Julie K. Desjardins

Female promiscuity promotes the evolution of faster sperm in cichlid fishes

Sperm competition, the contest among ejaculates from rival males to fertilize ova of a female, is a common and powerful evolutionary force influencing ejaculate traits. During competitive interactions between ejaculates, longer and faster spermatozoa are expected to have an edge; however, to date, there has been mixed support for this key prediction from sperm competition theory. Here, we use the spectacular radiation of cichlid fishes from Lake Tanganyika to examine sperm characteristics in 29 closely related species. We provide phylogenetically robust evidence that species experiencing greater levels of sperm competition have faster-swimming sperm. We also show that sperm competition selects for increases in the number, size, and longevity of spermatozoa in the ejaculate of a male, and, contrary to expectations from theory, we find no evidence of trade-offs among sperm traits in an interspecific analysis. Also, sperm swimming speed is positively correlated with sperm length among, but not within, species. These different responses to sperm competition at intra- and interspecific levels provide a simple, powerful explanation for equivocal results from previous studies. Using phylogenetic analyses, we also reconstructed the probable evolutionary route of trait evolution in this taxon, and show that, in response to increases in the magnitude of sperm competition, the evolution of sperm traits in this clade began with the evolution of faster (thus, more competitive) sperm.

Masculinized dominant females in a cooperatively breeding species

The molecular mechanisms underlying complex social behaviours such as dominance are largely unknown. Studying the cooperatively breeding African cichlid Neolamprologus pulcher, we show that dominant females were similar to dominant males in dominance behaviour, high testosterone levels and brain arginine vasotocin expression (a neuropeptide involved in vertebrate territorial, reproductive and social behaviours) compared to subordinate helpers, but had lower levels of 11‐ketotestosterone than males. Furthermore, brain gene expression profiles of dominant females were most similar to those of the males (independent of social rank). Dominant breeder females are masculinized at the molecular and hormonal level while being at the same time reproductively competent, suggesting a modular organization of molecular and endocrine functions, allowing for sex‐specific regulation.

What do fish make of mirror images

Fish act aggressively towards their mirror image suggesting that they consider it another individual, whereas in some mammals behavioural response to mirrors may be an evidence of self-recognition. Since fish cannot self-recognize, we asked whether they could distinguish between fighting a mirror image and fighting a real fish. We compared molecular, physiological and behavioural responses in each condition and found large differences in brain gene expression levels. Although neither levels of aggressive behaviour nor circulating androgens differed between these conditions, males fighting a mirror image had higher immediate early gene (IEG) expression in brain areas homologous to the amygdala and hippocampus than controls. Since amygdalar responses are associated with fear and fear conditioning in other species, higher levels of brain activation when fighting a mirror suggest fish experience fear in response to fights with a mirror image. Clearly, the fish recognize something unusual about the mirror image and the differential brain response may reflect a cognitive distinction.

Sex differences in rates of territory joining and inheritance in a cooperatively breeding cichlid fish

In social groups, subordinates may gain dominant breeding status either by inheriting the top position in their current group or by dispersing to join a new group. The pathway to breeder status is likely to vary between males and females as a result of sex differences in the costs of dispersal and inbreeding. We report results from a field study conducted to explore sex differences in the rates of territory joining and inheritance in a cooperatively breeding cichlid, Neolamprologus pulcher. We experimentally created 34 breeding vacancies and investigated the effects of breeder removal on the degree of cooperative behaviour and how changes in status influenced reproductive physiology. We found that 71% of male vacancies were filled by joiners (incoming fish, not previously members of the group) entering the territory. In contrast, only 15% of female vacancies were filled by joiners entering the group from elsewhere. Helpers increased their frequency of cooperative behaviour following the removal of a female breeder, but not following removal of a male breeder. Our results suggest that female breeder vacancies are typically filled by subordinate helpers who inherit from within the group and that male breeder vacancies are commonly filled by joining individuals (existing breeders or former helpers from other groups). Male social status and gonadal investment were positively correlated. This study represents one of the first experimental attempts to examine sexual differences in the pathway to breeding status in a cooperatively breeding species.

Androgens and dominance: Sex-specific patterns in a highly social fish (Neolamprologus pulcher)

In most vertebrates, aggression and dominance are tightly linked to circulating testosterone. Fish, however, have two androgens (testosterone, T and 11-ketotestosterone, 11KT) that influence aggression and dominance. To date, few studies have compared the relationship between androgen levels and the outcome of aggressive contests in both females and males of the same species. To investigate sex differences in androgens we staged size-matched, limited-resource (territory) contests with 14 female-female and 10 male-male pairs of the highly social cichlid Neolamprologus pulcher. We then examined androgen levels in recently established dominants, who won the contest and subsequently acquired a territory (for 3h), and subordinates, who lost and did not acquire a territory. Newly dominant females had higher plasma T but similar 11KT levels to newly subordinate females. In contrast, newly dominant males had higher 11KT but similar T levels to subordinate males. The ratio of 11KT to T, which demonstrates physiological importance of T conversion to 11KT, was positively correlated with submissive behavior in female winners, and correlated weakly with aggressive behavior in male winners (p=0.05). These findings provide support for the hypothesis that different androgens play equivalent roles in female versus male dominance establishment, and suggest that relative levels of 11KT and T are implicated in female dominance behavior and perhaps behavior of both sexes.

