Exploring the Evolution of Cichlids in Lake Tanganyika

Abstract

Lake Tanganyika is one of the most diverse, species-rich lakes located in the western section of the Great East African Lakes. It is the largest lake in the Great Rift Valley and second largest in the world. Among its splendor is the diversity of cichlid species. Almost all (98%) of these species are endemic (exclusively native) to the place.

This exhibits a spectacular example of adaptive radiation of fishes evident of evolution from a common ancestor. 17 cichlid tribes thrive along different water levels of the lake. These tribes are groups in the cichlid lineage originating in the lake that evolved into modern day tribes as a result of ecological, morphological and phylogenetical characteristics. Two methods are used in reconstructing the ancestors of each lineage, and possibly the common ancestor: the geometric morphometric approach and the mitochondrial DNA sequence analysis.

Introduction

The Great Lakes of East Africa are among the world’s largest freshwater lakes in terms of surface area, depth, and volume. These landlocked huge bodies of freshwater possess the world’s most diverse freshwater ecosystems (Clabaut 561). The confinement by mountains inhibited disturbances in these ecosystems from the surroundings thus maintaining a degree of endemism of its species. One of its highlights is the presence of unique species of cichlids endemic to the place (Clabaut 561). These fish’s diversity (i.e. large number of species, rapidity of lineage formation) would make it ideal model systems when studying adaptive radiation and explosive speciation (Clabaut 561; Salzburger 1).

Adaptive radiation in Simpson’s definition means “more or less simultaneous divergence of numerous lines from much the same adaptive type into different, also diverging adaptive zones” (qtd. Clabaut 561). The East African cichlids exhibited such diversification process and became so diverse that lineages became harder to trace (Clabaut 561; Koblmüller 4). In the study of its remarkable adaptive radiation, biologists examined not only the fish’s morphological diversity but also tested its phenotype-environment correlation which is vital in the exploration of evolution of the diverse East African cichlids found in Lake Tanganyika (Clabaut 561).

Lake Tanganyika is among the world’s largest freshwater lakes. It is one of the Great Lakes of East Africa. Covering 32,000 square kilometers and with a maximum depth of 1,470 meters, the lake holds 18,900 cubic kilometer of freshwater which makes it Africa’s largest lake in terms of volume and the world’s second largest in both volume and depth.

The estimated age of the lake is between nine to 12 years, the oldest among the Great Lakes (Clabaut 561; Cohen 511; Koblmüller 4). Using a technique called reflection seismic-radiocarbon method (RSRM), scientists were able to come up with age estimates that showed that some segments of the lake are younger as compared to early estimates (Cohen 511).

The lake contains approximately 250 cichlids species (Clabaut 561; Salzburger 2) and some 150 non-cichlid species most of which thrive along the shoreline down to a depth of 600 feet. These species are most diverse in its phylogeny, morphology, ecology and breeding behavior (Clabaut 561; Koblmüller 4; Salzburger 2). This diversity of cichlid fish in the area makes it an important biological resource in the study of adaptive radiation in evolution. A prior tribal grouping of the fish was made by M. Poll which divided the cichlid species into 12 tribes (Clabaut 561; Koblmüller 4). On 2003, Takahashi (Clabaut 561) discovered five additional tribes that were once identified as members of one of the initial tribal groups (Clabaut 561).

However, these were only the result of examination of the cichlids morphological characters (Clabaut 561). Based on molecular markings, several fish tribes were named which are believed to have been seeded millions of years. These tribal groups were Tylochromini, Trematocarini, Bathybatini, Tilapiini, Boulengerochromini, Eretmodini, the ancestor of the Lamprologini, while a C-lineage existed and later evolved parallel to the changes in the environment (Clabaut 561). This C-lineage of the cichlid fish family further split into 8 tribes namely Cyphotilapiini, Limnochromini, Cyprichromini, Perissodini, Orthochromini, Ectodini, and Haplochromini including the Tropheini (Clabaut 561; Koblmüller 4).

In studying the evolution of cichlids in Lake Tanganyika, it is important to identify the existing variations of the species belonging to the lineage. Factors that affect diversity of the Tanganyikan cichlid species were ecological, morphological, and phylogenetical traits can be the ground for the study. In most of the studies conducted in Lake Tanganyika, biologists based their findings on the morphological characteristics (i.e. body shape and size, coloration patterns, feeding preferences) of the cichlids (Clabaut 561). The approach used is called geometric morphometrics. It uses statistically comparable information that is useful in reconstructing the ancestors of each lineage as well as the common ancestor of the variants (Clabaut 561).

