Fluctuating asymmetries and reproductive success in the peacock blenny

In an investigation of the relationship between reproductive success and fluctuating asymmetry (FA) in the peacock blenny Salaria pavo , FA was measured in four bilaterally paired characters in successful and unsuccessful males during the breeding season. Reproductive success among successful males was assessed by calculating the number of eggs the males were defending. Absolute FA values relative to trait size were high for all characters and it is suggested that this could be a consequence of sub-optimal environmental conditions. Two of the traits presented higher absolute FA values suggesting a lower canalization during ontogeny. No difference in FA between successful and unsuccessful males was found and no relationship between FA and number of eggs among the successful males occurred for any of the measured traits. A composite index of FA, that should better reflect overall developmental competence, was also unrelated to reproductive success. These results indicate that FA is not associated with reproductive success among males of S. pavo . Successful males were larger than unsuccessful males and a strong positive correlation was detected between the body length of the parental males and the number of eggs they had in the nest, even when controlling for the internal nest area. Body size may give males a reproductive advantage by being preferred by females and by having an advantage in male-male competition for nests of higher quality.     

The role of male visual and chemical cues on the activation of female courtship behaviour in the sex-role reversed peacock blenny

Chemical cues during courtship in peacock blenny Salaria pavo did not add significantly to the response of visual stimuli and females did not court when a male was not visible. The results showed that female S. pavo courtship behaviour was elicited exclusively by male visual features and not by a multicomponent signal in different sensory modalities. The time spent by females courting the male and exhibiting the nuptial colouration during visual trials correlated with the size of the male's crest, suggesting a signalling function for this trait. Alternative hypothesis for the function of the putative pheromones released by the male's anal gland are discussed. Evidence that female sexual motivation decreases towards the end of the breeding season is also provided, which should be considered in future mate choice experiments.     

Sex differences in resource utilization by the peacock blenny

This paper presents data on the seasonal variation of gonadosomatic, hepatosomatic and feeding indices in nesting males, females and female-like males of the blenniid fish Salaria pavo . Eviscerated condition factors, female fecundity and feeding rates are also presented. The results are consistent with the hypothesis that females maximize their feeding rates during reproduction, converting food into eggs through repeated spawning. Nesting males feed at a very low rate during the breeding season. It is argued that one major component of the reproductive costs in these males is the reduction of feeding opportunities. Female-like males present lower reproductive costs, which probably reflects the compromise between fertilizing some eggs and growing.     

Endocrine control of sexual behavior in sneaker males of the peacock blenny Salaria pavo: effects of castration, aromatase inhibition, testosterone and estradiol

The effects of castration and sex steroid manipulations on the expression of sexual behavior were investigated in a small fish, the peacock blenny, Salaria pavo. In this species, large males defend nests and attract females while small "sneaker" males reproduce by imitating the female morphology and courtship behavior in order to approach nests during spawning events and parasitically fertilize eggs. Sneakers switch into nest holders in their second breeding season, thus displaying both male and female-like sexual behavior during their lifetime. We tested the effects of castration and of an aromatase inhibitor (Fadrozole, F), testosterone (T) or 17beta-estradiol (E(2)) implants on the expression of male and female-like behavior in sneakers. Sneakers were either sham-operated, castrated or castrated and implanted with vehicle, F, T+F or E(2)+F. Seven days after the treatment, sneakers were placed in a tank with a nesting male, two ripe females and an available nest. Castrated fish had lower levels of circulating T and increased the time spent displaying female typical nuptial coloration. T implants had the opposite effect, inhibiting the expression of female-like behavior and coloration. E(2) implants had no significant effect on the display of sexual behavior but the frequency of aggressive displays decreased. The results agree with previous findings in sneakers of S. pavo that demonstrated an inhibition of female-like behavior by 11-ketotestosterone (11-KT). The reported increase in T and 11-KT production when sneakers change into nest holders may thus contribute to behaviorally defeminize sneakers. Contrarily, both T and E(2) failed to promote male-like behavior, suggesting that behavioral masculization during tactic switching depends on other neuroendocrine mechanisms or that the time length of the experiment was insufficient to induce male-like behavioral changes in sneakers.     

