Socially controlled male-to-female sex reversal in the protogynous orange-spotted grouper,Epinephelus coioides

Socially controlled sex change in teleosts is a dramatic example of adaptive reproductive plasticity. In many cases, the occurrence of sex change is triggered by a change in the social context, such as the disappearance of the dominant individual. The orange-spotted grouper Epinephelus coioides is a typical protogynous hermaphrodite fish that changes sex from female to male and remains male throughout its life span. In this study, male-to-female sex reversal in male Epinephelus coioides was successfully induced by social isolation. The body length and mass, gonadal change, serum sex steroid hormone levels and sex-related gene expression patterns during the process of socially controlled male-to-female sex reversal in E. coioides were systematically examined. This report investigates the physiological mechanisms of the socially controlled male-to-female sex reversal process in a protogynous hermaphrodite grouper species. The results enable us to study the physiological control of sex change, not only from female to male, but also from male to female.     

Natural sex change in mature protogynous orange-spotted grouper (Epinephelus coioides): gonadal restructuring,sex hormone shifts and gene profiles

Sexual patterns of teleosts are extremely diverse and include both gonochorism and hermaphroditism. As a protogynous hermaphroditic fish, all orange-spotted groupers (Epinephelus coioides) develop directly into females, and some individuals change sex to become functional males later in life. This study investigated gonadal restructuring, shifts in sex hormone levels and gene profiles of cultured mature female groupers during the first (main) breeding season of 2019 in Huizhou, China (22° 42′ 02.6″ N, 114° 32′ 10.1″ E). Analysis of gonadal restructuring revealed that females with pre-vitellogenic ovaries underwent vitellogenesis, spawning and regression and then returned to the pre-vitellogenic stage in the late breeding season, at which point some changed sex to become males via the intersex gonad stage. A significant decrease in the level of serum 17β-estradiol (E2) was observed during ovary regression but not during sex change, whereas serum 11-ketotestosterone (11-KT) concentrations increased significantly during sex change with the highest concentration in newly developed males. Consistent with serum hormone changes, a significant decrease in cyp19a1a expression was observed during ovary regression but not during sex change, whereas the expression of cyp11c1 and hsd11b2 increased significantly during sex change. Interestingly, hsd11b2 but not cyp11c1 was significantly upregulated from the pre-vitellogenic ovary stage to the early intersex gonad stage. These results suggest that a decrease in serum E2 concentration and downregulation of cyp19a1a expression are not necessary to trigger the female-to-male transformation, whereas increased 11-KT concentration and upregulation of hsd11b2 expression may be key events for the initiation of sex change in the orange-spotted grouper.     

Etude des interactions sociales entre male et femelle chez la Genette (Genetta genetta L.): Relations entre marquage olfactif et agression

Study on Social Interactions between Male and Female Genets (Genetta genetta L.): Relations between Scent Marking and Aggression The aim of this work was to study the relations between marking behaviour and aggression in genets (Genetta genetta L.). Observations on social interactions were made on a socially stable pair and during encounters between unfamiliar pairs. In the first case, there appeared to be a relationship between marking activity in the male and aggression. During aggression periods, marking with the ano-urogenital region increased in the male and decreased in the female. Another striking variation concerned flank rubbing and hindleg rubbing. In both male and female these marking frequencies increased significantly during aggression periods and flank rubbing was modified by visual cues. Data recorded during encounters between unfamiliar pairs (one male being introduced in a female's cage) showed that agonistic behaviours were released through visual cues in females and olfactory cues in males. The same changes in marking frequencies were observed. These results also showed that ano-urogenital marking was inhibited in females during aggression periods. The adaptative significance of these phenomena is discussed.     

Olfactory Snake‐Predator Discrimination in the Cape Ground Squirrel

Small mammals have a number of means to detect and avoid predators, including visual, auditory and olfactory cues. Olfactory cues are particularly important for nocturnal or fossorial species where visual cues would not be as reliable. The Cape ground squirrel (Xerus inauris) is a semi‐fossorial, diurnal mammal from southern Africa. Cape ground squirrels encounter multiple species of predatory snake that pursue individuals underground where visual and social cues are limited. We assessed whether Cape ground squirrels use odours to discriminate between snakes by presenting a non‐venomous snake, a venomous snake and a control odour collected on polyethylene cubes to 11 adult female squirrels from 11 different social groups. Cape ground squirrels responded by inspecting the cube, displaying snake harassment–associated behaviours and decreasing time spent in close proximity to snake odours when compared with a control. They also displayed discrimination between two snake species by increasing the frequency of cube inspection and increasing harassment behaviours with venomous snake odours when compared with non‐venomous snake odours. We conclude that Cape ground squirrels respond with snake‐specific antipredator behaviours when presented olfactory cues alone. Olfactory discrimination may be maintained by the decreased utility of other methods of predator detection: sight and group detection, in below‐ground encounters.     

