[show abstract][hide abstract] ABSTRACT: 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.
Behavioral Ecology and Sociobiology 04/2012; 62(5):785-794. · 2.75 Impact Factor
[show abstract][hide abstract] ABSTRACT: 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.
PLoS ONE 01/2012; 7(7):e32781. · 3.73 Impact Factor
[show abstract][hide abstract] ABSTRACT: Within animal societies, the ecological and social underpinnings of mating system variation can be related to resource dispersion, sexual conflict between breeders, and the effects of non-breeders. Here, we conducted a broad-scale investigation into the evolution of mating systems in the cooperatively breeding cichlid, Neolamprologus pulcher, a species that exhibits both monogamy and polygyny within populations. Using long-term field data, we showed that polygynous groups were more spatially clustered and held by larger competitively superior males than were monogamous groups, supporting the role of resource dispersion. To explore the role of sexual conflict, we forced polygynous males to become experimentally monogamous (EM) in the field. EM males spent more time on their remaining territory than naturally polygynous males but otherwise did not change behaviorally or physiologically. Females mated to EM males performed more submissive acts, and in a forced choice experiment, females did not preferentially associate with the larger of two unmated males. Females may therefore incur an unexpected cost from mating monogamously with a large and competitively superior male, a cost that mitigates sexual conflict over the mating system. Helpers were more closely related in monogamous groups but did not behave differently under monogamy or polygyny. Helpers therefore seem neither to be affected by nor affect the mating system of breeders. Our results demonstrate the roles of resource availability and conflict mitigation in determining the mating system, and highlight the importance of experimental manipula-tion for revealing hidden costs of hypothetical mating patterns.
[show abstract][hide abstract] ABSTRACT: Natural environmental periodicity that occurs on both the small scale like day length, or larger scale like lunar light can provide animals with valuable information about resource availability and predation risk. Such environmental cycles are often linked to the timing of reproduction. Here, using the circulating androgen concentrations, gonadal investment patterns and detailed behavioral observations we show that wild populations of the group-living cichlid, Neolamprologus pulcher from Lake Tanganyika, have marked diurnal differences in behavior and lunar synchronicity in their reproductive physiology and behavior. Female ovarian investment peaked in the first quarter of the lunar cycle. In males, plasma steroid hormone levels and sperm swimming speed were highest at this same lunar stage, supporting the idea that egg laying occurs during this phase and that young will emerge at full moon, perhaps because nocturnal predators can be best detected then. Female subordinate group members' gonadal investment patterns mirrored the lunar pattern observed in dominant female breeders. In contrast, male subordinates did not show a change in gonadal investment or in steroid hormone concentrations across the lunar cycle, suggesting that female subordinates, but not male subordinates, reproduce within the social group. Neolamprologus pulcher demonstrated diurnal cycles in behavior, with higher rates of feeding in the morning. Male and female breeding pairs were strongly size matched potentially as a result of size-assortative mating; also the gonadal investment of male and female mated pairs was strongly correlated indicating within-pair reproductive synchronicity. In general, this study provides evidence for the impact of environmental cues (sunlight and moonlight) on circulating hormones and reproduction in a small tropical freshwater fish.
[show abstract][hide abstract] ABSTRACT: 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.
Proceedings of the National Academy of Sciences 12/2010; 107(49):21176-80. · 9.74 Impact Factor
[show abstract][hide abstract] ABSTRACT: Learning is ubiquitous in the animal kingdom but has been studied extensively in only a handful of species. Moreover, learning studied under laboratory conditions is typically unrelated to the animal's natural environment or life history. Here, we designed a task relevant to the natural behavior of male African cichlid fish (Astatotilapia burtoni), to determine if they could be trained on a spatial task to gain access to females and shelter. We measured both how successfully animals completed this task over time and whether and how immediate early gene and hormone expression profiles were related to success. While training fish in a maze, we measured time to task completion, circulating levels of three key hormones (cortisol, 11-ketotestosterone, and testosterone) and mRNA abundance of seven target genes including three immediate early genes (that served proxies for brain activity) in nine brain regions. Data from our subjects fell naturally into three phenotypes: fish that could be trained (learners), fish that could not be trained (non-learners) and fish that never attempted the task (non-attempters). Learners and non-learners had lower levels of circulating cortisol compared to fish that never attempted the task. Learners had the highest immediate early gene mRNA levels in the homologue of the hippocampus (dorsolateral telencephalon; Dl), lower cortisol (stress) levels and were more motivated to accomplish the task as measured by behavioral observations. Fish that never attempted the task showed the lowest activity within the Dl, high stress levels and little to no apparent motivation. Data from non-learners fell between these two extremes in behavior, stress, and motivation.