Species belonging to the same group exhibits similar morphology exclusive to that particular group (Clabaut 561). In this way also, it is possible to predict some future variations in the morphology of the existing species (Clabaut 561). Another method which is becoming more and more popular in recent years is mitochondrial DNA (mtDNA) analysis (Salzburger 6). The goal of the scientist is to study the phylogenetic algorithms, the phylogeny of East African Cichlids, embedded in the DNA of the species by comparing the mtDNA sequence of each samples (Salzburger 6).

The objective of this research is to determine how the cichlids in Lake Tanganyika evolved into its present biological state (i.e. body shape) by examining the relationships between ecology, morphological diversity and phylogeny among the identified Tanganyikan cichlid tribes.

Examination of the Different Cichlid Tribes

Takahashi identified 17 tribes of cichlid fish, 14 of which are found in Lake Tanganyika (Clabaut 562). All of these tribes are endemic to the place while some studies showed that majority of the cichlids found in the nearby lakes of Malawi and Victoria were members of one tribe that is found in the lake. The cichlid tribes are as follows: Bathybatini, Cyphotilapiini, Cyprichromini, Ectodini, Eretmodini, Haplochromini, Lamprologini, Limnochromini, Orthochromini, Perissodini, Tilapiini, Trematocarini, Tropheini, and Tychromini (Clabaut 565-567).

Bathybatini

Despite the fact that it is one of the ancient lineages seeded before the modern radiation, the fish’s evolution was gradual (Salzburger 12) making it (and Limnochromini) the least morphologically diverse among the tribes (Clabaut 571) found in Lake Tanganyika. Clabaut’s study (565) on the ecological characters of Bathybatini species showed that it inhabits in bathypelagic zones. This suggests that Bathybatini cichlids live in the dark depths of the lake. According to breeding type, this tribe is a mouth-brooder and the mother carries the offspring. Bathybatini species feeds on fish (Clabaut 565).

Cyphotilapiini

Cyphotilapiini species likes to live in rocky environments (Clabaut 565). This tribe is identified by its polygyny (harem) system of mating (Clabaut 565). This fish is also a mouth-brooder fish. It eats fish and other large invertebrates (Clabaut 565).

Cyprichromini

Clabaut’s study (565) of the ecological characters of the tribe were taken from the two species (Cyprichomis leptosoma and Paracyprichomis brieni) of the tribe had some differences in terms of habitat and feeding preferences. The former lives in rocky areas and feeds on pelagic zooplankton and copepads, while the later inhabits the littoral and the pelagic zones and feeds on zooplankton and microbenthos (Clabaut 565). Both species were maternal and mouth-brooders (Clabaut 565).

Ectodini

Ectodini and Laprologini species are the most morphologically diverse East African cichlid tribes (Clabaut 571). Ectodini tribe is composed of approximately 25 to 30 species (Salzburger 2), eight of which were studied to reveal their ecological characters: Ectodus descapsi, Callochromis stappersi, Eniantiopus melanogenys, Ophtalmotilapia nasuta, Cyathopharynx furcifer, Grammatotria lemairii, Cunningtonia longiventralis, and Xenotilapia ochrogenys (Clabaut 565).

Majority of the species were sand dwellers with three (Ophtalmotilapia nasuta, Cyathopharynx furcifer, and Cunningtonia longiventralis) living in intermediate habitat and Xenotilapia ochrogenys in sandy and muddy habitats (Clabaut 565). All species exhibited maternal parenting except the Xenotilapia ochrogenys which are biparental in nature (Clabaut 565). Most species exhibited polygamic mating system with some having harem or polyandry school. Ectodini species were all mouth-brooders. Feeding preferences of the tribe ranges from insects, invertebrates, plants, small snails, filamentous algae, diatoms, copepod, larvae, ostracods, benthos, and Aufwuchs (Clabaut 565).

Eretmodini

Eretmodini tribe likes to inhabit the rocky and surge water environments. Most species are biparental and show monogamic system of mating. Eretmodini tribe is among the ancient tribes that exhibit mouth-brooding. The feeding preferences include filamentous algae, diatoms, Aufwuchs and insects larvae.