A preliminary study of olfactory behavior of captiveLemur coronatus during the breeding season

The olfactory behavior of a captive population of crowned lemurs (Lemur coronatus)was studied during their annual breeding season in order to investigate its possible role in the fine-tuning of mating synchrony after photoperiodic initiation of reproductive activity. The frequencies of five stereotyped olfactory behavior patterns were recorded in four male-female groups during 315 1-hr observation sessions between October and March. The mean total scent-marking frequency of all males was positively correlated with their mean testicular size. Male anogenital-, head-, and allomarking frequencies decreased during the breeding season, whereas hand-marking frequencies remained constant. Male head-marking increased significantly in the 5 days preceding female vaginal estrus. Furthermore, males responded to many female scents by olfactory investigation and/or overmarking, whereas females never showed an observable behavioral response to male scent marks. The marking frequencies of two females did not change significantly during the breeding season, while those of two others decreased significantly. These results suggest qualitative changes of female scents during estrus and a less important role of male scents in intersexual communication in the context of reproduction than previously thought.     

Visual sex discrimination in goldfish: seasonal, sexual, and androgenic influences

The olfactory signals used by goldfish for sexual and aggressive communication have been studied extensively, but little work has addressed the role of other sensory modalities in social communication in this species. We therefore investigated the role that visual stimuli play in sex discrimination and the ability of androgens, which masculinize courtship behavior, to affect behavioral responses toward female visual stimuli. We found that males selectively orient toward female visual stimuli during the breeding season but not outside it, whereas prostaglandin F2-alpha (PGF2alpha)-injected females do not differentially approach male and female visual stimuli, even during the breeding season. Implanting adult females with testosterone (T) and 11-ketotestosterone (KT), however, induced orientation responses toward female visual stimuli similar to those observed in males. These results indicate that visual sexual stimuli are likely important for reproductive signaling in goldfish, potentially helping males identify ovulating females from a distance in a shoal of fish, and that androgens can influence mechanisms associated with orientation responses toward such stimuli.     

Early sex change: A possible mating strategy ofCentropyge angelfishes (Pisces: Pomacanthidae)

Although the presence of socially controlled sex change in pomacanthid fishes of the genusCentropyge has been known since 1978, it has always been assumed that such sex change occurred only after the death or disappearance of the dominant male in single male social groups. Between 1978 and 1983, we observed several incidences of sex change by ranking female angelfishes within their harems and in the presence of the dominant male in each such harem. This phenomenon was observed inCetropyge interruptus andCentropyge tibicen, and occurred frequently enough to suggest the possibility of early sex change as a normal reproductive strategy in these species. Possible advantages of early sex change are discussed.     

Water temperature and pH influence olfactory sensitivity to pre-ovulatory and post-ovulatory ovarian pheromones in male Barilius bendelisis

The attractive response and sexual activity elicited by pre-ovulatory steroid sulphate and post-ovulatory 15K-PGF pheromones are greater in wild caught tubercular males and immature males which express breeding tubercles on the snout (at 12–13 days post androgen implant) than in non-tubercular and non-androgen implanted males of freshwater fishBarilius bendelisis. This shows that circulatory androgens exert an activational effect on olfactory receptors of male fish. Wild caught tubercular males and androgen implanted juvenile males exhibit a high responsiveness to steroid sulphate at the water temperature and pH which fish experience during the pre-spawning phase. The male’s sensitivity to 15K-PGF is almost equally high at the water temperature and pH which they experience in wild during the both pre-spawning and spawning periods. This suggests that the differential olfactory sensitivity to the two classes of pheromones in androgen implanted males is due to the varied temperature and pH of water, and that during the breeding season the male’s olfactory sensitivity to PGF pheromone is more widespread than to the steroidal pheromone. An increased and decreased olfactory sensitivity in mature males to sex pheromones and L-alanine respectively during the breeding phase is in agreement with the hypothesis that pheromonal stimuli dominate over feeding stimuli to promote spawning success.     

