Monogamous Cichlid Fish Research Articles

Seasonal variation in cuckoldry rates in the socially monogamous cichlid fish Variabilichromis moorii

Mating patterns in animal populations can respond to environmental conditions and consequently vary across time. To examine this variation in nature, studies must include temporal replicates from the same population. Here, we report temporal variation in genetic parentage in the socially monogamous cichlid Variabilichromis moorii from Lake Tanganyika, using samples of broods and their brood-tending parents that were collected across five field trips from the same study population. The sampled broods were either spawned during the dry season (three field trips) or during the rainy season (two trips). In all seasons, we detected substantial rates of extra-pair paternity, which were ascribed to cuckoldry by bachelor males. Paternity shares of brood-tending males were consistently higher, and the numbers of sires per brood were consistently lower, in broods that were spawned in the dry seasons compared to broods from the rainy seasons. In contrast, the strength of size-assortative pairing in our V. moorii population did not vary temporally. Seasonal fluctuations in environmental conditions, such as water turbidity, are proposed as a mechanism behind variable cuckolder pressure. Our data demonstrate the utility of long-term monitoring to improve our understanding of animal mating patterns.

Intrasexual selection: Kin competition increases male-male territorial aggression in a monogamous cichlid fish.

During intrasexual competition, individuals of the same sex compete for access to breeding sites and mating partners, often accompanied by aggressive behavior. Kin selection theory predicts different kin‐directed social interactions ranging from cooperation to aggression depending on the context and the resource in question. Kin competition reducing indirect fitness might be avoided by actively expelling relatives from territories and by showing higher aggression against kin. The West‐African cichlid Pelvicachromis taeniatus is a monogamous cave breeder with males occupying and defending breeding sites against rivals. This species is capable of kin recognition and shows kin‐preference during juvenile shoaling and mate choice. However, subadults of P. taeniatus seem to avoid the proximity of same‐sex kin. In the present study, we examined territorial aggression of territory holders against intruding related and unrelated males as well as intruder's behavior. We observed higher aggression among related competitors suggesting that related males are less tolerated as neighbors. Avoidance of intrasexual competition with relatives might increase indirect fitness of males in monogamous species.

Dynamics of ovarian maturation throughout the reproductive cycle of the Neotropical cichlid fishCichlasomadimerus(Teleostei, Cichliformes)

In this study, we analyzed gene expression profiles, plasma steroids concentrations, and gonadal morphology throughout the reproductive cycle of female Cichlasoma dimerus (Heckel, 1840), a monogamous cichlid fish exhibiting social hierarchies. Fish were analyzed at six phases encompassing their annual cycle, namely resting (during the nonreproductive period), prespawning, 30 h post spawning, 4 days post spawning, 10 days post spawning, and subordinate (during the reproductive period). The histological and histomorphometric analysis showed that C. dimerus exhibits asynchronous ovarian development. Similar to resting females, subordinate females showed low gonadosomatic index, reduced expression levels of vitellogenin (vtgAb), zona pellucida (zpB), gonadal aromatase (cyp19a1A), and low concentrations of plasma sex steroids, thus indicating that social intimidation by dominant conspecifics elicited reproductive arrest. In reproductively active females, a direct positive correlation between plasma estradiol, vtgAb expression, percentage of late vitellogenic oocytes, and gonadosomatic index was observed. These parameters were maximal at the prespawning phase, decreased at 30 h post spawning and 4 days post spawning, and then reached a peak at 10 days post spawning. Our results indicate that female C. dimerus become spawning capable after 10 days post spawning, coincidently with the shortest time interval between successive spawns recorded in captivity.

Genetic evidence for prevalence of alloparental care in a socially monogamous biparental cichlid fish, Perissodus microlepis, from Lake Tanganyika supports the "selfish shepherd effect" hypothesis.

