The Impact of the Geologic History and Paleoclimate on the Diversification of East African Cichlids

Abstract

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.

Full text

Hindawi Publishing Corporation
International Journal of Evolutionary Biology
Volume 2012, Article ID 574851, 20 pages
doi:10.1155/2012/574851
Review Article
TheImpactoftheGeologicHistoryand
Paleoclimate on the Diversification of East African Cichlids
Patrick D. Danley,1Martin Husemann,1Baoqing Ding,1
Lyndsay M. DiPietro,2Emily J. Beverly,2and Daniel J. Peppe2
1Department of Biology, Baylor University, One Bear Place no. 97388, Waco, TX 76798, USA
2Department of Geology, Baylor University, One Bear Place no. 97388, Waco, TX 76798, USA
Correspondence should be addressed to Patrick D. Danley, patrick danley@baylor.edu
Received 24 January 2012; Revised 26 March 2012; Accepted 9 May 2012
Academic Editor: Stephan Koblmuller
Copyright © 2012 Patrick D. Danley et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.
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.
1. Introduction
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.
1.1. Geologic Setting and East African Climate. The East
Africa rift system (EARS) is the roughly north-south align-
ment of rift basins in East Africa (Figure 1) that defines the
boundary between the Somalian and African plates [2,3].
The EARS is divided into two structural branches that are
also oriented roughly north-south (Figure 1). Rifting in the
eastern branch began ∼30–35 Ma in the Afar and Ethiopian
Plateau and propagated north-south until it impinged on the
strong Precambrian Tanzanian cratonic block, which is in the
center of the East Africa Plateau [4]. The extensional stress
associated with the rifting or with widespread plume-related
uplift was then transported westward across the craton to
weaker mobile crust on the craton’s western edge creating the
western branch of the rift [4,5]. The timing of the initiation
of the western branch of the EARS is uncertain and has been
suggested to have begun as early as ∼25 Ma to as recently as
∼12–10 Ma [4,5]. After its onset, rifting then continued to
propagate in the western branch of the EARS forming the rift
basins that encompass Lakes Tanganyika and Malawi [2–7].
Extension and uplift associated with rifting created a reversal
in rivers flowing westward across the East African Plateau
and caused backponding into a topographic low in between
the two branches of the rift, forming Lake Victoria [6–12].

2 International Journal of Evolutionary Biology
LV
LT
LM
L. Kyoga
L. Turkana
L. Albert
L. Edward
L. George
L. Kivu
L. Rukwa
L. Mweru
L. Bangweulu
and Walilupe
L. Eyasi
L. Manyara
L. Natron
L. Naivasha
L. Magadi
Paleo-Lake Obweruka
Western
Rift branch
Eastern
Rift Branch
Figure 1: Geographic position of the study region and location of the East African rift. The position of paleo-Lake Obweruka is displayed in
light blue [1]. The approximate locations of the two main branches of the East African rift system are displayed in red-dashed line (LV: Lake
Victoria, LT: Lake Tanganyika, and LM: Lake Malawi).
TheclimateoftheAfricanGreatLakes(LakesTan-
ganyika, Malawi, and Victoria) is driven primarily by annual
changes in precipitation associated with the migration of the
intertropical convergence zone (ITCZ) (Figure 2). The ITCZ
is the zone of maximum insolation received by the Earth’s
surface and seasonally migrates between Tropics of Cancer
and Capricorn in June and December, respectively. The
warm air in the region of maximum heating rises, drawing
the cooler trade winds equatorward, where they converge,
effectively increasing convection and rainfall at the location
of the ITCZ. The movement of the ITCZ across the African
continent results in a wet-dry monsoonal climate for the
African Great Lakes. The southernmost extent of the ITCZ
is south of Lake Tanganyika; thus, it crosses the lake twice
between September and May as it migrates southward to the
Tropic of Capricorn and then back northward towards the
Tropic of Cancer. As a result, the lake experiences a long wet
season during which there is a lull in precipitation in January
and February [31] when the core of the ITCZ is south of Lake
Tanganyika and a pronounced, shorter dry season. The ITCZ
crosses Lake Malawi once a year producing pronounced wet
and dry seasons. The ITCZ crosses Lake Victoria twice due
to the lake’s position on the equator, resulting in two wet
and two dry seasons. In each of the African Great Lakes, a
significant portion of water loss is a result of evaporation;
thus, the lakes are very sensitive to changes in precipitation.