Neurobiology of Learning and Memory 12/2010; 95(3):277-85. · 3.33 Impact Factor
[show abstract][hide abstract] ABSTRACT: 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.
[show abstract][hide abstract] ABSTRACT: Wild groups (n = 167) of the cooperatively breeding Lake Tanganyika cichlid, Neolamprologus pulcher, were used to investigate how social status and sex influence liver investment. In contrast to expectations, males and females (controlling for body size) had similar liver investment and subordinates (both sexes) had relatively larger livers compared with dominants. Three hypotheses were considered for why social status results in liver size disparity: liver mass might reflect status-dependent differences in (1) energy expenditure, (2) energy storage and (3) energy acquisition. First, dominants performed more energetically costly behaviours (e.g. social policing and care) compared with subordinates, supporting the notion that energy expenditure drives liver investment. Moreover, dominants in large groups (with many subordinates to monitor) and those holding multiple territories (with large areas to patrol), tended to have smaller livers. Second, subordinates did not appear to use the liver as a strategic energy storage organ. In laboratory and field experiments, subordinates ascending in rank had similar or larger livers during periods of rapid growth compared with non-ascending controls. Third, although subordinates fed more frequently than dominants, a negative relationship was found between feeding rates and liver size. Hence, these results contrast with previous liver studies and suggest that liver investment patterns were linked to status-driven differences in energy expenditure but not to energy intake or storage in N. pulcher.
Journal of Fish Biology 07/2009; 75(1):1-16. · 1.83 Impact Factor
[show abstract][hide abstract] ABSTRACT: Genetic data collected on co-operatively breeding Neolamprologus pulcher groups from Lake Tanganyika revealed mixed parentage in 80% of the groups examined. A case (1/11) of shared maternity was detected where a subordinate female bred alongside the dominant female in a social group. Extra-pair paternity was assigned to other dominant males who held their own social groups, but subordinate males were not found to father young in any group (0/9).
Journal of Fish Biology 04/2009; 74(5):1129-35. · 1.83 Impact Factor
[show abstract][hide abstract] ABSTRACT: 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 3 h), 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.
[show abstract][hide abstract] ABSTRACT: 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.
Proceedings of the National Academy of Sciences 02/2009; 106(4):1128-32. · 9.74 Impact Factor
[show abstract][hide abstract] ABSTRACT: How does living in a social environment influence the brain? In particular, we ask the following questions: How do animals perceive and use social information? How does the perception of social information influence the reproductive system? Where is this represented in the brain? We present a model system in which these questions can be addressed, focusing on the brain's role in integrating information. In the social fish, Astatotilapia burtoni (Haplochromis), the relationship between social status and gonadotropin-releasing hormone (GnRH1) has been well established. Change in status results in numerous changes in the physiology of A. burtoni at every level of organization. Social status can regulate reproduction via the hypothalamic-pituitary-gonadal (HPG) axis. GnRH1 is used by the brain to signal the pituitary about reproductive state so reproductive control depends on regulation of this signaling peptide. In this fish, social dominance is tightly coupled to fertility. Here, we have exploited this link to understand the regulatory systems from circulating hormones, brain volume to gene expression.
Integrative and Comparative Biology 11/2008; 48(5):596-603. · 3.02 Impact Factor
[show abstract][hide abstract] ABSTRACT: In highly social species, dominant individuals often monopolize reproduction, resulting in reproductive investment that is status dependent. Yet, for subordinates, who typically invest less in reproduction, social status can change and opportunities to ascend to dominant social positions are presented suddenly, requiring abrupt changes in behaviour and physiology. In this study, we examined male reproductive anatomy, physiology and behaviour following experimental manipulations of social status in the cooperatively breeding cichlid fish, Neolamprologus pulcher. This unusual fish species lives in permanent social groups composed of a dominant breeding pair and 1-20 subordinates that form a linear social dominance hierarchy. By removing male breeders, we created 18 breeding vacancies and thus provided an opportunity for subordinate males to ascend in status. Dominant females play an important role in regulating status change, as males successfully ascended to breeder status only when they were slightly larger than the female breeder in their social group. Ascending males rapidly assumed behavioural dominance, demonstrated elevated gonadal investment and androgen concentrations compared with males remaining socially subordinate. Interestingly, to increase gonadal investment ascending males appeared to temporarily restrain somatic growth. These results highlight the complex interactions between social status, reproductive physiology and group dynamics, and underscore a convergent pattern of reproductive investment among highly social, cooperative species.
