Evolution of colour patterns in East African cichlid fish

African cichlid fishes have undergone outbursts of explosive speciation in several lakes, accompanied by rapid radiations in coloration and ecology. Little is known about the evolutionary forces that triggered these events but a hypothesis, published by Wallace Dominey in 1984, has figured prominently. It states that the evolution of colour patterns is driven by sexual selection and that these colour patterns are important in interspecific mate choice, a combination which holds the potential for rapid speciation. Here we present phylogenetic analyses that describe major events in colour evolution and test predictions yielded by Dominey's hypothesis. We assembled information on stripe patterns and the presence or absence of nuptial coloration from more than 700 cichlid species representing more than 90 taxa for which molecular phylogenetic hypotheses were available. We show that sexual selection is most likely the selection force that made male nuptial coloration arise and evolve quickly. In contrast, stripe patterns, though phylogenetically not conserved either, are constrained ecologically. The evolution of vertical bar patterns is associated with structurally complex habitats, such as rocky substrates or vegetation. The evolution of a horizontal stripe is associated with a piscivorous feeding mode. Horizontal stripes are also associated with shoaling behaviour. Strength of sexual selection, measured in terms of the mating system (weak in monogamous, strong in promiscuous species), has no detectable effects on stripe pattern evolution. In promiscuous species the frequency of difference between sister species in nuptial hue is higher than in pair bonding and harem forming species, but the frequency of difference in stripe pattern is lower. We argue that differences between the two components of coloration in their exposure to natural selection explain their very different evolutionary behaviour. Finally, we suggest that habitat-mediated selection upon chromomotor flexibility, a special form of phenotypic plasticity found in the river-dwelling outgroups of the lake-dwelling cichlids, explains the rapid and recurrent ecology-associated radiation of stripe patterns in lake environments, a new hypothesis that yields experimentally testable predictions.     

Temporal and sex-specific patterns of breeding territory defense in a color-polymorphic cichlid fish

In biparental species, the costs and benefits of parental investment can vary between the sexes and shift over time. However, such sex-specific and temporal changes in territory defense are not well understood. Here, we experimentally investigated parental investment in breeding territory defense in a feral population of the color-polymorphic, biparental cichlid fish, the red devil (Amphilophus labiatus). We presented either gold- or dark-colored conspecific intruder models (i.e., dummy models) to A. labiatus pairs at three key stages during the breeding cycle (i.e., after pair formation, after eggs have been laid, and when fry were free-swimming). We found that males were more aggressive when the pair first formed, whereas females significantly increased their territory defense with time, and were most aggressive when fry were free-swimming. These results show that parental roles in territory defense can markedly shift over key stages of the breeding cycle. Our results demonstrate that parental behaviors may not only vary between the sexes, but can also shift dramatically over the course of the brood cycle.     

Probing aggressive motivation in a cichlid fish

The duration of startles provides an inverse measure of motivation to resume the previous activity. Here, we use a novel method in which one convict cichlid fish (Amatitlania nigrofasciata) of a competing pair was startled independently of the opponent. Fish were given various opponents and the mean startle duration determined. This mean was negatively correlated with the mean use of highly escalated ‘frontal activities’ such as biting and frontal display, but not the less escalated lateral displays or tail beating. Thus the startle duration was a reliable surrogate measure of the most escalated components of aggressive interactions. That is, it provided a motivational probe for aggressiveness of individual fish. Fight motivation is often determined in terms of fight duration or physiological costs for losers, who reveal the costs they are prepared to pay. We discuss various potential advantages of the motivational probe over previous measures, particularly with respect to winners and losers and different times during the interactions.     

Depth equilibration of a shallow-water cichlid fish

The cichlid Melanochromis exasperatus has a natural distribution which is restricted to a single island in Lake Malawi, Africa. Diving observations indicated that it does not occur below 4.5 m depth. Measurements of depth equilibration in a pressure tank showed that males can equilibrate to a depth of 25 m and females to 18 m. Mean maximum sustained rate of depth equilibration was 2 m day⁻¹. M. exasperatus survived a pressure decrease of 40% every 12 h from the maximum equilibration depth to the surface. The fish swim actively during the day but rest on the bottom at night when they are equilibrated to a depth 1 m deeper than ambient. Reduced activity at night is reflected in a drop in oxygen consumption to nearly half of the daytime active value.     

A test of time-place learning in a cichlid fish

This paper presents a test of time-place learning in fish. Convict cichlids, Cichlasoma nigrofasciatum, were offered food several times a day for 10–30 consecutive days. A signal was given 1 min before each food presentation. If the food was always delivered in the same corner of the aquarium, the fish spent 66% of their time in that corner after the signal was given. But if the food was given in different corners throughout the day, each corner being associated with a specific daily time, the fish failed to show preference for the target corner, even after 30 days. Instead they learned which corners yielded food at any time of the day and visited these corners successively after the feeding signal was given. Failure to associate time and place may have been caused by a low cost of travel between corners, a limited number of rewards each day, and / or interference from learning the signal-food association.     