Alloparental care – care for unrelated young – is rare in animals, and its ecological or evolutionary advantages or, alternative maladaptive nature, remain unclear. We investigate alloparental care in the socially monogamous cichlid fish Perissodus microlepis from Lake Tanganyika that exhibits bi‐parental care. In a genetic parentage analysis, we discovered a surprisingly high percentage of alloparental care represented by brood mixing, extra‐pair paternity and extra‐pair maternity in all broods that we investigated. The percentage of nondescendant juveniles of other parents, i.e., brood mixing, ranged from 5% to 57% (mean = 28%). The distribution of genetic parentage also suggests that this socially monogamous species has, in fact, polygamous mating system. The prevalence of genetically mixed broods can be best explained by two, not mutually exclusive hypotheses on farming‐out and fostering behaviors. In the majority of broods, the sizes of the parents’ own (descendant) offspring were significantly larger than those of the adopted (nondescendant) juveniles, supporting the ‘selfish shepherd effect’ hypothesis, i.e., that foster parents preferentially accept unrelated “smaller or not larger” young since this would tend to lower the predation risks for their own larger offspring. There was also a tendency for larger parents particularly mothers, more so than smaller parents, to care predominantly for their own offspring. Larger parents might be better at defending against cuckoldry and having foreign young dumped into their broods through farming‐out behavior. This result might argue for maladaptive effects of allopatric care for the foster parents that only larger and possibly more experienced pairs can guard against. It needs to be determined why, apparently, the ability to recognize one's own young has not evolved in this species.

Benefits of kin shoaling in a cichlid fish: familiar and related juveniles show better growth

Group living is widespread in animals. In nature, groups usually not only differ in phenotypic characteristics but also in the social relationships among group members. Theory predicts that individuals adjusting their shoaling decisions—to join certain groups or not—based on social criteria, such as familiarity or genetic relatedness, can increase their fitness. Although numerous studies report grouping preferences based on social criteria, the benefits actually emerging from such behavioral preferences are less well studied. Here, we examine both shoaling preferences and their consequences in juveniles of Pelvicachromis taeniatus, a monogamous cichlid fish from Western Africa with biparental brood care. After juvenile P. taeniatus have left their parents, they form loose shoals. Then, juveniles may have the option either to stay in their sibling group or to join a novel shoal. Therefore, in a first experiment, we tested whether juveniles prefer to shoal with their familiar sibling group or a group consisting of unfamiliar unrelated individuals. Second, we examined whether the shoaling decision translates into fitness benefits. We used body size as proxy for fitness and compared the growth in groups consisting exclusively of familiar full-siblings with growth in groups consisting of members of different relatedness and familiarity. Juvenile P. taeniatus preferred shoaling with kin over shoaling with non-kin. Growth was significantly higher in kin-only groups than in mixed groups indicating that grouping with familiar kin yields fitness benefits in juvenile P. taeniatus. Our results suggest that individual shoaling decisions based on social criteria can be adaptive.

Female breeding experience affects parental care strategies of both parents in a monogamous cichlid fish

Previous breeding experience affects parental care, yet in biparental species it is unclear how the inexperience of only one parent influences parental dynamics and division of labour. Using the biparental convict cichlid, Amatitlania siquia, I assessed how female breeding experience affects male and female parental behaviour. Females that either had bred (experienced) or were virgins (inexperienced) were paired with experienced males. Inexperienced females were less likely to form pairs and took longer to spawn. Female experience also affected parental division of labour between direct offspring care and territory defence. Female behaviour was compared in the presence and absence of their male partners. When males were present, all females divided their time similarly: more time was spent in direct care. When male mates were removed, experienced females divided their time equally between territory defence and direct care, while inexperienced females continued to spend more time in direct care. Males paired to inexperienced females divided their time equally between territory defence and direct care, while males paired to experienced females spent more time in defence. Males were also more aggressive towards experienced females. Overall, experienced females tended to adopt the male-typical role of defence, which probably caused the increased intrapair conflict in these pairs. This aggression helps explain why both experienced and inexperienced females showed similar role choices in the presence of their male partner and supports previous claims that male aggression helps maintain the division of labour in this species. Female inexperience potentially presents a trade-off for males: males paired to inexperienced females engaged in less intrapair conflict, but showed less division of labour between parental roles than is typical and were less likely to pair and spawn. The effect of female experience on division of labour, parental dynamics and pair bonding success probably influences other factors such as mate choice, effectiveness of parental care and overall fitness.