Brain and gonadal aromatase activity and steroid hormone levels in female and polymorphic males of the peacock blenny Salaria pavo

In the peacock blenny Salaria pavo large males with well-developed secondary sexual characters establish nests and attract females while small “sneaker” males mimic female sexual displays in order to approach the nests of larger males and parasitically fertilize eggs. These alternative reproductive tactics are sequential, as sneakers irreversibly switch into nesting males. This transition involves major morphologic and behavioral changes and is likely to be mediated by hormones. This study focuses on the role of aromatase, an enzyme that catalyses the conversion of androgens into estrogens, in the regulation of male sexual polymorphism in S. pavo. For this, sex steroid plasma levels and aromatase activity (AA) in gonads, whole brain and brain macroareas were determined in sneakers, transitional males (i.e. sneakers undergoing the transition into nesting males), nesting males and females collected in the field. AA was much higher in ovarian tissue than in testicular tissue and accordingly circulating estradiol levels were highest in females. This supports the view that elevated AA and estradiol levels are associated with the development of a functional ovary. Transitional males are in a non-reproductive phase and had underdeveloped testes when compared with sneakers and nesting males. Testicular AA was approximately 10 times higher in transitional males when compared with sneakers and nesting males, suggesting high AA has a suppressive effect on testicular development. Nesting males had significantly higher plasma levels of both testosterone (T) and 11-ketotestosterone when compared with the other male morphs and previous studies demonstrated that these androgens suppress female-like displays in sneakers. In the brain, AA was highest in macroareas presumably containing hypothalamic nuclei traditionally associated with the regulation of reproductive behaviors. Overall, females presented the highest levels of brain AA. In male morphs AA increased from sneakers, to transitional males, to nesting males in all brain macroareas. These results suggest that the transition into the nesting male tactic is accompanied both by an increase in testicular androgen production and by a higher conversion of androgens into estrogens in the brain. The increase in androgen production is likely to mediate the development of male secondary sexual characters while the increase in brain AA may be related to the behavioral changes associated with tactic transition.     

Intersexual copying by sneaker males of the peacock blenny

In general, animals prefer to mate with individuals they have observed being courted or in close association with sexual partners. This phenomenon of mate copying has been demonstrated in several species, but so far no study has provided substantial evidence that it is adaptive. Furthermore, mate copying has been viewed only in the context of females copying other females or males copying other males. In the peacock blenny, Salaria pavo, parasitic males (sneakers) may gain an advantage by copying the association patterns of females with bourgeois males (large males that defend nests). We tested the sneaker's preference for one of two males and subsequently presented the nonpreferred male to the sneaker in the company of females, while the preferred male was presented alone. If the association of females with bourgeois males influences the sneaker's preference, we predicted the sneaker would spend more time close to the nonpreferred male, when females were no longer present. We found that (1) sneakers preferred to associate with the larger of the two males and (2) when the previously nonpreferred male was presented in the company of females the sneakers tended to approach that male sooner, although not significantly so, and to spend more time close to it. Thus, parasitic males seem to choose host males both by independent mechanisms (larger males were preferred) and by nonindependent mechanisms (males observed with females were preferred). We discuss the adaptive value of sneakers choosing males by each of these mechanisms. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Brain aromatase mRNA expression in two populations of the peacock blenny Salaria pavo with divergent mating systems