GnRH-systems in the forebrain of cichlid fish.

The neuronal systems that contain gonadotropin-releasing hormone (GnRH) were quantitatively examined in the forebrain of two cichlid species (Oreochromis niloticus Lin. and Tilapia maria Boulenger) using tracing methods and immunostaining. In both species the nucleus olfacto-retinalis and a population of neurons in the basal preoptic region contained GnRH. The nucleus olfacto-retinalis was divided into several neuronal subpopulations which differed with respect to cytology, projection pattern, and peptide content. GnRH cell number increased with body size, the rates being different for the different subpopulations. A sexual dimorphism was found in the basal preoptic region of Tilapia; males had significantly fewer GnRH-containing cells than females. Selective staining of the basal preoptic region demonstrated that this cell group is the main source of GnRH-innervation of the pituitary gland and indicate that the molecular forms of GnRH expressed in the two cell populations studied may be different.     

Parental response to brood size in a cichlid fish

This paper reports on an experiment designed to investigate whether guarding females of the cichlid Aequidens coeruleopunctatus adjust their parental behaviour in response to changes in brood size. It was found that females were easier to scare away from their broods when threatened, and stayed away for longer, after some of their fry had been removed, and that the reverse occurred when broods were experimentally augmented with foreign fry. Brood size manipulations change the expected benefits of future investment. These results therefore indicate that parental care strategies in A. coeruleopunctatus reflect future prospects for reproductive success rather than past investment.     

Sexual dimorphism in a trophically polymorphic cichlid fish?

Sexual dimorphism in ecologically relevant traits is ubiquitous in animals. However, other types of intraspecific phenotypic divergence, such as trophic polymorphism, are less common. Because linkage to sex should often lead to balancing selection, understanding the association between sex and phenotypic divergence could help explain why particular species show high morphological variability. To determine if sexual dimorphism could be helping to maintain ecomorphological variation in a classic case of intraspecific trophic polymorphism, we examined the association between sex and morphological divergence in the cichlid Herichthys minckleyi. Although H. minckleyi with enlarged molariform teeth on their pharyngeal jaws have been reported to more commonly be male, we did not find an association between sex and pharyngeal morphotype. Sex was associated with divergence in body size (as measured through standard length). But, sex was not associated with any of the other trophic traits examined. However, pharyngeal morphotype did show an association with gut length, gape, and tooth number. Sexual dimorphism is not playing a central role in enhancing trophic diversity within H. minckleyi. J. Morphol. 276:1448–1454, 2015. © 2015 Wiley Periodicals, Inc.     

Microsatellite support for active inbreeding in a cichlid fish

In wild animal populations, the degree of inbreeding differs between species and within species between populations. Because mating with kin often results in inbreeding depression, observed inbreeding is usually regarded to be caused by limited outbreeding opportunities due to demographic factors like small population size or population substructuring. However, theory predicts inclusive benefits from mating with kin, and thus part of the observed variation in inbreeding might be due to active inbreeding preferences. Although some recent studies indeed report kin mating preferences, the evidence is still highly ambiguous. Here, we investigate inbreeding in a natural population of the West African cichlid fish Pelvicachromis taeniatus which showed clear kin mating preferences in standardized laboratory experiments but no inbreeding depression. The presented microsatellite analysis reveals that the natural population has, in comparison to two reference populations, a reduced allelic diversity (A = 3) resulting in a low heterozygosity (H_o = 0.167) pointing to a highly inbred population. Furthermore, we found a significant heterozygote deficit not only at population (F_is = 0.116) but also at subpopulation level (F_is = 0.081) suggesting that inbreeding is not only a by-product of population substructuring but possibly a consequence of behavioral kin preferences.     

Social familiarity modulates personality trait in a cichlid fish

Personality traits, such as exploration–avoidance, are expected to be adaptive in a given context (e.g. low-risk environment) but to be maladaptive in others (e.g. high-risk environment). Therefore, it is expected that personality traits are flexible and respond to environmental fluctuations, given that consistency across different contexts is maintained, so that the relative individual responses in relation to others remains the same (i.e. although the magnitude of the response varies the differences between high and low responders are kept). Here, we tested the response of male cichlid fish (Oreochromis mossambicus) to a novel object (NO) in three different social contexts: (i) social isolation, (ii) in the presence of an unfamiliar conspecific, and (iii) in the presence of a familiar conspecific. Males in the familiar treatment exhibited more exploratory behaviour and less neophobia than males in either the unfamiliar or the social isolation treatments. However, there were no overall correlations in individual behaviour across the three treatments, suggesting a lack of consistency in exploration–avoidance as measured by the NO test in this species. Moreover, there were no differences in cortisol responsiveness to an acute stressor between the three treatments. Together, these results illustrate how behavioural traits usually taken as measures of personality may exhibit significant flexibility and lack the expected consistency across different social contexts.     