“Armpit effect” in an African cichlid fish: self-referent kin recognition in mating decisions of male Pelvicachromis taeniatus

Kin discrimination in nepotistic as well as in sexual contexts is widespread in animals including humans. However, the underlying mechanisms of kin discrimination are assumed to vary between species and—within species—between contexts. During solitary life stages, kin recognition based on social learning is assumed to be less reliable because kin templates that are not continuously updated may get lost. Therefore, self-referent phenotype matching (“armpit effect”), i.e., the comparison of unknown phenotypes with own characteristics, should be particularly relevant when no social cues are available. However, experimental evidence for this mechanism is scarce. Here, we examine self-referent kin recognition in a mate-choice context in adult male Pelvicachromis taeniatus, a socially monogamous cichlid fish from West Africa with biparental brood care and pronounced kin-mating preferences. Juvenile P. taeniatus live in groups, whereas adult males compete for access to breeding sites which they aggressively defend against rivals. Using computer-animated females as standardized visual stimuli in combination with olfactory cues of related and unrelated females, we show that adult males reared isolated from kin since egg stage were able to discriminate sisters from unrelated females. As males could have learned kin cues only from themselves, our study provides evidence for self-referent kin recognition and indicates that the observed inbreeding preferences are mediated by self-derived olfactory cues. Male preferences for sisters were correlated with male body size. We discuss the implications of quality-related mate choice for the evolution of kin-mating preferences.

Nonrandom brood mixing suggests adoption in a colonial cichlid

Parental care of unrelated offspring is widespread but not well understood. We used 11 polymorphic microsatellite loci to investigate the relatedness of fry and parentally caring adults in a 118-nest colony of the socially and genetically monogamous cichlid fish Neolamprologus caudopunctatus in Lake Tanganyika. There was a high proportion of brood mixing, with 59% of 32 broods containing fry unrelated to both parents, and 18% of all 291 sampled fry being unrelated to the breeding pair. There was no evidence of kin selection for adoption because the genetic and foster parents were not more related than expected by chance. Parentage was assigned to 12 adopted fry from 10 broods. Distances traversed by fry varied markedly, from less than one to over 40 meters. The larger distances suggest that at least some brood mixing was instigated by parents transporting portions of their broods in their mouths, as occurs in some cichlids. Further evidence of non-random brood mixing was that foreign fry did not differ in size from their foster siblings within broods, even though they were significantly larger than fry produced by the tending pairs within the colony. These findings suggest that at least some foreign fry had dispersed non-randomly and were adopted by their foster parents. Enlarged broods are known to provide reduced per capita predation, making it potentially adaptive for breeders to adopt unrelated offspring.

Kin recognition by phenotype matching is family- rather than self-referential in juvenile cichlid fish

The ability to differentiate between kin and nonkin is of importance in nepotistic as well as in mate choice contexts. Phenotype matching is a significant kin recognition mechanism, which is widespread in animals. However, the underlying proximate mechanisms are still poorly understood. Phenotype matching can be based on either self-reference or familial imprinting. We investigated phenotype matching in juvenile Pelvicachromis taeniatus based on chemical cues. Pelvicachromis taeniatus is a socially monogamous cichlid fish with biparental brood care. Previous studies indicate that the adults use phenotype matching to recognize kin. Juvenile fish were reared under three different conditions to manipulate recognition templates: (1) reared with kin, (2) reared in isolation or (3) reared with foster siblings. Pelvicachromis pulcher families served as foster families. In the experiments, test fish had to choose between olfactory cues obtained from two stimulus shoals differing in relatedness to the test fish. Test fish reared with kin discriminated unfamiliar kin from unfamiliar nonkin indicating that juvenile P. taeniatus also use phenotype matching to recognize kin. Focal fish reared in isolation or with foster siblings did not significantly discriminate unfamiliar kin from unfamiliar nonkin suggesting that juveniles did not imprint on their own phenotypic traits. However, individuals reared with foster siblings preferred unfamiliar olfactory stimuli of the foster species over those of their own indicating they used rearing partners as reference. Thus, phenotype matching is probably based on familial imprinting rather than self-reference in juvenile P. taeniatus.

