revealed a total of 35 spots that were up-regulated in parental mucus. In tandem, another 18 spots were uniquely expressed in parental mucus. MS analysis of these spots identified proteins such as fructose biphosphate aldolase, nucleoside diphosphate kinase, and heat shock proteins, which are essential to support energy provision, cell repair and proliferation, stress mediation, and defense mechanism in parental fish during parental-care period. Concurrently, the detection of several antioxidant-related proteins such as thioredoxin peroxidase and hemopexin suggests a need to overcome oxidative stress during hypermucosal production in parental-care behavior. A C-type lectin was also found to be uniquely expressed in parental mucus and could have important role in providing antimicrobial defense to both parental fish and fry. In summary, our study shows that discus mucus proteome undergoes changes in protein expression during parental-care period.     

Castration reduces male testosterone, estradiol, and territorial aggression, but not paternal behavior in biparental dwarf hamsters (Phodopus campbelli)

Biparental male hamsters, Phodopus campbelli, act as midwives during the birth of their litter and are highly responsive to an experimentally displaced pup. They also have high peripheral concentrations of estradiol, a hormone with known roles in maternal behavior. Surgical castration during the gestation of their first litter was used to investigate the source of that estradiol and the functional role of testicular sex steroids in paternal responsiveness. In Experiment I, castration reduced both testosterone and estradiol concentrations, confirming that the testes were the primary source of estradiol. However, neither paternal responsiveness nor multiple measures of reproductive success were altered by the castration. Aggression directed towards an intruder, however, was reduced by castration. In Experiment II, removal of prior experience with birth or pups also failed to alter paternal responsiveness in castrated males. Although the present results do not preclude a role for local estradiol synthesis in the brain, results do not support an association between high circulating estradiol in males and their paternal behavior.     

Evolution of parental care in dart poison frogs (Amphibia: Anura: Dendrobatidae)

Dendrobatid frogs perform a unique mode of parental care, ranging from egg attendance and tadpole transport to tadpole feeding. It is hypothesized that a behaviour in which the egg attending parent remains with the cluch is the most primitive condition. In more advanced forms or parental care, the male is able to attend several clutches of eggs. Tadpole attendance and feeding, finally, started as deceit; the male induced the female to lay eggs into a bromeliad leaf axil already occupied by a larva. Costs and benefits of the different modes of parental care and possible alternative reproductive tactics are discussed.     

Individual variation in testosterone and parental care in a female songbird; The dark-eyed junco (Junco hyemalis)

When competition for sex-specific resources overlaps in time with offspring production and care, trade-offs can occur. Steroid hormones, particularly testosterone (T), play a crucial role in mediating such trade-offs in males, often increasing competitive behaviors while decreasing paternal behavior. Recent research has shown that females also face such trade-offs; however, we know little about the role of T in mediating female phenotypes in general, and the role of T in mediating trade-offs in females in particular. Here we examine the relationship between individual variation in maternal effort and endogenous T in the dark-eyed junco, a common songbird. Specifically, we measure circulating T before and after a physiological challenge (injection of gonadotropin releasing hormone, GnRH), and determine whether either measure is related to provisioning, brooding, or the amount of T sequestered in egg yolk. We found that females producing more T in response to a challenge spent less time brooding nestlings, but provisioned nestlings more frequently, and deposited more T in their eggs. These findings suggest that, while T is likely important in mediating maternal phenotypes and female life history tradeoffs, the direction of the relationships between T and phenotype may differ from what is generally observed in males, and that high levels of endogenous T are not necessarily as costly as previous work might suggest.     

Chronic variable stress in fathers alters paternal and social behavior but not pup development in the biparental California mouse (Peromyscus californicus)

Stress and chronically elevated glucocorticoid levels have been shown to disrupt parental behavior in mothers; however, almost no studies have investigated corresponding effects in fathers. The present experiment tested the hypothesis that chronic variable stress inhibits paternal behavior and consequently alters pup development in the monogamous, biparental California mouse (Peromyscus californicus). First-time fathers were assigned to one of three experimental groups: chronic variable stress (CVS, n = 8), separation control (SC, n = 7), or unmanipulated control (UC, n = 8). The CVS paradigm (3 stressors per day for 7 days) successfully stressed mice, as evidenced by increased baseline plasma corticosterone concentrations, increased adrenal mass, decreased thymus mass, and a decrease in body mass over time. CVS altered paternal and social behavior of fathers, but major differences were observed only on day 6 of the 7-day paradigm. At that time point, CVS fathers spent less time with their pairmate and pups, and more time autogrooming, as compared to UC fathers; SC fathers spent more time behaving paternally and grooming the female mate than CVS and UC fathers. Thus, CVS blocked the separation-induced increase in social behaviors observed in the SC fathers. Nonetheless, chronic stress in fathers did not appear to alter survival or development of their offspring: pups from the three experimental conditions did not differ in body mass gain over time, in the day of eye opening, or in basal or post-stress corticosterone levels. These results demonstrate that chronic stress can transiently disrupt paternal and social behavior in P. californicus fathers, but does not alter pup development or survival under controlled, non-challenging laboratory conditions.     