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.     

Evolution of a cichlid fish in a Lake Malawi satellite lake

Allopatric divergence in peripheral habitats may lead to rapid evolution of populations with novel phenotypes. In this study we provide the first evidence that isolation in peripheral habitats may have played a critical role in generation of Lake Malawi's cichlid fish diversity. We show that Lake Chilingali, a satellite lake 11.5 km from the shore of Lake Malawi, contains a breeding population of Rhamphochromis, a predatory genus previously thought to be restricted to Lake Malawi and permanently connected water bodies. The Lake Chilingali population is the smallest known Rhamphochromis, has a unique male nuptial colour pattern and has significant differentiation in mitochondrial DNA from Lake Malawi species. In laboratory mate choice trials with a candidate sister population from Lake Malawi, females showed a strong tendency to mate assortatively indicating that they are incipient biological species. These data support the hypothesis that isolation and reconnection of peripheral habitats due to lake level changes have contributed to the generation of cichlid diversity within African lakes. Such cycles of habitat isolation and reconnection may also have been important in evolutionary diversification of numerous other abundant and wide-ranging aquatic organisms, such as marine fishes and invertebrates.     

Colour biases in territorial aggression in a Neotropical cichlid fish

Discrete colour morphs have provided important insights into the evolution of phenotypic diversity. One of the mechanisms that can help to explain coexistence of ecologically similar colour morphs and incipient species is (colour) biased aggression, which has the potential to promote continued existence of the morphs in a frequency-dependent manner. I addressed colour biases in territorial aggression in a field-based study on a Neotropical cichlid fish species, Amphilophus sagittae, which has two ecologically indistinguishable colour morphs that mate assortatively. I found that A. sagittae, in particular females, were more aggressive towards models of their own colour than those mimicking colours of the other morph. Such a behavioural pattern should result in a selection regime that benefits the rarer morph, and hence could help explain how novel, rare phenotypes may avoid competitive exclusion.     

Complete mitochondrial DNA replacement in a Lake Tanganyika cichlid fish

We used nuclear and mitochondrial DNA (mtDNA) sequences from specimens collected throughout Lake Tanganyika to clarify the evolutionary relationship between Lamprologus callipterus and Neolamprologus fasciatus . The nuclear data support the reciprocal monophyly of these two shell-breeding lamprologine cichlids. However, mtDNA sequences show that (i) L. callipterus includes two divergent and geographically disjunct (North–South) mtDNA lineages; and that (ii) N. fasciatus individuals cluster in a lineage sister group to the northern lineage of L. callipterus . The two mtDNA lineages of L. callipterus diverged c . 684 kya to 1.2 Ma, coinciding with a major water level low stand in Lake Tanganyika, which divided the lake into isolated sub-lakes. This suggests that the two mtDNA lineages originated as the result of the separation of L. callipterus populations in different sub-basins. The incongruent phylogenetic position of N. fasciatus can best be explained by an ancient unidirectional introgression from L. callipterus into N. fasciatus. Remarkably, our data indicate that this event resulted in the complete mtDNA replacement in N. fasciatus . Our data suggest that hybridization occurred soon after the divergence of the two L. callipterus mtDNA lineages, probably still during the water level low stand, and that subsequently the invading mtDNA lineage spread throughout the lake.     

Active inbreeding in a cichlid fish and its adaptive significance

Levels of inbreeding are highly variable in natural populations. Inbreeding can be due to random factors (like population size), limited dispersal, or active mate choice for relatives. Because of inbreeding depression, mating with kin is often avoided, although sometimes intermediately related individuals are preferred (optimal outbreeding). However, theory predicts that the advantages of mating with close kin can override the effects of inbreeding depression, but in the animal kingdom, empirical evidence for this is scarce. Here we show that both sexes of Pelvicachromis taeniatus, an African cichlid with biparental brood care, prefer mating with unfamiliar close kin over nonkin, suggesting inclusive fitness advantages for inbreeding individuals. Biparental care requires synchronous behavior among parents. Since parental care is costly, there is a conflict between parents over care, which can reduce offspring fitness. Relatedness is expected to enhance cooperation among individuals. The comparison of the parental behavior of in- and outbreeding pairs showed that related parents were more cooperative and invested more than unrelated parents. Since we found no evidence for inbreeding depression, our results suggest that in P. taeniatus, inbreeding is an advantageous strategy.