Isotocin regulates paternal care in a monogamous cichlid fish

While the survival value of paternal care is well understood, little is known about its physiological basis. Here we investigate the neuroendocrine contributions to paternal care in the monogamous cichlid, Amatitlania nigrofasciata. We first explored the dynamic range of paternal care in three experimental groups: biparental males (control fathers housed with their mate), single fathers (mate removed), or lone males (mate and offspring removed). We found that control males gradually increase paternal care over time, whereas single fathers increased care immediately after mate removal. Males with offspring present had lower levels of circulating 11-ketotestosterone (11-KT) yet still maintained aggressive displays toward brood predators. To determine what brain regions may contribute to paternal care, we quantified induction of the immediate early gene c-Fos, and found that single fathers have more c-Fos induction in the forebrain area Vv (putative lateral septum homologue), but not in the central pallium (area Dc). While overall preoptic area c-Fos induction was similar between groups, we found that parvocellular preoptic isotocin (IST) neurons in single fathers showed increased c-Fos induction, suggesting IST may facilitate the increase of paternal care after mate removal. To functionally test the role of IST in regulating paternal care, we treated biparental males with an IST receptor antagonist, which blocked paternal care. Our results indicate that isotocin plays a significant role in promoting paternal care, and more broadly suggest that the convergent evolution of paternal care across vertebrates may have recruited similar neuroendocrine mechanisms.

Rapid assessment of female preference for male size predicts subsequent choice of spawning partner in a socially monogamous cichlid fish

Although size-assortative mating in convict cichlids, Amatitliana nigrofasciata, is supposed to result from mutual mating preference for larger individuals, female choice in relation to male size remains ambiguous. We revisited the evidence for directional preference for larger males in female convict cichlids using a classical two-way choice apparatus in which each female could decide to spend time in front of a small male or a large one. We found evidence for female preference for large males, as assessed from association preference during a 4-hour period following encounter. Furthermore, females decided to spawn in front of the initially preferred male more often than expected by chance. Our results thus confirm the existence of a directional preference for large males in female convict cichlids, and indicate that association preference measured over a short period of time can provide a quick and reliable proxy for reproductive preference in this species.

Neuropeptide regulation of social behavior in a monogamous cichlid fish

The nonapeptides arginine vasopressin (AVP; including its non-mammalian homolog arginine vasotocin, AVT) and oxytocin (OT; including its non-mammalian homologs mesotocin, MT, and isotocin, IT) regulate social behavior, including aggression and reproduction, via receptors conserved across vertebrates. In monogamous prairie voles, the vasopressin and oxytocin pathways are crucially important for pair-bond formation, specifically by influencing affiliative behavior toward the mate and aggression toward non-mates. Monogamous social systems are found in diverse taxa. We hypothesized that the AVT/IT pathways are associated with mating behavior in monogamous teleost fishes. We used the monogamous convict cichlid, Amatitlania nigrofasciata, to test this idea. In the first experiment, we treated males with a general nonapeptide receptor antagonist during pair-bond formation. Control males were treated with vehicle. On the first day of treatment we observed a significant reduction in both affiliative behavior toward the potential mate and aggression toward neighbors. However, the antagonist did not prevent the pair-bond from forming and the behavioral effects disappeared on subsequent treatment days. In the second experiment, we administered on three consecutive days the AVP/OT receptor antagonist to males that were in an established pair-bond. In established pairs, male affiliation towards the mate and aggressive behavior towards territorial neighbors were not affected by the antagonist. Our results indicate that the basic social behaviors typically mediated by the AVP/OT pathways may provide the building blocks necessary for monogamous mating behavior.

You can't always get what you want: size assortative mating by mutual mate choice as a resolution of sexual conflict

