Feeding schools among Lake Malawi cichlid fishes

Synopsis Seven species of rock-frequenting cichlids, endemic to Lake Malawi, formed feeding-schools. Petrotilapia genalutea was the nuclear species comprising 92% of the school members (n = 2690 individuals from 50 schools). Fifty-eight per cent of all schools encountered consisted only of P. genalutea. School size ranged from 10 to 300 members (x = 81 ± 74 SD, median = 62). Schooling behaviour was facultative. Ninety-seven per cent of the feeding sites used by the schools occurred within the territories of highly aggressive, territorial species. These sites support considerably greater standing crops of algae, the food of the schooling species, than undefended sites. Individuals of schooling species were unable to gain access to the aggresively defended areas unless they joined schools.     

Sibling species complexes in sympatric populations of Petrotilapia Trewavas (Cichlidae, Lake Malawi)

The endemic Lake Malawi cichlid, Petrotilapia tridentiger Trewavas, was found to be a complex of sibling species. The various sympatric species show considerable homogeneity in body form and dentition but are separable on the basis of differences in adult coloration, size at maturity, depth distribution, size and degree of overlap of territories, aggression and courtship. Colour is considered to be important for specific mate recognition in this genus. Examination of wild populations is a valuable, perhaps essential, adjunct to classical taxonomy when dealing with the systematics of sibling species in Lake Malawi.     

Morphometric analysis on ecomorphologically equivalent cichlid species from Lakes Malawi and Tanganyika

Landmark-based geometric morphometric techniques were used to test the hypothesis that Petrochromis spp. from Lake Tanganyika are ecomorphologically equivalent to Petrotilapia spp. from Lake Malawi. Both genera are epilithic algal feeders and inhabit the rocky shores of their respective lakes. We investigated the morphological component of the ecomorphology hypothesis by investigating body shape, using landmark-based morphometric techniques. A MANOVA revealed significant differences among species and an ordination of all species along the first two CV axes showed clear separation of the two genera in the morphospace with Petrochromis fasciolatus as an intermediate. A thin-plate spline analysis revealed that Petrochromis spp. had a deeper, broader anterior body, larger gape, shorter anal fin base and narrower caudal peduncle than Petrotilapia spp. Basically, differences between lakes were found, but there were no similarities or clusters of presumptive ecomorphs. Based on such results, we reject the hypothesis of morphological equivalence between these two genera. However, considering the non-significant difference in body shape revealed between P. fasciolatus , Petrotilapia genalutea and Petrotilapia 'mumbo blue', we conclude that these three species represent morphological equivalence and hence display a best example of convergent evolution.     

Aggression in closely related Malawi cichlids varies inversely with habitat complexity

Within the past 2 million years, the cichlids of Lake Malawi have diversified into well over 500 species resulting in one of the worlds largest lacustrine fish radiations. As a result, many of the habitats within the lake support a high diversity of species. In these highly species rich communities, male cichlids must acquire and defend a territory to successfully reproduce. Within the rock-dwelling cichlids of Lake Malawi (mbuna), this has resulted in the formation of polyspecific leks on the heterogeneous rocky benthos. Aggression is fairly common in these leks and has been tied not only to individual reproduction but to the larger phenomenon of community assembly and the maintenance of biological diversity. In this study, I examined the patterns of aggressive acts of four species within the mbuna genus Maylandia at two locations in the southern Lake Malawi. The number of aggressive acts of two sympatric species was examined at each location. At each site, one species defends territories over bedrock and the other over cobble. The number of aggressive acts across the four species was compared. The influence of habitat type on male aggression was examined and the targets of male aggression were identified to evaluate several hypotheses concerning the evolution of male aggression. The results show that aggression quantitatively varied among species, was largely directed towards heterospecifics, and was strongly influenced by habitat type. The aggressive behavior of one sympatric species pair, Maylandia benetos and Maylandia zebra, was observed under controlled laboratory conditions. Laboratory results support field observations: the bedrock associated species performed more aggressive acts and aggressive acts were directed equally at con- and heterospecifics. The results of this study suggest that habitat complexity plays a larger role in shaping aggressive behavior than other suggested factors such as competition for resources.     