Haplochromini

Lake Tanganyika is the ancestral home of all haplochromines lineages found in East African Great Lakes (Salzburger 1). This tribe prefers to live in rivers, rocky environments and some are ubiquitous (Clabaut 565). Parental care is maternal and like most of the ancient tribes, it is a mouth-brooder (Clabaut 565). Some are generalists, ominivores, and molluscs eaters with few vegetarian species (Clabaut 565).

Lamprologini

As stated earlier, Lamprologini and Ectodini tribes are the most morphologically diverse tribes among the East African cichlids (Clabaut 571-566). Among the 14 tribes, it is the most species-rich with at most 100 species. In Clabaut’s (565-566) study of ecological characters, most of the Lamprologini species thrive in rocky habitat with the exception of some intermediate habitat dwellers.

Most was exhibiting maternal parenting, but biparental and cooperative parenting also exists. Some of the species are polygamous but majority of the tribe are monogamous. All of the Lamprologini species are substrate spawners (Clabaut 565-566). They feed on invertebrates, zoobiocover, zooplankton, benthic arthopods, Aufwuchs and algae (Clabaut 565-566).

Limnochromini

Limnochromini species are mud dwellers. In general, they are biparental, monogamous, and mouth-brooders (Clabaut 566). Feeding preference is from invertebrates, snails to small fishes (Clabaut 566).

Orthochromini

Orthochromini species are mouth-brooders (Clabaut 566). They live in the shallow waters of the rivers and eat tiny plankton and algae (Clabaut 566). Parenting is maternal (Clabaut 566).

Perissodini

Perissodini, as mentioned earlier, is one of the tribes that split from the C-lineage. Species that belong to this tribe are known as scale-eaters (Koblmüller 4). They live ubiquitously. Parenting is divided into biparental and maternal (Clabaut 566). Perissodini species are monogamous and are mouth-brooders (Clabaut 566). Food preference, they feed on scales of other fishes, as their name suggests, but they also feed on microbenthos and eggs (Clabaut 566). Scale-eaters are either left-biting or right-biting and nothing in between. The population of the two types is fairly the same.

Tilapiini

Tilapiini species are ubiquitous. Most species are maternal parents, though, some showed biparental care (Clabaut 566). Most of Tilapiini are polygamous but some species are substrate spawners. They feed on aquatic plants, detritus, and phytoplankton (Clabaut 566).

Trematocarini

The species belonging to Trematocarini tribe are mud dwellers. The study of Clabaut suggests that species are maternal parents. It also showed that Trematocarini are mouth-brooders. They feed on diatoms, detritus, gastropods, crustaceans, and zooplankton (Clabaut 566).

Tropheini

Tropheini species is among the most morphology diverse tribes. Majority of Tropheini species are rock dwellers (Clabaut 566), but some species are ubiquitous or sand dweller as well (Clabaut 566). Tropheini species are exhibit maternal parenting (Clabaut 566). Polygamy is more common in this tribe (Clabaut 566). Species are all mouth-brooders (Clabaut 566). Feeding preference of this tribe include aquatic weeds, algae, benthos, smaller fishes, invertebrates, gastropods, crabs, and Aufwuchs (Clabaut 566).

Tylochromini

Tylochromini species thrive on mud and sand (Clabaut 566). Parental care is maternal (Clabaut 566). Tylochromines exhibit polygyny (Clabaut 566). They eat mollusks, vegetal matters, and water plants.

Phylogenetic Impact

The most prominent method used in the study of Tanganyikan cichlid taxa has been the use morphological characters (i.e. body shape, coloration patterns) of species. The data collected are regarded as statistical data which are examined further to classify the organisms into the taxonomic structure. However, cichlid species in Lake Tanganyika are very hard to cluster into the tribe level because some morphological markers sometimes belong to other tribes making the species polyphyletic (Salzburger 6; Clabaut 569). Only the tribes Eretmodini and Tilapiini are consistent in their morphological characters (Clabaut 569).

Because of its excessive radiation, tribe level taxonomy is hard to retrieve. Even the use of statistical data does not guarantee plausible results on the taxonomic classification except the Eretmodini and Tilapiini tribes (Clabaut 569). This morphological diversity of organisms is due to rapidity of adaptive radiation. Morphological diversification is not directly affected by phylogeny. This means that species of the same tribe do not necessarily appear the same (Clabaut 569) but DNA sequences do.

