The cichlid fishes of the East African Great Lakes are the largest extant vertebrate radiation identified to date. These lakes and their surrounding waters support over 2,000 species of cichlid fish, many of which are descended from a single common ancestor within the past 10 Ma. The extraordinary East African cichlid diversity is intricately linked to the highly variable geologic and paleoclimatic history of this region. Greater than 10 Ma, the western arm of the East African rift system began to separate, thereby creating a series of rift basins that would come to contain several water bodies, including the extremely deep Lakes Tanganyika and Malawi. Uplifting associated with this rifting backponded many rivers and created the extremely large, but shallow Lake Victoria. Since their creation, the size, shape, and existence of these lakes have changed dramatically which has, in turn, significantly influenced the evolutionary history of the lakes' cichlids. This paper reviews the geologic history and paleoclimate of the East African Great Lakes and the impact of these forces on the region's endemic cichlid flocks.
East Africa had a highly dynamic geological and ecological history. Over the past 35 million years (Ma), tectonic plates have shifted, rifts in the landscape have opened, rivers have reversed course, and lakes have formed and desiccated. It is within this environment that the world’s largest extant vertebrate radiation has originated. Centered within the East African Great Lakes, over 2,000 species of cichlid fish have diversified to fill nearly every niche available to a freshwater fish. All of these fish are endemic to East Africa, many are single lake endemics, and several are microendemics found only at isolated areas within a given lake. Here, we examine the geologic and climatic history of East Africa and discuss how these forces have influenced this spectacular vertebrate radiation.
The East Africa rift system (EARS) is the roughly north-south alignment of rift basins in East Africa (Figure
Geographic position of the study region and location of the East African rift. The position of paleo-Lake Obweruka is displayed in light blue [
The climate of the African Great Lakes (Lakes Tanganyika, Malawi, and Victoria) is driven primarily by annual changes in precipitation associated with the migration of the intertropical convergence zone (ITCZ) (Figure
Seasonal position of the intertropical convergence zone (ITCZ). LV: Lake Victoria, LM: Lake Malawi, and LT: Lake Tanganyika.
The East African climate has been and continues to be dynamic [
Simultaneous with this onset of bipolar glaciation and glacial-interglacial cyclity is a cyclic trend in aridity across Africa [
Bathymetric maps of Lakes Tanganyika, Malawi, and Victoria for modern, Last Glacial Maximum (15–32 ka), megadrought period (~100 ka), and the middle Pleistocene (~1 Ma). Reconstruction for ~1 Ma is based on data from Lake Tanganyika’s subbasin [
Few taxa have been as influenced by the environmental and geological history of this region than fishes in the family Cichlidae. Cichlids are believed to have originated 121–165 Ma [
Characteristics of the three great East African Lakes and their cichlid lineages.
Lake | Lake | Lake Victoria | |
---|---|---|---|
Tanganyika | Malawi | ||
Maximum water depth (m) [ |
1470 | 700 | 79 |
Average water depth (m) [ |
580 | 264 | 40 |
Anoxic hypolimnion [ |
50–240 | 250 | None |
Surface area (km2) [ |
32,600 | 29,500 | 68,800 |
Approximate formation of lake [ |
9–12 Ma | >8.6 Ma | >0.4–1.6 Ma |
Approximate number of species [ |
~250 | ~700 | ~700 |
Number of cichlids tribes [ |
12–16 | 2 | 2 |
References in the first column refer to the table’s sources.