Ecotype differences in aggression,neural activity and behaviorally relevant gene expression in cichlid fish

In Lake Malawi, two ecologically distinct lineages of cichlid fishes (rock‐ vs sand‐dwelling ecotypes, each comprised of over 200 species) evolved within the last million years. The rock‐dwelling species (Mbuna) are aggressively territorial year‐round and males court and spawn with females over rocky substrate. In contrast, males of sand‐dwelling species are not territorial and instead aggregate on seasonal breeding leks in which males construct courtship “bowers” in the sand. However, little is known about how phenotypic variation in aggression is produced by the genome. In this study, we first quantify and compare behavior in seven cichlid species, demonstrating substantial ecotype and species differences in unconditioned mirror‐elicited aggression. Second, we compare neural activity in mirror‐elicited aggression in two representative species, Mchenga conophoros (sand‐dwelling) and Petrotilapia chitimba (rock‐dwelling). Finally, we compare gene expression patterns between these two species, specifically within neurons activated during mirror aggression. We identified a large number of genes showing differential expression in mirror‐elicited aggression, as well as many genes that differ between ecotypes. These genes, which may underly species differences in behavior, include several neuropeptides, genes involved in the synthesis of steroid hormones and neurotransmitter activity. This work lays the foundation for future experiments using this emerging genetic model system to investigate the genomic basis of evolved species differences in both brain and behavior.     

The Social Organization of the Cape Ground Squirrel (Xerus inauris; Rodentia: Sciuridae)

The Cape ground squirrel (Xerus inauris) of southern Africa is a tropical species that does not hibernate. Field observations using scan and all-occurrence sampling revealed that this species was highly social. Female Cape ground squirrels formed social units of related females and their subadult young, as is typical for other ground squirrels. Female social groups were usually composed of 2–3 adult females and 2–3 subadults of either sex. Members of these female social groups shared sleeping burrows and feeding ranges. Female social groups did not cooperatively defend their feeding ranges from adjacent groups in other burrow clusters. Interactions within female social groups were highly amicable, and no dominance hierarchy was evident. Males in this species also lived in groups. These all-male bands of up to 19 individuals lived almost independently from female groups. The entire male band shared one home range, although ephemeral sub-bands were formed daily. The composition and size of these sub-bands changed daily. Interactions among males, which were largely amicable, included allogrooming and sleeping together. Analysis of interactions within the band indicated a stable, linear, dominance hierarchy among males. Dispersal in this species appeared to be male biased as is typical of other ground-dwelling squirrels, with males dispersing at reproductive maturity. Males joining male bands were thus dispersers and were not likely to be closely related. Sociality in the Cape ground squirrel may be summarized as highly social female kin clusters and associated social non-kin bands of males.     

Social Network Analysis of Male Dominance in the Paper Wasp Mischocyttarus mastigophorus (Hymenoptera: Vespidae)

Social aggression is a pervasive feature of insect societies. In eusocial Hymenoptera, aggression among females can affect task performance and competition over direct reproduction (egg laying); in most species males participate in social interactions relatively rarely. Males of the independent-founding paper wasp Mischocyttarus mastigophorus are exceptional: they are aggressive toward female nestmates, leading us to explore the function of this unusual behavior. We applied social network analyses to data on M. mastigophorus social aggression to quantify sex differences in giving and receiving social aggression. The network analyses supported the pattern of biased male aggression toward female nestmates; females are relatively rarely aggressive to males. We then asked whether male aggression toward females was biased by females’ relative ovary development. Males were more aggressive toward females with better-developed ovaries, opposite to patterns of aggression among females. Because food brought to the colonies is often monopolized by dominant females, we suggest that males direct aggression toward socially dominant females with better-developed ovaries to obtain food. The implications of biased male aggression for female task performance and physiology are unknown.

     

Nuclear gene variation and molecular dating of the cichlid species flock of Lake Malawi