Effect of light intensity on the shoaling behaviour of the guppy (Poecilia reticulata)

It has been shown that the tendency of fish to shoal decreases as night falls. Much is known about shoaling in the daytime, however, little is known about the social behaviour of fish at night. Although the nocturnal disintegration of shoal structure is the conventional expectation for most diurnal marine fish, it has not yet been investigated for diurnal freshwater fish. This possibility has been investigated using guppies (Poecilia reticulata), collected from the wild, as an experimental model. Three preference tanks were used, one of which permitted only visual cues, another only olfactory cues and the other both visual and olfactory cues. Shoaling tendency was observed at four different light intensities (8 wt/m, 0·05 wt/m, 0·025 wt/m, 0·003 wt/m). These light intensities were chosen to mimic daylight, dawn/dusk, clear night and cloudy night conditions, respectively. Trials were carried out on randomly selected male guppies. Results indicated that with both modalities present fish significantly preferred the stimulus shoal at all light intensities. However with only one modality to indicate the presence of the shoal, fish showed no significant shoaling tendency at any of the diminished light intensities. A test of shoal cohesion at the four different light intensities was carried out on freely interacting fish. This test condition was chosen to mimic the situation of guppies in the wild. The results to date suggest that guppies continue to shoal during dusk (at low light intensities) but not during the night. These findings make an important contribution to our understanding of the social behaviour of fish at night and deserve further investigation.     

Larval Ischnura verticalis (Odonata: Coenagrionidae) Respond to Visual Cues of Predator Presence

Larvae of some species of damselflies respond to chemical cues of fish predators but, while larvae of many species are thought to detect prey through vision, there is little evidence that larvae respond to visual cues of predator presence. This laboratory study indicated larval Ischnura verticalis behaviours are affected by visual cues and, to a much lesser extent, chemical cues of fish; there was no significant interaction between the effects of visual and chemical cues. Responses to chemical cues of fish did not depend on whether fish were fed I. verticalis larvae versus commercial fish food. Larvae were more active in the spring than the fall when they were likely in diapause. Results suggest larvae can use vision to detect large, active predators but can also detect predators through olfaction when visual cues are unreliable.     

Baby on board: olfactory cues indicate pregnancy and fetal sex in a non-human primate

Olfactory cues play an integral, albeit underappreciated, role in mediating vertebrate social and reproductive behaviour. These cues fluctuate with the signaller''s hormonal condition, coincident with and informative about relevant aspects of its reproductive state, such as pubertal onset, change in season and, in females, timing of ovulation. Although pregnancy dramatically alters a female''s endocrine profiles, which can be further influenced by fetal sex, the relationship between gestation and olfactory cues is poorly understood. We therefore examined the effects of pregnancy and fetal sex on volatile genital secretions in the ring-tailed lemur (Lemur catta), a strepsirrhine primate possessing complex olfactory mechanisms of reproductive signalling. While pregnant, dams altered and dampened their expression of volatile chemicals, with compound richness being particularly reduced in dams bearing sons. These changes were comparable in magnitude with other, published chemical differences among lemurs that are salient to conspecifics. Such olfactory ‘signatures’ of pregnancy may help guide social interactions, potentially promoting mother–infant recognition, reducing intragroup conflict or counteracting behavioural mechanisms of paternity confusion; cues that also advertise fetal sex may additionally facilitate differential sex allocation.     

Behavioural plasticity and sex differences in host finding of a specialized bee species

Many animals feed on flowers, and visual as well as olfactory cues are considered as most important mediators in animal–plant interactions. However, the relative importance of these cues is not well understood. Bees are the most important animal pollinators worldwide and here, we determined the importance of decoupled and combined visual and olfactory cues of Lysimachia punctata (Primulaceae) for host plant location in both sexes of the specialized, solitary bee, Macropis fulvipes (Melittidae). Lysimachia-inexperienced female bees preferred olfactory over visual cues though visual cues increased the attractiveness of olfactory ones. In experienced females, the importance of visual cues was increased. Both Lysimachia-naive and -experienced males relied more on visual cues as compared to females. This study demonstrates that the relative weighting of cues used for host plant finding depends on the sex and experience of M. fulvipes. The latter finding reveals the presence of learning-induced behavioural plasticity in host plant finding for a bee species. It may allow the bee to forage highly efficient. Visually guided female detection on flowers by males is a likely functional explanation for the differences in the weighting of visual and olfactory cues between the sexes.     