(A) The distribution of phylogenetic lineages. Colors indicate the distribution of genetic lineages: the distribution of the Lake Malawi lineage is displayed in purple, the Lake Tanganyika lineage is shaded in dark blue, the Malagarasi and Rukwa lineage are shown in green, the Lake Kivu lineage is colored purple, light red shading indicates the distribution of the Lake Victoria Superflock (LVSF), and the distribution of the South Kenyan—North Tanzanian lineage is displayed in yellow. (B) The possible colonization scenario for East African cichlids; the color of the arrows coincides with the colors of the lineages illustrated in part (A). (C) The distribution and possible colonization pathway for the North African and Israeli outposts of the LVSF. Phylogenetic data and colonization pathways are based on data from [
An estimated 2,000 species of cichlids occur in Lakes Victoria, Tanganyika, and Malawi, the majority of which are believed to have diverged within the past 10 Ma [
The aim of this paper is to synthesize the current understanding of the relationships between paleoclimate, geology, and the diversification of the East African cichlid species flock. Below, we explore these relationships in each of the lakes. In doing so, we hope to summarize the evolutionary diversification of East African cichlids within the context of the environmental and geological factors that have shaped their divergence.
Lake Tanganyika sits within the annual migration path of the ITCZ [
A number of paleoecological factors influence the cichlid diversity in Lake Tanganyika. Principle among these factors is the historic variability in lake level. Variation in lake level has been driven primarily by two major forces: tectonism and climate. Below, both mechanisms for lake level change will be summarized chronologically, and lake level lowstands will be identified. In addition, the historic connections between Lake Tanganyika and other water bodies in East Africa will be explored to (1) identify the likely origin of Lake Tanganyika’s cichlids and (2) identify possible migratory pathways for Tanganyikan cichlids that colonized Lakes Victoria and Malawi.
Lake Tanganyika formed as a series of half-grabens, which are down dropped blocks of land that are bordered by normal faults, within the western arm of the EARS. The geometry of rifting in Tanganyika is highly dependent upon the prerifting basement terrain and the remnants of a preexisting Permian-aged ancient rift [
The onset of rifting, the evolution of the lake basin, and the early history of Lake Tanganyika are dated relatively imprecisely because there are no direct dates from that time interval. Most of the lake basin’s early record has been dated using the reflection seismic-radiocarbon method (RSRM). RSRM estimates ages using sediment thickness estimates derived from reflection-seismic data combined with short-term sedimentation rates calculated from radiocarbon-dated cores. There is some inherent uncertainty in the reflection-seismic estimates of sediment thickness, and RSRM must make the sometimes tenuous assumption that sedimentation rates do not vary through time. Therefore, RSRM age estimates have large uncertainties. The RSRM ages discussed in this paper must be interpreted cautiously until corroborated by direct dating methods. The more recent history of Lake Tanganyika is very well constrained, and the dates for the last ~150 ka can be considered very reliable because they are derived from sediment core data.
Persistence of previous drainage patterns is a common early-stage feature in developing rifts [
Detailed seismic studies of the early history of Lake Tanganyika have been primarily focused on the north basin [
The timing of the earliest deposition in the central basin is difficult to resolve [
Following this early period of extremely active tectonism, a second period of geologic activity associated with modification of the existing half-grabens, uplift within the subbasins, renewed volcanic doming, and formation of syn-rift deposits occurred in the northern basin from about one million years ago until ~0.40 Ma [
Lake level has fluctuated dramatically throughout the history of Lake Tanganyika. During the first phase of deposition from approximately seven and a half million to one million years ago, there is evidence for several major unconformities in the northern basin [
The next phase of tectonism began at approximately one million years ago. During this time, lake level in the northern basin was 650–700 m below present lake level (bpll) [
Following this lowstand, lake level fluctuated dramatically, and the lake significantly contracted in the northern basin several times at ~390–~360, ~290–~260, ~190–~160, ~120–~100, ~40, and 32–14 ka [
Uplift related to rifting processes has caused Lake Tanganyika to have a highly dynamic history of connections to many of the major lakes in East Africa. These variable connections between Lake Tanganyika and the other waters of East Africa have allowed the dispersal of many cichlid lineages, including the haplochromines that seeded the highly diverse species flocks in Lakes Malawi and Victoria [