The cichlid fishes of Lake Malawi are famously diverse. However, evolutionary studies have been difficult because of their recent and uncertain phylogenetic history. Portions of 12 nuclear loci were sequenced in nine rock-dwelling species (mbuna) and three representatives of pelagic nonmbuna species. In contrast to the pattern of variation at mitochondrial genes, which do provide phylogenetic resolution at the level of mbuna versus nonmbuna, and among some genera, the nuclear loci were virtually devoid of phylogenetic signal. Only a small minority of variable positions were phylogenetically informative, and no phylogenetic branches are supported by more than one site. From the nuclear gene perspective the Malawian radiation appears to be a star phylogeny, as if the founding of the lake was accompanied by a partial bottleneck. The pattern is different from that found in Lake Victoria, in which nuclear loci share large amounts of ancestral variation. In the case of nuclear genes of Lake Malawi, the absence of phylogenetically informative variation suggests a relative absence of ancestral variation. Nuclear genes also differed from the mitochondria in having nearly twice the amount of divergence from Oreochromis (tilapia). An approximate splitting time between mbuna and nonmbuna lineages was estimated as 0.7 Myr. Oreochromis is estimated to have diverged from the cichlids in Lake Malawi and Lake Tanganyika about 18 MYA.     

The effect of territory quality on female preference in Metriaclima zebra

The cichlid fishes of Lake Malawi are an excellent model group with which to study adaptive radiation and speciation; due to the vast number of individual species, large variation in feeding adaptations and behaviours, and relatively recent divergence are found. Males of many cichlid species will obtain and defend lek‐like territories, where they court potential mates in addition to foraging for food. Aspects of territory quality warrant investigation because of the relationship between reproductive success and territory defence success. In this study, we tested whether the presence of a small or large food resource had any effect on the preference of a gravid female for a potential mate. The results of this experiment suggest that the presence of a large food resource increases the attractiveness of a male to a potential mate. This may suggest that the presence of food alone may not be the most important factor, or there may be a threshold amount over which females are attracted. These results indicate that certain aspects of territory quality such as habitat type or proximity to a food resource may play a role in both intersexual and intrasexual selection mechanisms: perhaps even driving and possibly accelerating the speciation of certain lineages of cichlid fishes.     

Signal and preference divergence among populations of the non‐endemic basal Lake Malawi cichlid fish Astatotilapia calliptera (Perciformes: Cichlidae)

In Lake Malawi and Lake Victoria, cichlid fishes have diversified into hundreds of species, many reproductively isolated by mate choice. Territorial males tend to be more aggressive to similar‐coloured males, facilitating coexistence of divergent colour morphs or species. Behavioural mate choice and aggression biases of species and allopatric populations of specialized rocky shore cichlids are influenced by divergent signals such as male colour. Believed to be basal to the Lake Malawi haplochromine radiation, and inhabiting shallow weedy areas of the lake and neighbouring water bodies, Astatotilapia calliptera also shows allopatric variation in colour. Here, it is demonstrated that such signal divergence is associated with tendencies of females to mate with males of their own population and also for males to preferentially attack males of their own population, indicating that preference divergence related to signal divergence in allopatry may have operated throughout the adaptive radiation of the Malawian cichlids. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 180–188.     

Is speciation of demersal fishes in Lake Tanganyika restrained by physical limnological conditions?

Both Lake Malawi and Lake Victoria have many species of offshore demersal cichlids, most of which are stenotopic. In Lake Tanganyika there are fewer, more eurytopic, demersal species. These differences may be the effect of the physical regimes of the lakes. In Lake Victoria there is no permanent anoxic layer. In both the other lakes, water below 250 m depth is permanently anoxic and the seasonal cycle is dominated by upwelling. In Lake Malawi this is mainly derived from intermediate water containing free oxygen. In Lake Tanganyika upwelling involves hypolimnetic water, which may rise to within 80 m of the surface, causing great short-term changes in oxygen concentration over the depth range 50–250 m. This has inhibited the development of deep water species restricted to narrow depth ranges.     

Elevated mtDNA diversity in introduced populations of Cynotilapia afra (Günther 1894) in Lake Malawi National Park is evidence for multiple source populations and hybridization

Genetic variation in many invasive species shows little or no signs of a founder event, suggesting that high genetic diversity may facilitate establishment success. The rocky‐shore, plankton‐feeding cichlid fish Cynotilapia afra is endemic to Lake Malawi, but naturally absent from many suitable sites. In the 1960s, this species was introduced to the southern areas of the lake, presumably as a result of the aquarium fish trade. It has now become established on a number of rocky areas within the Lake Malawi National Park. Here, we analysed DNA sequence variation in the mitochondrial control region of six native and four introduced populations of C. afra, and three populations of the closely‐related and hybridizing Pseudotropheus zebra. In contrast to previous studies of Lake Malawi rock dwelling cichlids, network analyses suggested that native populations of C. afra showed high levels of lineage sorting in mtDNA. Introduced populations showed higher sequence and haplotype diversity than their native counterparts. Our analyses suggested that the elevated gene diversity was largely attributed to the fact that the introduced C. afra populations were derived from several genetically distinct and geographically separate populations, and to a lesser extent because of introgressive hybridization with native P. zebra. The establishment and spread of C. afra may be partly because of its ability to occupy a vacant ecological niche, but it may also have been facilitated by its enhanced genetic diversity.     