Aromatase, the key enzyme in the conversion of androgens to estrogens, regulates the availability of these hormones in tissues and controls many physiological and behavioral processes. In fish and other vertebrates, the regulation of aromatase expression in the brain has been implicated in the modulation of male sexual and aggressive behaviors. Here, the pattern of mRNA expression of the brain aromatase isoform (encoded by the CYP19A2 gene also referred as CYP19b) was quantified at the peak of spawning season in brain macroareas from males and females of the blenny Salaria pavo originated from two populations displaying male alternative reproductive tactics but differing in their mating systems. In Trieste (Adriatic) nesting males aggressively defend nests and take the initiative in courtship and perform sexual displays more often than females while in Ria Formosa (Southern Portugal) the pattern is reversed as a result of shortage of appropriate nesting sites. Nesting males from Ria Formosa had overall higher levels of brain aromatase mRNA expression than nesting males from Trieste, suggesting a higher brain estrogen synthesis in these males. Since in some fish species exogenous estradiol administration has been shown to decrease sexual and agonistic behaviors, the higher levels of brain aromatase in Ria Formosa nesting males may explain their reduced expression of sexual and aggressive displays when compared with nesting males from Trieste. Alternatively, the higher brain aromatase levels in nesting males from Ria Formosa could be a mechanism to decrease the putative androgen-induced activation of aggressive and sexual displays by reducing the local availability of androgens through their metabolization into estrogens. Although females and parasitic female-like males also differ in their displays between populations, the interpopulational pattern of brain aromatase mRNA expression was similar, suggesting that other neuroendocrine agents mediate the expression of female and female-like behaviors. In conclusion, brain aromatase availability seems like a probable mechanism to regulate the effects of steroids on the brain circuits underlying the expression of sexual and agonistic displays in S. pavo.     

Factors affecting aggressive behaviour of spawning migratory males towards mature male parr in masu salmon Oncorhynchus masou

This study examined whether dominant migratory males (adopting fighter tactics) of the masu salmon Oncorhynchus masou would more aggressively attack large mature male parr (adopting sneaker tactics) as large mature male parr are expected to have the potential to cause a greater decrease in fertilization success. The frequency of aggressive behaviour was not related to the body size of males, and it increased with the frequency of interactions with mature male parr. The fertilization success of mature male parr was much lower than migratory males, and no relationship was observed between fertilization success and aggressive behaviour. The low fertilization success of mature male parr, despite infrequent aggressive behaviour by migratory males, indicates that there might be little benefit for migratory males to attack mature male parr more aggressively according to their body size.     

Gonadal investment of young males in two blenniid fishes with alternative mating tactics

The males of two blenniid species which exhibited alternative life history tactics and matured in their first year of life varied in size distribution within the age class and in behaviour. Salaria pavo were the smaller fish of the age class and behaved as sneaker males whereas Parablennius sanguinolentus parvicornis were the larger fish and behaved as satellites.     

Reproductive phenology of the Azorean rock pool blenny a fish with alternative mating tactics

Both male and female Parablennius sanguinolentus parvicornis were ready to mate by the end of May. Seventy-five per cent of the 1-year-old males were mature, but only 25% of the females reached maturity at this age. In females, gonads formed an increasingly greater proportion of the total weight with age, but in males the proportion decreased. A bimodal distribution of gonadosomatic indices classes was observed in 2-year-old males (intermediate size), which reflected the lower opportunity that intermediate size males have to spend the ejaculates than have the younger and older males. The liver played an important role in the storage of energy before the reproductive season and reserves were utilized during the breeding season. Physical condition was at its lowest in July in both sexes, but in May, just before the breeding season began, large maturing females had significantly lower eviscerated condition than males. This could be due to females investing in oocyte development, while the priority for the males was to reserve their energy for the parental activities to come. In both males and females, older and bigger animals had lower hepatosomatic and body conditions than younger ones.     

Reproductive parasitism: male and female responses to conspecific and heterospecific intrusions at spawning in a mouth‐brooding cichlid Ophthalmotilapia ventralis

A rare form of alternative reproductive behaviour without simultaneous parasitic spawning was observed in Ophthalmotilapia ventralis, a lekking mouth‐brooding cichlid from Lake Tanganyika. Floater males attempted to sneak opportunistically into the territory to actively court the female, while the owner (bourgeois male) defended the territory against other potential intruders. Floater males had more body fat than territory owners and generally higher condition factors. In field experiments, the response of bourgeois males and courted females was tested towards floaters and egg predators (a catfish Synodontis multipunctatus) present in the territories. Territory owners responded aggressively particularly to floaters, and female responsiveness to bourgeois male courtship tended to decline when floaters were present. The potential influence of reproductive parasitism on sexual selection in mouth‐brooding cichlids is discussed.     

