Rosemary Knapp

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.

Endocrine Mediation of Vertebrate Male Alternative Reproductive Tactics: The Next Generation of Studies

Abstract In many species of animals, males may achieve reproductive success via one of several alternative reproductive tactics. Over the past decade or so, there has been a concerted effort to investigate endocrine mechanisms that underlie such discrete behavioral (and often morphological) variation. In vertebrates, the first generation of studies focused on potential organizational or activational effects of steroid hormones (Moore, 1991; Moore et al., 1998). Some of these studies have made it clear that, in addition to circulating hormone levels, one must also consider other aspects of the endocrine system, including hormone receptors, binding globulins and potential interactions among endocrine axes. In this paper, I review recent work on endocrine mechanisms and suggest possibilities for future investigation. I highlight how individual variation in sensitivity to environmental conditions, particularly with respect to various stressors, may account for the existence of alternative male reproductive phenotypes. Along these lines, I briefly explain the logic behind our work with male phenotypes of longear sunfish (Lepomis megalotis) that is aimed at determining the tissue-specific distribution and activity of two enzymes that are common to androgen and glucocorticoid metabolism. A major goal of our work is to examine the potential role of steroidogenic enzymes in the transduction of environmental information to influence the expression of alternative male reproductive phenotypes.

Hormonal Responses to Aggression Vary in Different Types of Agonistic Encounters in Male Tree Lizards, Urosaurus ornatus

Hormonal responses to male-male interactions have been detected in some studies of vertebrates but not others. One hypothesis that may partially explain these discrepancies is that differences in the duration of male-male interactions cause different hormonal responses. In social systems based on dominance-subordinance hierarchies interactions often last longer than if exclusive territories are maintained. Tests of the hypothesis that encounter duration explains discrepancies in hormonal responses would be facilitated by a species that shows elements of both types of social systems, such as species in which males practice alternative reproductive tactics. We compared plasma levels of corticosterone and testosterone in males of the territorial morph of the tree lizard (Urosaurus ornatus) subjected either to short (15 min) male-male encounters or to long (7 days) dominance interactions. In the long interactions, dominant males had lower levels of corticosterone than did subordinate males over the first day, but this difference subsequently disappeared. In sharp contrast, winners of short-term encounters had elevated plasma corticosterone levels which peaked the day after the encounter. Thus, males isolated after a short encounter experienced an increase in corticosterone that was apparently inhibited in males who continued interacting with other males. The delayed increase in corticosterone after a short encounter may facilitate metabolic recovery from the encounter, mobilize metabolic substrates useful in subsequent encounters, or may alter subsequent behavior. The response does not appear to be simply recovery from exercise because in a second experiment males exercised for 15 min did not show a similar delayed increase in corticosterone the following day. Testosterone levels were also monitored and did not change in any of these treatments. These results demonstrate that the duration and the outcome of male-male interactions may each independently influence hormone levels.

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 males 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.

Stress Hormone Is Implicated in Satellite‐Caller Associations and Sexual Selection in the Great Plains Toad

The effects of androgens on male‐typical traits suggest that variation among males in circulating levels can play a major role in sexual selection. We examined whether variation in vocal attractiveness is attributable to differences in androgen levels among Great Plains toads (Bufo cognatus). We found that noncalling “satellite” males practicing an alternative mating tactic were more likely to associate with males producing long calls. However, callers with satellites did not have higher androgen levels than callers without satellites. Rather, callers with satellites had significantly lower corticosterone (CORT) levels than callers without satellites. A CORT manipulation experiment suggested that differences in calls for males with and without satellites were related to differences in CORT levels. Furthermore, there was a negative correlation between CORT level and call duration within most nights of chorus activity. However, the correlation was weak for the pooled data (across all nights), suggesting that local environmental and/or social factors also affect call duration. Last, we show that females preferred broadcast calls of longer duration, characteristic of males with satellites and low CORT. These results imply that satellites optimize their reproductive success by associating with males producing long calls. However, this association should negatively affect the fitness of attractive callers.

Steroid hormones in bluegill, a species with male alternative reproductive tactics including female mimicry

The proximate mechanisms underlying the evolution and maintenance of within-sex variation in mating behaviour are still poorly understood. Species characterized by alternative reproductive tactics provide ideal opportunities to investigate such mechanisms. Bluegill (Lepomis macrochirus) are noteworthy in this regard because they exhibit two distinct cuckolder (parasitic) morphs (called sneaker and satellite) in addition to the parental males that court females. Here we confirm previous findings that spawning cuckolder and parental males have significantly different levels of testosterone and 11-ketotestosterone. We also report, for the first time, that oestradiol and cortisol levels are higher in cuckolders than in parental males. The two cuckolder morphs did not differ in average levels of any of the four hormones. However, among satellite males which mimic females in appearance and behaviour, there was a strong negative relationship between oestradiol levels and body length, a surrogate for age. This finding suggests that for satellite males, oestradiol dependency of mating behaviour decreases with increasing mating experience. Although such decreased hormone dependence of mating behaviour has been reported in other taxa, our data represent the first suggestion of the relationship in fishes.