Genetic and morphological studies of Nothobranchius (Cyprinodontiformes) from Malawi with description of Nothobranchius wattersi sp. nov.

Molecular and morphological data were used to explore evolutionary differentiation among populations of Nothobranchius in the Lake Malawi–upper Shire River and the Lakes Chilwa–Chiuta drainage systems in Malawi. The aim of the study was to test the hypothesis that Nothobranchius of the Malawi–Shire system constitute a separate evolutionary group from Nothobranchius kirki. Mitochondrial and nuclear sequence data show a strongly supported phylogenetic split into two monophyletic groups separating the Lake Malawi basin fish from N. kirki. Unlike N. kirki, Lake Malawi–Shire fish do not deviate from neutrality and express an excess of rare haplotypes and mutations in terminal branches, characteristic of recently expanded populations. Further, the two groups significantly differ in morphology. Two body characters (dorsal‐fin base length and pre‐pelvic–pre‐anal distance) are significantly different between the two species in both sexes. Several other characters are significantly different in either male or female comparisons with respect to both standard and head lengths, and robust morphological differentiation is detected by multivariate analysis. The two groups are readily distinguished on the basis of male colouration, especially in scale centres and the caudal fin. On the basis of this differentiation at the molecular and morphological levels, in addition to colouration, the Lake Malawi–Shire fish are hereby formally recognized as constituting a new species, Nothobranchius wattersi. This distinction is in agreement with the geomorphologic and recent climatic history in the region.     

Laboratory mating trials indicate incipient speciation by sexual selection among populations of the cichlid fish Pseudotropheus zebra from Lake Malawi

It has been suggested that sexual selection may have played a major role in the rapid evolution of hundreds of species of cichlid fishes in Lake Malawi. We report the results of a laboratory test of assortative mating among Lake Malawi cichlid fishes from five closely related geographical populations differing in male courtship colour. Paternity of clutches was tested using microsatellite DNA typing of offspring. Out of 1955 offspring typed, 1296 (66.3%) were sired by the male from the same population as the female, which is more than three times the rate expected if females do not differentiate among males of the different populations (20%). This result indicates that mate preferences of geographical races are strongly differentiated, consistent with the races representing incipient geographical species diverging under sexual selection exerted by female preferences for different male courtship colours.     

Genetic homogeneity among breeding grounds and nursery areas of an exploited Lake Malawi cichlid fish

1. Nursery areas are commonly recognized as important habitats for the management and conservation of fish stocks. Here we report the use of nursery areas by an exploited offshore cichlid in Lake Malawi, Rhamphochromis longiceps .
2. Like all haplochromine cichlids that have been studied, the species is a maternal mouthbrooder that broods eggs for several weeks following spawning. We found evidence that during this brooding period females migrate from open water to release juveniles in three shallow peripheral waterbodies (Chia Lagoon, Unaka Lagoon, Lake Malombe). However, it was unclear whether there is geographical population structuring within the species, which could indicate stock differences in their use of these nursery habitats, or if the lake contains a genetically panmictic population that employs nursery habitats opportunistically.
3. To investigate spatial and temporal population structuring within the lake we genotyped populations at seven microsatellite DNA loci. Overall, we found no significant spatial structuring among juveniles from the peripheral lagoons or among breeding males within the main lake body. Moreover, we found no evidence of temporal structuring among males on the breeding grounds within Lake Malawi or females entering Chia lagoon. Together, these results suggest that Lake Malawi contains a genetically homogeneous population of R. longiceps .
4. At present we know little of the distribution of juvenile R. longiceps elsewhere in the Lake Malawi basin, but their absence from surveyed rocky and sandy littoral habitats makes it possible that the species is dependent upon a small number of nearshore nursery areas, including these lagoons. As such, conservation of lagoon habitats and monitoring of exploited fish stocks within them may be important for effective preservation of biodiversity within the catchment.     