BackgroundAssortative mating patterns for mate quality traits like body size are often observed in nature. However, the underlying mechanisms that cause assortative mating patterns are less well known. Sexual selection is one important explanation for assortment, suggesting that i) one (usually the female) or both sexes could show preferences for mates of similar size or ii) mutual mate choice could resolve sexual conflict over quality traits into assortment. We tested these hypotheses experimentally in the socially monogamous cichlid fish Pelvicachromis taeniatus, in which mate choice is mutual.ResultsIn mate choice experiments, both sexes preferred large mates irrespective of own body size suggesting mating preferences are not size-assortative. Especially males were highly selective for large females, probably because female body size signals direct fitness benefits. However, when potential mates were able to interact and assess each other mutually they showed size-assortative mating patterns, i.e. the likelihood to mate was higher in pairs with low size differences between mates.ConclusionDue to variation in body size, general preferences for large mating partners result in a sexual conflict: small, lower quality individuals who prefer themselves large partners are unacceptable for larger individuals. Relative size mismatches between mates translate into a lower likelihood to mate, suggesting that the threshold to accept mates depends on own body size. These results suggest that the underlying mechanism of assortment in P. taeniatus is mutual mate choice resolving the sexual conflict over mates, rather than preference for mates of similar size.

High frequency of multiple paternity in broods of a socially monogamous cichlid fish with biparental nest defence

In several animal taxa, genetic analyses have demonstrated that social monogamy and biparental brood care do not preclude polygamous reproduction. Few studies have been conducted in fish, but in fish species without alternative reproductive phenotypes, social monogamy was largely congruent with genetic parentage. In contrast to these findings, we report an exceptionally high level of multiple paternity in a socially monogamous cichlid fish with biparental nest defence (Variabilichromis moorii), inferred from microsatellite and mitochondrial data of 10 broods. Whereas all offspring in a nest shared a common mother, each brood was sired by 2 to > 10 males. None of the inferred sires was assigned a large proportion of the brood. Paternity was estimated as the minimum number of sires required to explain multilocus offspring genotypes, and as the maximum-likelihood number of sires given population allele frequencies. Analysis of simulated brood genotypes suggested that, although these two methods tend to under- and overestimate, respectively, the true number of sires, primary sires with many offspring in a brood would have been detected. Hence, the genetic data indicate that the nest tending males suffer substantial cuckoldry and provide alloparental care for a large number of unrelated fry. We have no data on the social status of the cuckolding males, but due to synchronous spawning of pairs and commitment to brood care of paired males, it is possible that most of the parasitic spawners are solitary males.

Female convict cichlids (Archocentrus nigrofasciatus) prefer to consort with same-sized males

In the monogamous cichlid fish Archocentrus nigrofasciatus, the convict cichlid, males have been shown to prefer large females, even females larger than themselves. However, convict cichlids normally form male-larger assortative pairs, with males approximately 30% larger than their mates. We tested female preference for male body size by examining their allocation of visiting behavior (consorting) in a laboratory three way choice experiment. Females consorted most with the smallest of three available males, and the preferred males were usually closely matched in size to the choosing female. The most discriminating females exhibited greater concordance in preference than the least discriminating females. Female consorting behavior in the lab differs dramatically from that of males and female mate preferences may be similarly different from those of males.

Sexual Differences in Offspring Defense in a Monogamous Cichlid Fish

AbstractSolitary male and female Texas cichlids, Cichlasoma cyanoguttatum employ different tactics when defending their offspring. Males emphasize the lateral display against an intruder and make infrequent return visits to the young while the intruder is present. The female is more likely to attack, attempting to bite the intruder and also making frequent return visits to the offspring. These differences disappear with increasing age of the offspring as the male becomes more like the female with more violent attacks. Both defense systems appear effective, in the short term, against intruders.

Mate size and breeding success in a monogamous cichlid fish

The patterns of mate size and parental care of a monogamous cichlid fish,Cichlasoma maculicauda, were studied in Gatun Lake, Panama. Males defend territories which serve as courtship and nest sites. Within a population most mates in pairs are of equal size rank. In each pair the male is larger than the female, probably because most mature males are larger than most mature females. Clutch size increases with female body size. Male size affects breeding success in two ways. First, larger males provide nest sites less susceptible to destructive wave action. Second, young of larger males grow faster than young of smaller males. Large males defeat small males in contests for position in feeding areas, and this may provide their young with better feeding conditions. In the laboratory young growth rates increase with food abundance, and at high levels of food surpass those observed in nature. Fast growth of young reduces their vulnerability to predators and should allow parents to breed more often. Young survival rates improve with the size of the parents, so that larger fish raise more offspring at each breeding attempt. These observations suggest why preference for large mates should occur.