Oscillatory Electric Potential on the Olfactory Epithelium Observed during the Breeding Migration Period in the Japanese Toad, Bufo japonicus

Japanese toad (Bufo japonicus) tracks the route to and from the breeding sites using the olfactory cues from the migration route and not from the destination (). We recorded a slow extracellular potential change (electro-olfactogram or EOG) evoked on the olfactory epithelium by applying an olfactory stimulus with an air stream. In September toads, only a simple typical EOG that is common in various vertebrate species was observed. Oscillatory potential changes (OSC) superimposed on the typical EOG were observed in the breeding season when studied throughout a year. There were no sexual differences in the occurrence and the amplitude of the OSC. Oscillatory potentials were observed also from the olfactory nerve of the brain. The OSC in the olfactory epithelium remained even after denervation. In addition, it was suggested that there are multiple sites of OSC initiation in the olfactory epithelium. These results suggest an intimate relationship between OSC appearance and the breeding migration in the toad.     

Smelling right: the scent of male lemurs advertises genetic quality and relatedness

Sexual selection theory predicts that competitors or potential mates signal their quality or relatedness to conspecifics. Researchers have focused on visual or auditory modes of signal transmission; however, the importance of olfactory indicators is gaining recognition. Using a primate model and a new integrative analytical approach, we provide the first evidence relating male olfactory cues to individual genome-wide heterozygosity and to the genetic distance between individuals. The relationships between male semiochemical profiles and genetic characteristics are apparent only during the highly competitive and stressful breeding season. As heterozygosity accurately predicts health and survivorship in this population, we identify scrotal olfactory cues as honest indicators of male quality, with relevance possibly to both sexes. Beyond showing that semiochemicals could underlie kin recognition and nepotism, we provide a putative olfactory mechanism to guide male–male competition and female mate choice.     

Turbidity Hampers Mate Choice in a Pipefish

European coastal waters have in recent years become more turbid as algal growth has increased, probably due to eutrophication, global warming and changes in fish communities. Turbidity reduces visibility, and such changes may in turn affect animal behaviour as well as evolutionary processes that are dependent on visual stimuli. In this study we experimentally manipulated water visibility and olfactory cues to investigate mate choice using the sex role‐reversed broad‐nosed pipefish Syngnathus typhle as our study organism. We show that males spent significantly longer time assessing females when they had access to full visual cues, compared to when visibility was reduced. Presence or absence of olfactory cues from females did not affect mate choice, suggesting that the possible use of smell could not make up for a reduction in visibility. This implies that mate choice is environmentally dependent and that an increased turbidity may affect processes of sexual selection through an impaired possibility for visually based mate choice.     

Electrocommunication behaviour and non invasively-measured androgen changes following induced seasonal breeding in the weakly electric fish, Apteronotus leptorhynchus

Androgens are known to be involved in reproductive behaviours including courtship and aggression. According to the Challenge Hypothesis, androgen activity upregulates male reproductive behaviour seasonally and also modulates short term adaptation of these behaviours in response to social context. In the weakly electric fish, Apteronotus leptorhynchus, 11-ketotestosterone (11-KT) has been previously implicated in the regulation of electrocommunication behaviours that are believed to have roles in both aggression and courtship. Changes in male 11-KT levels were quantified using a non-invasive measurement technique alongside changes in electrocommunication behaviour following environmental cues that simulated the onset of the breeding season. Males showed an increase in mean electric organ discharge frequency (EODf), which is consistent with earlier results showing a female preference for high EODf. A subset of males with high initial EODfs showed increases in both 11-KT and EODf, which provides support for an EODf-based dominance hierarchy in this species. Males housed in social conditions and exposed to breeding conditioning also showed higher overall electric organ discharge frequencies and 11-KT compared to males housed in isolation. Evidence is presented that another type of electrocommunication signal previously implicated in courtship may also serve as an inter-male signal of submission. Our results are consistent with earlier observations that electrocommunication signals produced during inter-male aggression serve in deterring attacks, and their pattern of production further suggested the formation of a dominance hierarchy.     