Factors in habitat partitioning in Pseudotropheus aurora (Pisces: Cichlidae), an introduced species to a species-rich community of Lake Malawi

The territorial behaviour of a small rock-dwelling cichlid, Pseudotropheus aurora , was studied at Thumbi Island West at the southern end of Lake Malawi. P. aurora is one of several species that have been introduced to an already diverse fish community. Many of the endemic and introduced species are highly territorial. The coexistence of an introduced territorial species within a speciesrich community of other territorial species is examined. Territories from which P. aurora individuals were removed were invariably re-occupied by conspecifics. Similarly, when all territories of a certain area were emptied of all territory owners of any existing species, the former P. aurora territories were re-occupied by conspecifics.
The possible roles of site specificity, competitive exclusion and behaviourally transmitted traditions regarding territories are discussed.     

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.     

AN ASSESSMENT OF THE GROWTH RATE OF MPASA,OPSABIDIUM MICROLEPIS (GUNTHER, 1864) (PISCES: CRYPRINIDAE), BY LENGTH FREQUENCY ANALYSIS

SUMMARY

The mpasa, Opsaridium microlepis, is an important commercial species in areas of Lake Malawi near major inflowing rivers during annual spawning migrations. Plots of length frequency data collected over a series of years from mpasa catches in the Bua and North Rukuru Rivers show consistent peaks and these are believed to represent year classes. Growth in length is approximately linear, about 11 cm per year, until about five years of age. Males and females have similar growth rates.

Catch per unit effort is positively related to river level at time of sampling, and to river levels in earlier years, thus high river levels improve recruitment.     

Identification of a novel sex determining chromosome in cichlid fishes that acts as XY or ZW in different lineages

Sex determination systems are highly conserved among most vertebrates with genetic sex determination, but can be variable and evolve rapidly in some. Here, we study sex determination in a clade with exceptionally high sex chromosome turnover rates. We identify the sex determining chromosomes in three interspecific crosses of haplochromine cichlid fishes from Lakes Victoria and Malawi. We find evidence for different sex determiners in each cross. In the Malawi cross and one Victoria cross the same chromosome is sex-linked but while females are the heterogametic sex in the Malawi species, males are the heterogametic sex in the Victoria species. This chromosome has not previously been reported to be sex determining in cichlids, increasing the number of different chromosomes shown to be sex determining in cichlids to 12. All Lake Victoria species of our crosses are less than 15,000 years divergent, and we identified different sex determiners among them. Our study provides further evidence for the diversity and evolutionary flexibility of sex determination in cichlids, factors which might contribute to their rapid adaptive radiations.

     

Ancient hybridization and phenotypic novelty within Lake Malawi's cichlid fish radiation

Does hybridization play a broad innovative role in evolution? Many studies have shown hybrid origins of individual species, particularly in major adaptive radiations, but this may be a consequence, rather than a cause, of the existence of many closely related species. Cases of hybridization in the early stages of major adaptive radiations are comparatively rare. Here, we report phylogenetic evidence for ancient introgression between distinct lineages of the species-rich Lake Malawi haplochromine cichlid fishes. Mitochondrial DNA (mtDNA) sequences indicated surprisingly close relationships between the shallow-water rocky habitat "Mbuna" species and a group of dark-adapted "Deep-Benthic" species specialized for feeding in low-light conditions (dawn/dusk, under overhangs, and deep water). By contrast, analyses of nuclear amplified fragment length polymorphism data demonstrated that these Deep-Benthic cichlids were more closely related to shallow water "Shallow-Benthic" soft-sediment feeders, a group that shares similar head and body morphology. A coalescent-based computer simulation indicated that the mtDNA similarity of rocky habitat Mbuna species and dark-adapted Deep-Benthic species was due to hybridization rather than incomplete lineage sorting. Comparisons of morphology indicated that some Deep-Benthic species possessed novel morphology not present in other Lake Malawi species groups. Thus, these analyses support the hypothesis that ancient hybridization occurred within the Lake Malawi cichlid radiation, that the event occurred before the radiation of a species group adapted to low-light benthic habitats, and that this group went on to dominate the deep-water regions of Lake Malawi. The results of this study contribute to a growing literature consistent with a creative role of hybridization in the evolution of species diversity and adaptive radiations.