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.     

Plasma levels of androgens and cortisol in relation to breeding behavior in parental male bluegill sunfish, Lepomis macrochirus

Like many teleosts, male bluegill sunfish (Lepomis macrochirus) provide sole parental care. To understand some of the proximate costs of parental care, we measured body condition and plasma levels of testosterone (T), 11-ketotestosterone (11KT) and cortisol in nesting bluegill males during pre-spawning, spawning and parental care stages. T and 11KT were at their highest mean levels during the pre-spawning period and decreased to lower levels early during the parental care period before rising again when the eggs hatched. Cortisol levels fluctuated across the breeding stages, but there was a noticeable increase from low levels on the day of spawning during the first 2 days of parental care when egg fanning is most intense. Levels of all hormones varied considerably among males, with androgen levels often correlating positively with a male's body condition. We also demonstrate, using a brood reduction experiment and repeated sampling of known individuals, that the presence of eggs affects hormone levels shortly after eggs hatch. Parental males in better body condition had higher levels of androgens during parental care. Males that were known to renest later in the season also had higher androgen levels and were in better body condition during the first nesting bout than males only known to have nested once. However, circulating levels of cortisol did not differ significantly between these groups. We discuss our findings in the context of proximate and ultimate costs of parental care and propose several reasons why elevated androgen levels may not be as incompatible with the expression of paternal care in male teleosts, as compared with avian and mammalian fathers.     

Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird

In many species, male territorial aggression is tightly coupled with gonadal secretion of testosterone (T). In contrast, in song sparrows (Melospiza melodia morphna), males are highly aggressive during the breeding (spring) and nonbreeding (autumn and early winter) seasons, but not during molt (late summer). In aggressive nonbreeding song sparrows, plasma T levels are basal (< or = 0.10 ng/ml), and castration has no effect on aggression. However, aromatase inhibitors reduce nonbreeding aggression, indicating a role for estrogen in wintering males. In the nonbreeding season, the substrate for brain aromatase is unclear, because plasma T and androstenedione levels are basal. Aromatizable androgen may be derived from plasma dehydroepiandrosterone (DHEA), an androgen precursor. DHEA circulates at elevated levels in wintering males (approximately 0.8 ng/ml) and might be locally converted to T in the brain. Moreover, plasma DHEA is reduced during molt, as is aggression. Here, we experimentally increased DHEA in wild nonbreeding male song sparrows and examined territorial behaviors (e.g., singing) and discrete neural regions controlling the production of song. A physiological dose of DHEA for 15 days increased singing in response to simulated territorial intrusions. In addition, DHEA treatment increased the volume of a telencephalic brain region (the HVc) controlling song, indicating that DHEA can have large-scale neuroanatomical effects in adult animals. The DHEA treatment also caused a slight increase in plasma T. Exogenous DHEA may have been metabolized to sex steroids within the brain to exert these behavioral and neural effects, and it is also possible that peripheral metabolism contributed to these effects. These are the first results to suggest that exogenous DHEA increases male-male aggression and the size of an entire brain region in adults. The data are consistent with the hypothesis that DHEA regulates territorial behavior, especially in the nonbreeding season, when plasma T is basal.     

Causes and consequences of voluntary anorexia during the parental care period of wild male smallmouth bass (Micropterus dolomieu)

By definition, parental care behaviors increase offspring survival, and individual fitness, at some cost to the parent. In smallmouth bass (Micropterus dolomieu), parental males provide sole care for the developing brood that includes an increase in activity during brood defense and decreased foraging resulting in a decline in endogenous energy reserves. No mechanisms have been proposed for cessation of voluntary foraging, though regulation of appetite hormones such as ghrelin have been documented to affect feeding behavior in other fishes. We documented baseline fluctuations in plasma ghrelin concentrations across parental care. Plasma ghrelin concentrations were lowest during the early stages of parental care before increasing as the brood developed to independence. Additionally, we performed an intervention experiment whereby plasma ghrelin levels were artificially increased through an injection of rodent ghrelin at the onset of parental care. Despite measuring a significant increase in plasma ghrelin approximately 1 week after injection, we noted no differences in plasma-borne indicators of recent foraging activity indicating that voluntary anorexia is possibly reinforced by receptor insensitivity to appetite hormones. Finally, we assessed the ultimate consequences of foraging during parental care by feeding fish to satiation and measuring post-prandial changes in swimming performance and aggression. Fish fed to satiation showed significant decreases in burst swimming ability and aggressiveness towards potential brood predators. Voluntary anorexia during smallmouth bass parental care is an adaptive behavior that avoids potentially deleterious declines in swimming performance and aggression apparently through a modulation of production and reception of appetite hormones including ghrelin.     