In the Cretaceous and early Cenozoic, prior to the initiation of rifting in the eastern arm of the EARS, the main drainage direction was west to east across the African continent into the proto-Indian Ocean [
Lakes Malawi and Tanganyika have a more complex relationship. Today, the two are not connected; however, the Malawian haplochromine cichlids are clearly derived from the Tanganyikan haplochromines [
Lake Tanganyika contains one of the most diverse fish faunas in the world. Though the exact number of fish species in Lake Tanganyika (or any of the three Great Lakes) is unknown, estimates suggest that Lake Tanganyika supports more than 365 species of fish, at least 115 of which are noncichlids [
Prior to rifting and the formation of any Tanganyikan basin, it has been suggested that an ancient river system that drained west into the Congo River system existed in the location of modern Lake Tanganyika (see above) [
Among the cichlids, it is clear that the Tanganyikan radiation is nested within cichlids endemic to the Congo River system [
The relationship between Tanganyikan and Congolese cichlids, however, is far from simple [
The diversification of the Haplochromini demonstrates the complex patterns of dispersal between the cichlids of Lake Tanganyika and its surrounding rivers. The common ancestor to the haplochromines evolved within a larger, lacustrine cichlid diversification in Lake Tanganyika. These haplochromines then colonized the rivers in the surrounding catchment of Lake Tanganyika. These generalized riverine haplochromines then secondarily invaded the lacustrine habitats in Lakes Tanganyika, Malawi, and Victoria. In each lake, the haplochromines (the “modern” haplochromines) then experienced a remarkable radiation [
In contrast to a predominately intralacustrine radiation, Lake Tanganyika could have been colonized by a larger number of more diverse taxa [
To resolve these alternative hypotheses, an accurate estimate of the divergence time for Lake Tanganyika’s cichlids is needed. Unfortunately, different calibration methods yield highly incongruent estimates. By calibrating the molecular clock to recent geologic events (e.g., the formation of Lake Malawi and the inundation of the Lukaga valley), Salzburger et al. [
Genner et al. [
It is worth noting, however, that these divergence times are highly dependent on the estimated timing of geologic events that have large uncertainties. Estimating the time since divergence in many cichlid lineages is further complicated by the age of the events used to calibrate the molecular clock. Many of cichlid diversification events occurred relatively recently, while the events used to calibrate the molecular clock are comparatively old (e.g., the breakup of supercontinents, the formation of lake basins) [
Incomplete taxon sampling is another major limitation of the current dating estimates [
The dynamic geological history and variable paleoclimate of Lake Tanganyika have shaped the cichlid diversity in this lake. The effect of these factors can be seen in three major areas: the maintenance of ancient cichlid lineages, the isolation of populations, and the admixture of previously isolated populations.
East Africa has experienced multiple periods of extreme aridity during the Pleistocene. For cichlid lineages to have persisted through such events, water sources must have remained available. Owing to the great depth of the lake, even during periods of extreme aridity [
Though these periods of aridity apparently did not extirpate the seeding lineages in Tanganyika, the resulting low lake levels likely had a significant impact on the distribution of genetic variation within and among these lineages. For example, an analysis by Sturmbauer et al. [
While the cross-lake affinities of mitochondrial haplotypes reflect the impact of major regressive events on the distribution of genetic variation in Lake Tanganyika’s cichlids, the interaction of historic hydrology and bathymetry can have a more subtle influence. Examining the genetic diversity in a collection of
At 700 m deep, 580 km long, and 30–80 km wide, Lake Malawi is one of the largest lakes in the world. Rifting in the Malawi Rift began during the Late Miocene, probably no less than ~8.5 Ma, and propagated from north to south resulting in three drainage basins [
The climate of Lake Malawi is strongly influenced by the seasonal migration of the ITCZ producing a wet-dry monsoonal cycle with the wet season extending from December to April. Annual precipitation is seasonal and ranges from <800 mm/yr in the south to >2400 mm/yr in the north [
Lake Malawi is permanently stratified with a chemocline depth of ~250 m [
The geologic and paleoclimatic history of Lake Malawi, which has influenced the connectivity of Lake Malawi to the surrounding waters and generated highly variable lake levels, has played an important role in the evolution of its endemic species. Below we review the geologic and paleoclimatic history of Lake Malawi and discuss their influences on the divergence of its haplochromine flock.