Tactic changes in dusky frillgoby Bathygobius fuscus sneaker males: effects of body size and nest availability

Field and laboratory studies were conducted to examine the effects of nest availability and body size on changes in male mating tactics from sneaking to nest‐holding in the dusky frillgoby Bathygobius fuscus. In the field, the body size of nest‐holding males decreased from early to mid‐breeding season, suggesting the possibility of a change in the tactics of sneaker males to nest‐holding. Many sneaker males did not use vacant spawning nests even when size‐matched nests were available, but they continued to reproduce as sneakers. Similarly, in aquarium experiments with available vacant nests, some sneaker males became nest‐holders irrespective of their body size, but some did not. These results showed that nest availability is not a limiting factor for changes in tactics by sneaker males in this species. Because tactic‐unchanged sneaker males were co‐housed with larger nest‐holding males in the tanks, the body size of nearby nest‐holding males may have affected the decision to change tactics for sneaker males. Moreover, smaller individuals among tactic‐changed males tended to spend more time until spawning, probably because they had relatively larger costs and smaller benefits of reproduction as nest‐holding males compared to larger males.     

Alternative life histories in the Atlantic salmon: genetic covariances within the sneaker sexual tactic in males

Alternative reproductive tactics are ubiquitous in many species. Tactic expression often depends on whether an individual's condition surpasses thresholds that are responsible for activating particular developmental pathways. Two central goals in understanding the evolution of reproductive tactics are quantifying the extent to which thresholds are explained by additive genetic effects, and describing their covariation with condition-related traits. We monitored the development of early sexual maturation that leads to the sneaker reproductive tactic in Atlantic salmon (Salmo salar L.). We found evidence for additive genetic variance in the timing of sexual maturity (which is a measure of the surpassing of threshold values) and body-size traits. This suggests that selection can affect the patterns of sexual development by changing the timing of this event and/or body size. Significant levels of covariation between these traits also occurred, implying a potential for correlated responses to selection. Closer examination of genetic covariances suggests that the detected genetic variation is distributed along at least five directions of phenotypic variation. Our results show that the potential for evolution of the life-history traits constituting this reproductive phenotype is greatly influenced by their patterns of genetic covariance.     

Alternative male reproductive strategies in the peacock blenny

A 4-year study (1989–1992) of a population of Lipophrys pavo living in a brackish lagoon (Maugio, France) revealed three types of male during the spawning season (April to September): (i) nest-breeder males which are territorial, and have well-developed secondary sexual characteristics; (ii) non-functional males which were abundant only in 1991 when population density was very high and (iii) 1-year-old kleptogamic males with small body size which possess neither secondary sexual organs nor a testicular gland, although their testes are functional and hyperdeveloped (up to 10.5% of carcass weight). The percentage of kleptogamic males was fairly stable in the population (from 7.9 to 10.0%) and highly variable in their age class (from 8.5 to 51.3%). It is suggested that kleptogamy is a conditional strategy adopted by smaller males.     

From sneaker to bourgeois male: Long-term observations on recognized tompot blenny Parablennius gattorugine individuals reveal new information on their biology

The behaviour of the tompot blenny Parablennius gattorugine was studied by underwater observation and photography on the south-west coast of the UK over an 11 year period, with >50 individuals identified at two locations by their distinctive skin markings. Observations showed males engaging in rapid swimming behaviour when approached by a female, and younger males using alternative ‘sneaker’ tactics before becoming ‘bourgeois’ territory-holders. The noninvasive recognition technique also facilitated detailed observations on territory retention (up to 7 years) and agonistic behaviours among both males and females.     