The lack of influence of exogenous testosterone on male parental behavior in a neotropical frog (Eleutherodactylus): a field experiment

Males of the Puerto Rican frog Eleutherodactylus coqui exhibit prolonged parental care (nest attendance and defense) of direct-developing eggs in nonaquatic nest sites. Earlier work showed that plasma androgen levels are significantly lower in males caring for eggs than in noncaring, calling males. In this study, we investigated the effects of elevated plasma androgens on parental care behavior by implanting either testosterone (T) or placebo (P) pellets in parental males brooding eggs in the field. Plasma androgen levels, assessed 4 days after pellet implantation, were six times higher in T males than in P males. Despite this increase, T males exhibited no changes in nest fidelity or brooding behavior. The results indicate that lower androgen levels, at least those corresponding to a decline in T during parental care, are not necessary to maintain parental behavior in this tropical frog.     

Parental care behavior in the monogamous,sexually dimorphic Madagascar paradise flycatcher: sex differences and the effect of brood size

I studied the parental care behavior of the Madagascar paradise flycatcher Terpsiphone mutata in northwestern Madagascar. I especially focused on feeding, brooding and vigilance behaviors. Feeding rate did not differ between males and females, but females spent more time at the nest than males. Females dedicated their time to brooding, while males perched on the nest and were vigilant. Both parents changed the feeding rate in relation to brood size, so the feeding rate per nestling was not different among nests of different brood size. Duration of brooding by females increased with decreasing brood size, suggesting that the Royama effect, the pattern of lower feeding rate per nestling in larger broods, did not apply in this study. Males spent more time on vigilance than females. Anti-predator vigilance by males should be important for nestling survival given the high predation pressure typical of this population. In conclusion, males provide considerable parental care probably to minimize nestling starvation and to avoid nest predation. My results are not consistent with the general pattern of less parental effort by males in monogamous, sexually dimorphic species.     

Comparative analysis of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation

Male androgen responses to social challenges have been predicted to vary with mating system, male-male aggressiveness, and the degree of paternal investment in birds ("challenge hypothesis," Am. Nat. 136 (1990), 829). This study focused on the interspecific predictions of the challenge hypothesis. Comparative methods were used to control for effects of the phylogenetic relatedness among the sampled species. Male androgen data of 84 bird species were collected from literature records on seasonal androgen patterns. From these, the androgen responsiveness (AR) was calculated as described in the original challenge hypothesis (i.e., maximum physiological level/breeding baseline). Scatterplots of AR versus mating strategy, male-male aggressiveness, and the degree of paternal care confirmed the expected interspecific patterns. When phylogenetic analyses were performed among all of the sampled species, the effects of paternal investment disappeared while the AR remained covarying to a high degree with mating system and male-male aggressiveness. Although these mechanisms may be different at the intraspecific level, this suggests that interspecific differences of AR in male birds may have evolved in response to changes of mating strategies, rather than in response to altered paternal duties. However, control for phylogeny among the subsample of 32 passerine species revealed that if any paternal investment contributed to the observed variance in AR, then the change from "no male incubation" to "male shares incubation duties" represented the most effective, whereas the male's contribution to feeding offspring did not explain the observed variation of AR.     

川金丝猴非母亲照料行为的影响因素及其母亲获益——以神农架川金丝猴投食群为例

灵长类社会中存在着非母亲成员(成年雌猴、青少年猴和成年雄猴)对婴儿的照料行为,即非母亲照料行为,该行为直接影响新生婴儿的存活与发育以及婴儿母亲的日常活动,是灵长类学研究领域的热点问题.本研究于2019年3月至2019年11月,采用焦点动物取样和瞬时扫描取样,探究了川金丝猴非母亲照料行为的影响因素及其对母亲活动分配的影响...     