Olfactory gene expression in migrating adult sockeye salmon Oncorhynchus nerka

Expression of 12 olfactory genes was analysed in adult sockeye salmon Oncorhynchus nerka nearing spawning grounds and O. nerka that had strayed from their natal migration route. Variation was found in six of these genes, all of which were olfc olfactory receptors and had lower expression levels in salmon nearing spawning grounds. The results may reflect decreased sensitivity to natal water olfactory cues as these fish are no longer seeking the correct migratory route. The expression of olfactory genes during the olfactory‐mediated spawning migration of Pacific salmon Oncorhynchus spp. is largely unexplored and these findings demonstrate a link between migratory behaviours and olfactory plasticity that provides a basis for future molecular research on salmon homing.     

Seasonal changes of serum sex steroids concentration and aromatase activity of gonad and brain in red-spotted grouper (Epinephelus akaara)

Levels of serum sex steroids (estradiol-17beta, E2; testosterone, T; 11-ketotestosterone, 11-KT) in male, female and natural sex-reversing red-spotted grouper (Epinephelus akaara), and aromatase activity of gonad and brain in both male and female were investigated throughout an annually reproductive cycle. In females, serum E2 and T peaked during vitellogenesis, but in males and natural sex-reversing fish, 11-KT, T and E2 reached peak during spermatogenesis. In addition, in females, serum 11-KT levels (monthly means: 0.32 +/- 0.03 ng/ml) which were very low did not significantly fluctuate during the annual reproductive cycle. In breeding season, females displayed higher E2 levels than males and sex-reversing fish, while males and sex-reversing fish showed higher 11-KT levels and, to a lesser extent, higher T levels than females. Furthermore, the changing pattern of sex steroids in males was similar to that in natural sex-reversing fish, and a second peak of serum androgens 11-KT and T appeared in December both in male and natural sex-reversing fish; significantly higher serum 11-KT levels were observed in natural sex-reversing fish than that in females from December to April. In females, but not in males, aromatase activity of brain and gonad demonstrated significantly seasonal changes (exhibiting a peak in breeding season); moreover, aromatase activity in females was higher than that in males. Furthermore, significantly lower aromatase activity in testis was observed in breeding season, in contrast to that in ovary. Taken together, the present findings indicated that changes of serum sex steroids levels and aromatase activity in red-spotted grouper were closely associated with sex inversion. In addition, the present results also suggested that sex inversion in red-spotted grouper peaked mainly from December to March.     

Male-biased Adult Sex Ratios and their Significance for Cooperative Breeding in Dhole,Cuon alpinus,Packs

Two free-ranging packs of dholes (Asiatic wild dog, Cuon alpinus) were monitored for a period of 6 yr (Sep. 1990-Sep. 1996) in the Mudumalai sanctuary, southern India. Demographic data on age structure, litter-size, sex ratio and age and sex specific dispersal were collected. Behavioural data on social interactions and reproductive behaviour among pack members were obtained to determine the frequencies of dominant and subordinate behaviours shown by male and female pack members and a measure of each male's reproductive access to females. Behaviours displayed by pack members at dens were recorded to determine whether any age- or sex-specific role specialization existed during pup care. Tenures for dominant males and females within the pack were calculated to ascertain the rate of breeding vacancies occurring within packs. Approximate levels of genetic relatedness within packs were determined by studying pedigrees. In most years one study pack had a male-biased adult sex ratio. This was caused by almost two-fold higher dispersal of adult females over adult males. A considerable variance existed in the percentage of sub-adults dispersing from the two packs. Differences existed in the frequencies of dominant and subordinate behaviours shown by males. For males, dominance ranks and ranks based on submissive behaviours were not correlated with frequencies of reproductive behaviours. Subordinate males also displayed reproductive behaviours. In packs, dominant males had lower tenures than dominant females indicating that among males breeding vacancies arose more quickly. The litter size was found to be negatively correlated with the age of the breeding female. There were no significant differences across individuals of varying age or sex classes in the display of pup care behaviours. Significant differences did exist among individual adults. Genetic relatedness among packs tended to vary temporally as a consequence of possible mating by subordinate animals and immigration of new males into the pack. In conclusion, it appears that males delay dispersal and cooperate within their natal packs because of the variety of reproductive strategies they could pursue within. A combination of ecological constraints and the difficulties of achieving breeding status within non-natal packs may make early dispersal and independent breeding less beneficial.