The Malawi Rift is located at the southern end of the western arm of East Africa rift between 9°and 14°S, and almost two-thirds of the rift is filled by Lake Malawi. The rift zone is comprised of four alternating asymmetrical half-grabens and several smaller basins, resulting in three main structural and drainage basins [
The exact timing of the onset of rifting is unknown; however, the earliest sediments that are associated with Cenozoic rifting in the Rungwe volcanic province, which borders the Malawi Rift to the north, are associated with welded tuffs dated to 8.6 Ma [
The early history of Lake Malawi is somewhat difficult to resolve. Radiometric dates from lavas and tuffs surrounding Lake Malawi [
Sedimentation in the Malawi Rift occurred contemporaneously with two of the early pulses of the Rungwe Volcanic province to the north of the lake between 8.6 and 1.7 Ma [
Between ~150 and 60 ka, there were dramatic fluctuations in lake level [
In many respects, the origin and diversification of Lake Malawi’s cichlid fish is the least complex of the three Great Lake radiations. Lake Malawi contains both tilapiine and haplochromine cichlids. The tilapia are represented by two distantly related lineages [
With over 700 endemic species [
The age of Lake Malawi’s species flock, like the ages of other East African cichlid flocks, is debated. Sturmbauer et al. [
Assuming an origination age of ~1 Ma for the Malawi cichlid flock, a riverine generalist similar to
Regressive events probably played an important role in shaping the evolutionary history of Lake Malawi cichlids. For example, Genner and Turner [
During the following transgressive period which brought the lake to its current level, the littoral areas north and south of the central basin were reinundated. The newly emerging habitats provided the opportunity for expansion and diversification of many species, which is reflected in both the patterns of genetic [
Within historical times, Lake Malawi has experienced meaningful but less dramatic regressive/transgressive events. For example, Owen et al. [
Lake Victoria is the largest freshwater lake in the tropics by surface area (68,800 km2) and the second largest in the world. The lake spans the equator in between the western and eastern branches of the EARS (Figure
Modern climate in the Lake Victoria region is primarily controlled by the ITCZ, which crosses Lake Victoria twice a year in March (long rains) and again in October (short rains) [
Today, the lake is hydrologically open with its major inlets being the Kagera and Katonga Rivers in the west. The primary outlet is the Victoria Nile at the northern end of lake. As much as 90% of water loss is from evaporation and 80% of the input is from direct precipitation on the lake surface [
The geologic and paleoclimatic history of Lake Victoria is considerably different than that of Lakes Tanganyika and Malawi. Principal among these differences is the depths of the lakes and the influence of arid intervals on the lake’s persistence. Lake Victoria is a relatively young, shallow lake that completely desiccated ~15 ka. Despite this event, the cichlids of Lake Victoria are species-rich and widely distributed outside the lake basin [
Prior to the onset of rifting in the Miocene, the Lake Victoria region drained from east to west. Rifting in the western branch of EARS during the late Miocene and the Pliocene probably created an NE-SW-oriented basin that began to capture some of the tributaries feeding the Congo River [
After formation of the lake, rifting continued to tilt the basin eastward, moving the center of lake 50 km to the east and exposing mid- to late-Pleistocene lacustrine sediments west of the lake [
The original outflow of Lake Victoria was probably to the west directly into Lake Albert [
Lake Victoria is extremely dependent on precipitation because as much as 80% of water input is from direct precipitation on the lake surface [
In Lake Albert, two paleosols have been identified between 18 ka and 12.5 ka, indicating that Lake Albert probably also desiccated at least twice since the LGM [
Across Africa, the early- to mid-Holocene was generally much wetter [
The evolutionary history of the cichlids of Lake Victoria cannot be fully understood without a broader discussion of the greater Lake Victoria species flock. While Lake Victoria supports at least 150 endemic species of cichlids, this diversification is only a fraction of cichlids belonging to the Lake Victoria superflock (LVSF) [