Proceedings of the Royal Society B: Biological Sciences 05/2008; 275(1637):929-36. · 5.68 Impact Factor
[show abstract][hide abstract] ABSTRACT: In cooperatively breeding species, members of social groups will risk serious injury or even their lives by actively codefending the communal territory and young in the territory. However, individuals within the group vary in the intensity and frequency of defence. To date little is known about how sex, body size and social status interact with the degree of threat to influence defence activities. To this end, we experimentally manipulated the need for defence in wild groups of the cooperatively breeding cichlid, Neolamprologus pulcher by exposing social groups to four intruder types representing different forms of threat. Intruders were introduced singly (experiment 1) to assess the costs and benefits associated with defence and in tandem (experiment 2) to assess how individuals prioritize perceived threats. Dominant breeders defended more than subordinate helpers, females were more aggressive than males, and female breeders defended more than any other individual in the group. Individual body size, or the difference in body size between intruders and defenders, had no influence on the frequency of defence. Dominant male breeders defended most vigorously against threats to their dominance position, while dominant female breeders showed the highest defence rates to both threats to their position and the security of young to a similar degree relative to all others. Predators evoked the strongest defence responses by subordinate helpers, and conspecific intruders evoked the weakest responses relative to all other intruder types. The results suggest that both costs and benefits have shaped aggressive defence patterns in this cooperatively breeding teleost fish.
[show abstract][hide abstract] ABSTRACT: Polygyny is regarded as a beneficial strategy for males, whereas females mated with polygynous males (males simultaneously paired to more than one female) often suffer a reduction in pair male contributions. This study examined the costs and benefits associated with polygyny in the cooperatively breeding cichlid Neolamprologus pulcher. In this species, males are facultatively polygynous; some males hold only one territory with one breeding female whereas other males hold multiple territories, each with its own breeding female. Polygynous males were larger than monogamous males and body-scraped less, a behaviour often associated with ectoparasite loads. Polygynous males also had larger testes (controlling for body mass) and higher circulating 11-ketotestosterone levels than monogamous males. Paradoxically, monogamous males occupied higher-quality territories with more shelter and fewer predators. Monogamous males also provided more parental care than polygynous males but the number and survival of young did not vary according to male mating behaviour. The results of our study suggest that females trade-off between male genetic quality and resources in N. pulcher. Our results imply that males holding only one territory may provide their mates with significant assets but may not be able to outcompete neighbours for additional breeding positions because of their small body size and possible higher parasite load. The lack of differences between monogamous and polygynous groups in terms of offspring survival (a measure of reproductive success) suggests that there may be few if any fitness consequences of polygynous pairing for females.
[show abstract][hide abstract] ABSTRACT: Breeding with relatives can have severe fitness consequences, so avoiding these costs is often evolutionarily favored. There are a number of mechanisms that reduce the likelihood of mating with relatives, including avoiding relatives as mates (through sex-biased dispersal and mate choice) and delayed sexual maturity in the presence of relatives. Here, we examine these mechanisms in Neolamprologus pulcher, a group-living cichlid fish that exhibits male-biased dispersal. Despite sex-biased dispersal in this species, mean relatedness between social mates was not different from that expected if pairs had formed randomly, suggesting individuals neither actively avoid nor prefer pairing with relatives. Furthermore, gonadal investment of subordinates living in social groups was not correlated with their relatedness to the opposite-sex dominant breeder in the group, suggesting that sexual maturation does not depend on the presence or absence of a relative. Highly related social pairs showed higher rates of within-pair aggression and lower rates of nonaggressive social affiliation than less-related social pairs. Breeder investment and indicators of female breeder and group quality were not correlated with relatedness values between social mates. However, scraping rates (a potential quality indicator) were lower in males paired with more closely related females. We consider whether the apparent lack of inbreeding avoidance reflects an evolutionary history of limited breeding opportunities in N. pulcher or a facultative strategy of more-fit individuals and discuss the behavioral results in light of the suggested nonassortative mating with regard to relatedness. Copyright 2008, Oxford University Press.
[show abstract][hide abstract] 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.
Biology of Reproduction 09/2007; 77(2):280-4. · 4.03 Impact Factor
[show abstract][hide abstract] ABSTRACT: 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.
[show abstract][hide abstract] ABSTRACT: 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.