Even if the phylogeny is imposing no distinguished morphological feature on the rapid speciation of Tanganyikan cichlids, testing for DNA sequences can lead to the outright clustering of the existing species to the tribes. Test for phylogeny involves DNA analysis: mitochondrial phylogeny by mitochondrial DNA analysis and AFLP (Amplified Fragment Length Polymorphism) phylogeny by AFLP DNA analysis (Koblmüller 3; Salzburger 6, 9). DNA sequences are studied using mitochondrial gene segments (i.e. NADH dehydrogenase subunit 2, D-Loop) and AFLP markers to construct the taxonomy in the tribal level (Koblmüller 5; Salzburger 6).

Monophyly is achieved using DNA analysis techniques. The examination of cichlid species at the nuclear level showed that the ancient tribes were divided into two major groups or clads: Eretmodini plus Laprologini and the rest in the C-lineage (Clabaut 569).

The C-lineage was the ancestral lineage of Cyprichromini, Perissodini, Orthochromini, Ectodini, Haplochromini and Tropheini which was included in the Haplocromines.  (Clabaut 569; Salzburger 8)). From these ancestors descended the existing species found in Lake Tanganyika today. Also, the results of the nuclear DNA phylogeny negates the earlier phylogenetic hypotheses derived from statistical morphological data presented by Liem and Stewart (Koblmüller 14). This resulted to revisions in the tribal designation of Tanganyikan cichlid species.

Ecological Impact

Clabaut’s study (569) on independent regression of ecological characters using 6-phosphogluconolactonase (abbreviated as PGLS) showed that the only reliable predictor for morphological diversification is feeding preferences; however, water depth is also significant. Table 1 shows the tabulated F– and P-tests results on PGLS taken from different ecological trait.

Table 1. Tabulated F- and P-tests data on the results of the PGLS models on the different ecological traits (Clabaut 569).

It appears that the only significant ecological character reliable to be used in predicting the Tanganyikan cichlid radiation based on Clabaut’s study is feeding preferences (Clabaut 569). Further research showed that there is an improved physiological fitness when other traits are also examined (Clabaut 569). Breeding type and water depth are significant contributors to the cichlids’ body shape. However, when doing the doing the multiple comparisons, feeding preferences no longer is a significant predictor (Clabaut 569).

But if the results of the F-tests and likelihood ratio tests as basis, it is more likely that feeding preference followed by water depth are the most influential to the body shape evolution of the Tanganyikan cichlids (Clabaut 570). The trait values show that invertebrate feeders, piscivores, and generalists correspond to the species that inhabits the intermediate and deep water environment (Clabaut 570). No other values of the specified traits show consistency in predicting body shapes of the species. Thus, feeding preference and water depth are the two most significant ecological traits that affect body shape evolution of the Tanganyikan cichlids (Clabaut 570).

Further analysis of the ecological traits was done to examine the morphological diversity of the cichlid species. Disparity values within and among tribes will show some correlation with the species flock in the different tribes. Table 2 shows the disparity values recorded by Clabaut (570).

Table 2. Disparity values of tribes with largest influence on disparity of the morphospace with their equivalent 95% confidence intervals (Clabaut 570).

Clabaut’s study (570) showed that differences within and among the tribes is slightly parallel with the number of specimen species per tribe and greater disparity correlation is observed with the number of species belonging to the tribe. As seen in Figure 1, tribes with largest influence on the morphospace disparity follow an increasing trend on the correlation graph. Disparity values of the whole morphospace were plotted against the number of species found in the particular tribe. It showed a regression trend.

In the graph, Tropheini and Perissodini tribes are away from the regression line (Clabaut 571). This follows that Tropheini, despite large species flock, has a relatively low disparity value. On the contrary, Perissodini has a very high disparity despite its relatively low number of species. The graph also showed that Lamprologini and Ectodini have the highest disparity values as well as the number of species flock found in these tribes (Clabaut 571). The Bathybatini and Limnochromini tribes are the least morphologically diverse as depicted in the graph.

Figure 1. Relationship between disparity values of the tribes (morphological diversity within a tribe) and number of specimen species examined in the particular tribe (Clabaut 570).

Clabaut’s disparity analysis showed that the species Cyphotilapia frontosa is the most significant contributor to the disparity of the whole morphospace (Clabaut 571). It has the highest value of disparity among the tribes. Exclusion of the species had significant effects on the disparity of the whole morphospace (Clabaut 571). The results also showed that other tribes not listed in Table 2 can not be included in the disparity analysis because no correlation was found that is important in calculating disparity (i.e. number of species; Clabaut 571).