Relationships among steroid hormone levels, vocal effort and body condition in an explosive-breeding toad

Mutually reinforcing hormone–behaviour relationships may drive temporal changes in steroid hormone levels and vocal effort in anuran amphibians. Recent models propose that chorus activity stimulates the production of androgens in signallers and receivers, thereby mediating an increase in vocal effort. The energetic demands associated with high vocal effort should, in turn, elevate circulating corticosterone levels to promote the mobilization of energy reserves. High threshold corticosterone levels, however, are expected to negatively affect androgen levels and, hence, vocal effort. Steroid hormone levels and vocal effort are thus expected to be low at the onset of chorus activity, increase over sequential nights of calling until peak levels are reached, and subsequently decline; energy reserves should show inverse temporal trends. To test these predictions, we examined temporal changes in androgen (dihydrotestosterone and testosterone) levels, corticosterone levels, vocal effort and body condition in Woodhouses toads, Bufo woodhousii . Contrary to model predictions, androgen levels, vocal effort and body condition remained relatively unchanged and circulating corticosterone levels tended to decrease within and across nights of chorus activity. Furthermore, although vocal effort was not correlated with circulating androgen levels, it was positively correlated with circulating corticosterone levels, supporting the prediction that high vocal effort promotes the production of corticosterone. Yet despite this correlation, poor body condition was not associated with high corticosterone levels, suggesting that factors other than energetic state influence corticosterone levels in B. woodhousii . We discuss alternative hypotheses regarding relationships among the measured parameters in this explosive-breeding species.

The stress of elaborate male traits: integrating glucocorticoids with androgen-based models of sexual selection

Stress hormones are emerging as major factors regulating the expression of elaborate male traits. Surprisingly, however, the effects of glucocorticoids on such traits have not been formally integrated with androgen-based models of sexual selection. Here we point out that consideration of glucocorticoid-mediated effects on the phenotype provides new insight into long-standing hypotheses and controversies associated with such models. In particular, androgen-based ‘handicap’ models of sexual selection characteristically hinge on graded effects of androgens on male traits, but few studies have found support for such a relationship, suggesting that androgens may not be a primary target of selection. We propose, however, that in many instances, androgens may not appear to have a graded effect on the phenotype because elevated glucocorticoids mask the effects of androgens. Glucocorticoids may be inextricably linked to elaborate traits because the energetic demands associated with such traits promote glucocorticoid production. We thus propose that glucocorticoid-mediated effects on male traits warrant re-evaluation of androgen-based models of sexual selection. In particular, we argue that androgen-based handicap models cannot be dismissed based on the lack of evidence for a graded relationship between androgen level and the extent or magnitude of the trait. Our review of the literature indicates that most studies have examined either the effects of androgens or the effects of glucocorticoids, but not both. A more integrated approach involving the effects of both steroids is necessary to fully understand the role of androgens and the endocrine targets of selection associated with the expression of elaborate male traits.

Paternity, parental behavior and circulating steroid hormone concentrations in nest-tending male bluegill.

Like many teleost fishes, bluegill (Lepomis macrochirus) are characterized by sole male parental care of offspring. In addition, bluegill parental males experience cuckoldry by specialized parasitic male morphs. This cuckoldry has previously been shown to influence the expression of parental care behavior. To better understand some of the proximate mechanisms mediating parental behavior, we examined the relationships between circulating steroid hormones, paternity, and parental behavior during the egg and fry stages of care in parentals that spawned during the first third of the breeding season. During the egg stage of care, we found that males with higher paternity had lower levels of testosterone, but there was no relationship between paternity and either 11-ketotestosterone or cortisol. There also was no relationship between the hormones and care behavior comprising fanning of the eggs, nest rim circles, chases of brood predators, or pecking at the eggs (indicative of egg cannibalism), except for a negative relationship between cortisol and pecking behavior. During the fry stage of care, we conversely found that males with higher paternity had higher levels of testosterone and 11-ketotestosterone. There also was a negative relationship between the concentrations of these two androgens and the defensive behavior of males when exposed to a potential brood predator (a pumpkinseed, Lepomis gibbosus). We discuss these results in relation to previous work in fishes and other vertebrate taxa. Overall, our data suggest a complex relationship between circulating steroid hormone levels, paternity and parental behavior.

Early development of the motor and premotor circuitry of a sexually dimorphic vocal pathway in a teleost fish

The plainfin midshipman fish (Porichthys notatus) has a caudal hindbrain vocal motor circuit that has been proposed to share a common embryonic origin with the hindbrain vocal networks of other vertebrates. In midshipman, this vocal circuit includes three groups of neurons: sonic motor, pacemaker, and ventral medullary. Here, transneuronal transport of biocytin or neurobiotin was used to delineate the early ontogeny of the three hindbrain vocal nuclei and their pattern of connectivity. The organization of the vocal nuclei was studied in animals beginning soon after hatching until the nuclei have the adult phenotype at the time fish become free-swimming. There is a clear sequence of events whereby motoneurons establish their connections with the sonic muscle prior to establishing connections with premotor neurons; developmental milestones of the vocal pathway parallel those of the sonic muscle. The results also indicate that sexual differentiation of the vocal motor system in midshipman begins early in development, well before any evidence of sexual maturation. Embryonic males and females differ in the relationship between soma size and body length for the three hindbrain nuclei. Males are also more variable than females in body mass, volume of the sonic motor nucleus, and motoneuron cell size.