Reproductive-Tactic-Specific Variation in Sperm Swimming Speeds in a Shell-Brooding Cichlid

Abstract Theory predicts that males experiencing elevated levels of sperm competition will invest more in gonads and produce faster-swimming sperm. Although there is ample evidence in support of the first prediction, few studies have examined sperm swimming speed in relation to sperm competition. In this study, we tested these predictions from sperm competition theory by examining sperm characteristics in Telmatochromis vittatus, a small shell-brooding cichlid fish endemic to Lake Tanganyika. Males exhibit four different reproductive tactics: pirate, territorial, satellite, and sneaker. Pirate males temporarily displace all other competing males from a shell nest, whereas sneaker males always release sperm in the presence of territorial and satellite males. Due to the fact that sneakers spawn in the presence of another male, sneakers face the highest levels of sperm competition and pirates the lowest, whereas satellites and territorials experience intermediate levels. In accordance with predictions, sperm from sneakers swam faster than sperm from males adopting the other reproductive tactics, whereas sperm from pirates was slowest. Interestingly, we were unable to detect any variation in sperm tail length among these reproductive tactics. Thus, sperm competition appears to have influenced sperm energetics in this species without having any influence on sperm size.

Sex and status in a cooperative breeding fish: behavior and androgens

Among taxonomically widespread cooperatively breeding vertebrates, those with non-breeding helpers-at-the-nest provide an excellent opportunity to understand the proximate mechanisms underlying care and allocare. In this study, we examined androgen levels in relation to care behavior in a cooperatively breeding cichlid fish, Neolamprologus pulcher, from Lake Tanganyika. We concentrated on androgens, as these hormones have been linked to the defense behavior, and the defense of young is a common form of parental care in fishes. N. pulcher dominant female breeders performed the most care and also displayed the highest levels of plasma testosterone (T) compared with other individuals within the social group. We also found that dominant male breeders provided a similar amount of care as did the subordinate helpers, but breeding males had the highest levels of 11-ketotestosterone (11KT), an important androgen in fish. Breeders had higher levels of both androgens (T and 11KT) compared to helpers. There was a weak but significant positive correlation between T levels and the frequency of care regardless of sex and status. Our results suggest that androgens may promote defense of young and are in contrast to the commonly reported trade-off between androgen and parental care.

Evidence for size and sex-specific dispersal in a cooperatively breeding cichlid fish

African Great Lake cichlid populations are divided into thousands of genetic subpopulations. The low gene flow between these subpopulations is thought to result from high degrees of natal philopatry, heavy predation pressure, and a patchy distribution of preferred habitats. While predation pressure and habitat distribution are fairly straightforward to assess, data on dispersal distances and rates are scarce. In fishes, direct observations of dispersal events are unlikely, but dispersal can be studied using molecular markers. Using seven microsatellite loci, we examined dispersal in the cooperatively breeding cichlid fish, Neolamprologus pulcher. As this species is found in well‐defined groups clustered into subpopulations, we could assess dispersal on a narrow (within subpopulation) and broad (between subpopulation) scale. While fish were generally more related to others in their own subpopulation than they were to fish from other subpopulations, large males diverged from this pattern. Large males were more related to other large males from different subpopulations than they were to large males from their own subpopulation, suggesting more frequent dispersal by large males. Across subpopulations, relatedness between large males was higher than the relatedness among large females; this pattern was not detected in small males and small females. Within a subpopulation, individuals appeared to be preferentially moving away from relatives, and movement was unrestricted by the physical distance between groups. Our results highlight the importance of examining multiple spatial scales when studying individual dispersal biases.

Female genomic response to mate information

Females should be choosier than males about prospective mates because of the high costs of inappropriate mating decisions. Both theoretical and empirical studies have identified factors likely to influence female mate choices. However, male–male social interactions also can affect mating decisions, because information about a potential mate can trigger changes in female reproductive physiology. We asked how social information about a preferred male influenced neural activity in females, using immediate early gene (IEG) expression as a proxy for brain activity. A gravid female cichlid fish (Astatotilapia burtoni) chose between two socially equivalent males and then saw fights between these two males in which her preferred male either won or lost. We measured IEG expression levels in several brain nuclei including those in the vertebrate social behavior network (SBN), a collection of brain nuclei known to be important in social behavior. When the female saw her preferred male win a fight, SBN nuclei associated with reproduction were activated, but when she saw her preferred male lose a fight, the lateral septum, a nucleus associated with anxiety, was activated instead. Thus social information alone, independent of actual social interactions, activates specific brain regions that differ significantly depending on what the female sees. In female brains, reproductive centers are activated when she chooses a winner, and anxiety-like response centers are activated when she chooses a loser. These experiments assessing the role of mate-choice information on the brain using a paradigm of successive presentations of mate information suggest ways to understand the consequences of social information on animals using IEG expression.

Social Context Influences Aggressive and Courtship Behavior in a Cichlid Fish

Social interactions require knowledge of the environment and status of others, which can be acquired indirectly by observing the behavior of others. When being observed, animals can also alter their signals based on who is watching. Here we observed how male cichlid fish (Astatotilapia burtoni) behave when being watched in two different contexts. In the first, we show that aggressive and courtship behaviors displayed by subordinate males depends critically on whether dominant males can see them, and in the second, we manipulated who was watching aggressive interactions and showed that dominant males will change their behavior depending on audience composition. In both cases, when a more dominant individual is out of view and the audience consists of more subordinate individuals, those males signal key social information to females by displaying courtship and dominant behaviors. In contrast, when a dominant male is present, males cease both aggression and courtship. These data suggest that males are keenly aware of their social environment and modulate their aggressive and courtship behaviors strategically for reproductive and social advantage.