In order to understand the complex relationships of fish in this superflock, multiple phylogenetic, biogeographic, and population genetic studies have been performed. These have revealed a complex phylogeographic pattern, which reflects the influence of past geological and climatic events on the colonization of new habitats [
Molecular phylogenetic evidence indicates that the LVSF predates the most recent complete desiccation event at ~14-15 ka. The LVSF appears to have emerged at about 200 ka [
On the basis of these estimates of lineage divergence, several authors suggested that the lake never completely desiccated [
The rapid diversification of the LVSF has been attributed by some [
To find the source of the lineages that colonized the Lake Victoria region, multiple phylogenetic and population genetic studies have been performed. These studies identified several potential colonization sources, including the Kagera and Katonga Rivers [
Lake Kivu harbors 15 endemic haplochromine species in addition to three tilapiine species one of which is native (
Lake Kivu may be an important, though not ultimate, source of cichlid diversity. While at least two lineages from Lake Kivu have invaded the Lake Victoria region and diversified, it appears that a third lineage left Lake Kivu earlier and seeded a smaller radiation in North Eastern Tanzania [
While most researchers agree on the postdesiccation colonization and diversification of Lake Victoria’s endemic cichlids, the number of invading lineages appears to be less clear. Nagl et al. [
Nagl et al. [
While these relationships within the lake and the region are fairly complex, the phylogeography of the superflock becomes even more complicated when one considers members of the LVSF that occur in water bodies far from Lake Victoria. Members of the LVSF have been found as far south as Lake Rukwa [
The cyclical periods of aridity/humidity and the resulting contraction, diversification, and expansion of species resemble the classic biogeographic theory formulated by Bush [
It is clear that similar climatic cycles have influenced the diversification of East African cichlids [
The diversification of East African cichlids also informs on the “cradle” versus “museum” dichotomy in biogeographic theory. In attempting to explain higher diversity found at lower latitudes, Stebbins [
Fundamental to the extraordinary diversification of East African cichlids is the geologically, climatically, and ecologically dynamic environment in which they arose. Beginning at least 10–12 Ma, the western East African rift opened and created a lake basin in place of a swampy, meandering tributary to the Congo River. Seeded by Congolese cichlids, proto-Lake Tanganyika expanded and its cichlids diversified. Several of these diversifying lineages reinvaded the surrounding rivers and one lineage, the haplochromines, migrated south, perhaps via Lake Rukwa, to Lake Malawi, and north, possibly via Lake Kivu, to Lake Victoria. In each of these Great Lakes, the haplochromine cichlids formed remarkably large species flocks in an exceedingly short length of time. The evolutionary histories of the East African Great Lake cichlids were further influenced by fluctuating climatic conditions. During episodes of aridification in East Africa, the lakes were reduced in size and occasionally fully desiccated. The reduction of lake levels reshaped the lake habitats, dividing once connected populations and causing the admixture of previously isolated populations. Such processes facilitated the continued diversification of species and, at least in one instance, lead to the creation of a diverse monophyletic clade of hybrid origin. Lake Victoria most recently completely desiccated ~15 ka causing the extirpation of its endemic cichlids. As the lake infilled in the Holocene, it was then recolonized by cichlids that persisted through the arid interval in the extremely deep, but relatively small, Lake Kivu. The cichlids of Lake Kivu then went on to seed the Lake Victoria superflock, which while centered in Lake Victoria is distributed throughout the water bodies of East Africa and reaches far north into Israel via the Nile River. The cichlids of East Africa have long been recognized as an evolutionary model system in which to study phenotypic divergence and speciation. It is clear that this system also provides researchers with an exemplary system to study the impact of geologic, paleoecological, and paleoclimatic factors on the biogeography of a lineage.
The authors would like to thank S. Koblmüller as well as three anonymous reviewers whose comments greatly improved this paper.