Androgen levels and social interactions in breeding males of the peacock blenny

Nest-holder male Salaria pavo have lower circulating concentrations of 11-ketotestosterone (KT) at the beginning of the breeding season than at its peak. At that peak density of nesting males was higher as were the number of visits of sneaker males to nests and of agonistic interactions between nest-holders and sneaker males. There was no difference between the two dates either in the frequency of male-male interactions or in the frequency of courtship episodes. Thus, higher plasma levels in nest-holders might be explained by a more intense sneaking pressure at the peak of the breeding season. At that peak, nest-holders had higher plasma levels of KT and a higher testosterone (T) to KT metabolization index in the gonads than did floater males. Both nest-holders and floaters had higher levels of KT and T in the testicular gland than in the testis. The levels of both androgens in the testicular gland, but not in the testis, were correlated with circulating concentrations of KT. These results suggest that the testicular gland is the major source of circulating KT in blenniids. Nest-holders had higher metabolization indexes than floaters both in the testis and in the testicular gland, which suggests that nest holding status promotes the conversion of T into KT.     

Mating tactics and male-male courtship in the lek-breeding cichlid Oreochromis mossambicus

Data are presented on the breeding behaviour of Oreochromis mossambicus under captive conditions. Males tended to synchronize their occupation of territories and breeding activities. Different male mating tactics were observed, namely establishing a breeding territory, acting as a floater, or behaving as a sneaker. The majority of spawnings observed involved dominant males and were subjected to interference from other males. Males were found to court other males that frequently responded to these attempts by adopting a female-like behaviour. Results are discussed in terms of a probable time constraint in territoriality, which promotes male-male competition and a low level of sex discrimination by territorial fish.     

Does the Refuge Availability Influence the Spawning Behavior of Mature Male Parr in Salmonids? A Test in the Miyabe Charr

In many salmon and charr, both 'migratory males' and 'precocious males' are maintained as alternative life-histories within a population. During breeding, precocious males gather around the mating pair of migratory fish and attempt to sneak in the spawning between larger male and female charr. Refuges such as debris and shallow areas may provide shelter from aggressive attacks and allow precocious males to hold positions closer to the pair (nest) and/or sneak more easily during the mating. Here we examine whether the availability of refuges influences the breeding behavior of precocious male parr of the Miyabe charr under experimental and natural conditions. Aggressive attacks directed toward precocious parr by the mating pair or other parr was not influenced by the refuge availability either under experimental conditions or in the wild. We did not find the effect of high refuge availability on the proximity of parr to the nest beyond the experimental conditions where the density of refuges was probably higher than in the natural stream. There were no effects of high refuge availability either on parr's attempts at sneak mating or on their success in spawning. Thus, our results provide little evidence that the refuge availability influences parr sneaking behavior. Other possible effects of high refuge availability, for example, the increase of fertilization success and the decrease of energy expenditure and risk taking, remain to be considered.     

Experimentally induced variation in neuroendocrine processes affects male reproductive behaviour,sperm characteristics and social interactions

While extensive research has focused on how social interactions evolve, the fitness consequences of the neuroendocrine mechanisms underlying these interactions have rarely been documented, especially in the wild. Here, we measure how the neuroendocrine mechanisms underlying male behaviour affect mating success and sperm competition in the ocellated wrasse (Symphodus ocellatus). In this species, males exhibit three alternative reproductive types. “Nesting males” provide parental care, defend territories and form cooperative associations with unrelated “satellites,” who cheat by sneaking fertilizations but help by reducing sperm competition from “sneakers” who do not cooperate or provide care. To measure the fitness consequences of the mechanisms underlying these social interactions, we used “phenotypic engineering” that involved administering an androgen receptor antagonist (flutamide) to wild, free‐living fish. Nesting males treated with flutamide shifted their aggression from sneakers to satellite males and experienced decreased submissiveness by sneaker males (which correlated with decreased nesting male mating success). The preoptic area (POA), a region controlling male reproductive behaviours, exhibited dramatic down‐regulation of androgen receptor (AR) and vasotocin 1a receptor (V1aR) mRNA following experimental manipulation of androgen signalling. We did not find a direct effect of the manipulation on male mating success, paternity or larval production. However, variation in neuroendocrine mechanisms generated by the experimental manipulation was significantly correlated with changes in behaviour and mating success: V1aR expression was negatively correlated with satellite‐directed aggression, and expression of its ligand arginine vasotocin (AVT) was positively correlated with courtship and mating success, thus revealing the potential for sexual selection on these mechanisms.