The analysis of the two most important ecological traits showed some significant results. The pre-defined group was not consistent with the disparity tests of the different ecological characters. Feeding preference and water depth were identified as the most significant contributor in the body shape evolution of the fish, therefore, discreteness is achieved and that the fishes can be structured accordingly.

Morphological Diversity

The previous phylogenetic tree did not show consistency in the body shape evolution from the data gathered in Clabaut’s test (572). No directional trend was observed in the taxonomic classification. Thus, the problem of morphological diversity of the cichlids is recognized as caused by this erroneous hypothesis. In Clabaut’s study (572), morphological diversity was leveled to discrete units as a result of the disparity tests largely based on the ecological traits. The traits that had the most significant effect on the evolution of body shape within and among cichlid tribes were feeding preferences and water depth (Clabaut 570).

Lamprogini and Ectodini are the most prominent among the tribes as it occupy a large portion in the evolution morphospace because (i) it contains the most number of species and (ii) the species had the most diverse morphological characteristics (Clabaut 572). Examples of the extremity of Lamprogini shapes are the deep-bodied Altolamprologus calvus, and Telmatochromis vittatus which are elongated and short-headed (Clabaut 572). On the other hand, Ectodini species are elongated fish with a heads more pointed compared to the majority of the cichlids (Clabaut 572).

Another interesting result of the study is the contrary correlation of Perissodini and Tropheini tribes. It shows that the morphological diversity of the two tribes is not directly affected by the number of species. Perissodini tribe is comprised of approximately 25 to 30 species that are highly diverse in terms of morphological characters. On the contrary, Tropheini composed of more that 100 species exhibit minimal diversification.

Conclusion

Lake Tanganyika is home to the cichlid species considered by many as the best example of adaptive radiation. It contains cichlid species which is an ideal model system because of its rapid speciation despite the landlocked environment. Prior tribal classification of cichlid species found in Lake Tanganyika was proven erroneous because the use of statistical records based on morphological markers were not consistent within the tribal level of classification as some species that belong to one tribe also exhibit similar characteristics of a few other tribes.

However, the use of DNA analysis and geometric morphometrics methods provided solution to this problem of multiple plylogeny. DNA analysis using mitochondrial DNA sequence tests revealed that despite the difference in morphological characteristics, tribal classification is possible at least at the nuclear DNA level. These results were furthered by AFLP markers analysis.

The results of geometric morphometrics showed that the ecological characteristics—feeding preferences and water depth—are the most significant contributor to the body shape evolution of the cichlid species. Using disparity methods, biologists were able to provide a logical solution to the polyphylogeny problem at the tribal level classification. The conclusion was that “…morphological variation is strongly related to what a species specializes on trophically” (Clabaut 575). Disparity methods also provided evidence that phylogenetic characters are of little influence on the evolution of Tanganyikan cichlids.

The future of Tanganyikan cichlid species can now be predicted using the ecological traits, feeding preferences and water depth. The rapid speciation which resulted to diversification within the tribal assignments will further the morphological disparity in the future. The speciation however, is affected mostly by the fish’s ecological characters while phylogenetic traits are of little significance in the evolution of cichlid species found in the lake.

Works Cited

(Clabaut, 2006; Cohen, 1993; Koblmüller, 2007; Salzburger, 2005)

Clabaut, C., Paul M. E. Bunje, Walter Salzburger, and Axel Meye. (2006). GEOMETRIC MORPHOMETRIC ANALYSES PROVIDE EVIDENCE FOR THE ADAPTIVE CHARACTER OF THE TANGANYIKAN CICHLID FISH RADIATIONS. 2007 The Society for the Study of Evolution, 560-578.

Cohen, A. S., Michael J. Soreghan, Christopher A. Scholz. (1993). Estimating the age of formation of lakes: An example from Lake Tanganyika, East African Rift System. Geology, 21, 511-514.

Koblmüller, S., Egger, B., Sturmbauer, C., Sefc, K.M.(2007). Evolutionary history of Lake Tanganyika’s scale-eating cichlid fishes. Molecular Phylogenetics and Evolution, doi: 10.1016/j.ympev.2007.02.010

Salzburger, W., Tanja Mack, Erik Verheyen, and Axel Meyer. (2005). Out of Tanganyika: Genesis, explosive speciation, key-innovation, and phylogeography of the haplochrmine cichlid fishes. BMC Evolutionary Biology 2005, 5:17 doi: 10.1186/1471-2148-5-17