Exogenous corticosterone and nest abandonment: A study in a long-lived bird, the Adélie penguin

Breeding individuals enter an emergency life-history stage when their body reserves reach a minimum threshold. Consequently, they redirect current activity toward survival, leading to egg abandonment in birds. Corticosterone (CORT) is known to promote this stage. How and to what extent CORT triggers egg abandonment when breeding is associated with prolonged fasting, however, requires further investigation.We manipulated free-living male Adélie penguins with CORT-pellets before their laying period. We then examined their behavioral response with respect to nest abandonment in parallel with their prolactin levels (regulating parental care), and the subsequent effects of treatment on breeding success in relieved birds.Exogenous CORT triggered nest abandonment in 60% of the treated penguins ~ 14 days after treatment and induced a concomitant decline in prolactin levels. Interestingly, prolactin levels in treated penguins that did not abandon their nest were higher at the point of implantation and also after being relieved by females, when compared with abandoning penguins. Among successful birds, the treatment did not affect the number of chicks, nor the brood mass.Our results show the involvement of CORT in the decision-making process regarding egg abandonment in Adélie penguins when incubation is associated with a natural long fast. However, we suggest that CORT alone is not sufficient to trigger nest abandonment but that 1) prolactin levels need to reach a low threshold value, and 2) a rise in proteolysis (i.e. utilization of protein as main energy substrate) seems also to be required.     

Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse (Peromyscus californicus)

In the laboratory rat and mouse, neonatal handling enhances hippocampal-dependent learning in adulthood, an effect mediated by changes in maternal behavior toward the handled young. In the present study, we examined the interaction between neonatal handling and biparental care during the early postnatal period and its effect on cognitive function in adult California mice (Peromyscus californicus). We characterized the parental behavior of handled and nonhandled father-present and father-absent families over the first 15 days of life. We then assessed cognitive performance of male and female offspring in the Barnes maze and object recognition test after they were 60 days of age. We found that the amount of licking and grooming received by pups was decreased in father-absent families. By postnatal days 12-15, licking and grooming in handled, father-absent families were equivalent to that of nonhandled, father-present families. Handling enhanced novel object recognition in father-present male mice with no effect in females. In the nonhandled group, the presence of the father had no effect on object recognition learning in male or female mice. Handling also enhanced spatial learning in the Barnes maze. In nonhandled families, the presence of the father appeared to have no effect on spatial learning in the male offspring. Interestingly, spatial learning in nonhandled, father-absent, female offspring was similar to that of handled animals. The average amount of licking and grooming received by pups was negatively correlated with the average number of errors made on the first day of reversal training in the Barnes maze. These data support previous findings that neonatal handling facilitates learning and memory in adulthood, suggest that under certain environmental conditions, there is a sex difference in the response of pups to paternal care, and further demonstrate the importance of active parental investment for offspring cognitive development.     

Allopaternal care in the tessellated darter,Etheostoma olmstedi (Pisces: Percidae)

Synopsis Large male tessellated darters, Etheostoma olmstedi, defend flat-bottomed rocks, the undersides of which serve as spawning substrates. Because females attach eggs directly onto bare stone, a spawning bout necessarily decreases the surface area available for further breeding at a nest. In apparent response to the female preference of ovipositing on rocks with the most bare surface, fathers abandon nests with their attached offspring to search for rocks with more uncovered surface. Egg abandonment also results after roving fathers intercept and spawn with ripe females and remain at a different rock to care for a new clutch. In essence, large males appear to maximize the number of eggs they fertilize by sequentially monopolizing breeding patches that are temporarily most desirable to females. The costs to a father of abandoning his eggs appear to be low for two reasons: (1) non-territorial males, created by a scarcity of suitable rocks, readily occupy vacant nests, and clean and aerate the abandoned eggs; and (2) after water hardening, eggs are less vulnerable to cannibalism. The maintenance of eggs by nonparental males may be both incidental to scrubbing the ceiling for their own breeding and adaptive in that viable eggs stimulate females to spawn; neither would appear to involve parental investment costs. Thus, allopaternal care in the tessellated darter may have evolved because it is performed in the selfish pursuit of spawning opportunities while entailing little, if any, of the costs normally subsumed within parental investment.     

Mothers, not fathers, determine the delayed onset of male carrying in Goeldi's monkey (Callimico goeldii)

In biparental species, females are thought to accept and even to seek male assistance in rearing of the young. In this study, we present data that suggests that Goeldi's monkey females (Callimico goeldii) actually reject male parental care for a certain period. In Callimico, which have biparental care, mothers carry the infant exclusively for the first three weeks despite the fact that fathers are interested in their infants directly after birth. Fathers initiated significantly more body contact with their mates when newborn infants were present and retrieved one-day-old infants that were experimentally presented to them. The onset of paternal carrying in our colony was 27.5 days compared to 11.5 days (medians) observed in the field. However, presentation of a live potential predator induced earlier onset of paternal carrying by about 10 days. Additional costs to maternal carrying such as foraging and predator avoidance are likely factors influencing the decision of the mother as to when to share the cost of infant carrying with the father. We conclude that Goeldi's monkey fathers start carrying their infants so late because they do not get them earlier from the mother. We suggest that one ultimate explanation for that delay might be increased infant mortality when infant transfer starts at an earlier stage.