International Journal of Evolutionary Biology 3
LV
LT
LM
July
January
Figure 2: Seasonal position of the intertropical convergence zone
(ITCZ). LV: Lake Victoria, LM: Lake Malawi, and LT: Lake Tangan-
yika.
Variations in the position and intensity of the ITCZ can affect
the duration of the wet seasons in each lake, causing aridity
and significant changes in lake level [14,15,32].
1.2. East African Paleoclimate (10 Ma–Present). The East
African climate has been and continues to be dynamic [33].
Late Miocene (∼8–10 Ma) climate in East Africa was humid
and supported a variety of savanna and forest habitats,
including rain forests [34]. Following this humid period,
from ∼7–5 Ma, the ice volume of the Antarctic ice sheet
expanded and global temperatures fell [35–38]. This time
period is also associated with aridification across East Africa
[39,40], as well as the uplift of the Himalayas and the result-
ing intensification of the Indian Monsoon [41], which may
also have contributed to increased aridity. The early Pliocene
(5–3 Ma) is characterized by warmer and wetter conditions
globally and across Africa [42–46]. During this global warm,
wet period, East Africa was also very humid [44], perhaps
driving the expansion of Lake Tanganyika during the middle
Pliocene [47]. Significant Northern Hemisphere Glaciation
began and intensified between 3.2 and 2.6 Ma [48,49]
and beginning at ∼2.0 Ma, Southern Hemisphere Glaciation
expanded [50]. The interval beginning at ∼2.8 Ma represents
the onset of the glacial-interglacial cycles that characterizes
the Pleistocene [51–53].
Simultaneous with this onset of bipolar glaciation and
glacial-interglacial cyclity is a cyclic trend in aridity across
Tab le 1: Characteristics of the three great East African Lakes and
their cichlid lineages.
Lake Lake Lake Victoria
Tang any ik a Mal aw i
Maximum water depth
(m) [54]1470 700 79
Average water depth
(m) [54]580 264 40
Anoxic hypolimnion [54]50–240 250 None
Surface area (km2)[54]32,600 29,500 68,800
Approximate formation of
lake [7,9,10,55–57]9–12 Ma >8.6 Ma >0.4–1.6 Ma
Approximate number of
species [58]∼250 ∼700 ∼700
Number of cichlids tribes
[28,59,60]12–16 2 2
References in the first column refer to the table’s sources.
Africa [53,61–64]. In particular, the climate in East Africa
during the last 500 thousand years (ka) has been extremely
variable transitioning between wet and dry intervals that
have caused significant fluctuations in the lake levels of the
African Great Lakes (Figure 3)[10,13–18,37,65–71]. Of
particular importance for cichlid populations is an interval
from 135 to 70 ka when there were at least two intervals
of extreme aridity, called megadroughts, during which lake
levels in Lakes Malawi and Tanganyika probably fell dra-
matically, and Lake Victoria was likely completely desiccated
(Figure 3)[15,17–19]. Following this megadrought interval,
climate variability decreased considerably [19]. During the
Last Glacial Maximum (LGM), ∼20–15 ka, Africa again
experienced an increase in aridity, which caused the complete
desiccation of Lake Victoria, a significant drop in lake level of
Lake Tanganyika (∼250–300 m), and only a relatively minor
drop in the lake levels of Lake Malawi [9,12,15,17,19,20,
31,64,65,70,71].TheHolocenerepresentsanintervalofa
moderately fluctuating climate during which there have been
modest fluctuations in the lake levels of the African Great
Lakes [21,47,72].
1.3. East African Cichlids. 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 [73] within the Gondwanal
supercontinent. Their Gondwanan origin is reflected in the
current distribution of cichlids [74]: cichlids can be found
throughout Africa, the Neotropics, and Madagascar with
several additional species occurring in the Middle East, India,
and Sri Lanka. With an estimated 3,000 species, cichlids are
the most species-rich teleost family, and the focus of this
extraordinary species diversity is the East African Great Lakes
(Table 1, Figure 4).
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 [75]. Many of
these species are narrow endemics that are not found outside

4 International Journal of Evolutionary Biology
Lake Malawi Lake Tanganyika
Lake Victoria
Modern
750
750
750
250
250
250
1250
1250
1400
250
250
500
40
40
60
79
750
750
750
250
250
250
1250
1250
1400
250
250
500
250
250
500
750
750
750
250
250
250
1250
1250
1400
750
750
750
250
250
250
1250
1250
1400
No lake record.
Probably dry.
Lake record
poorly resolved.
Probably small,
shallow lake.
No lake record.
If lake basin
existed,
probably dry.
Lake was dry.
100 km
60 km
100 km 100 km 100 km
100 km
100 km
100 km
Last Glacial
Maximum
Megadrought
interval
(∼100 Ka)
Middle
Pleistocene
(∼1 Ma)
(32–14 Ka)
Figure 3: 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 [13], which
has been extrapolated to the rest of the lake. Thus, this reconstruction is speculative and must be verified by additional data from the central
and southern subbasins of Lake Tanganyika. Shaded areas show the maximum extent of lake during each interval. Lake Victoria’s islands are
showninblack.Lakelevelsbasedon[10,13–22]. Bathymetric maps based on data from the World Lake Database (http://wldb.ilec.or.jp/).
the lake (or a location within the lake) in which they exist.
This extraordinarily rapid, recent, and extensive species radi-
ation has been shaped by the environmental and geological
features that have affected the age, depth, and patterns of
connectivity of the waters in which the cichlids diversified.
The aim of this paper is to synthesize the current under-
standing 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

International Journal of Evolutionary Biology 5
Figure 4: (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 [23–30]
and modified from a Figure 4(a) of [23].
diversification of East African cichlids within the context of
the environmental and geological factors that have shaped
their divergence.
2. Lake Tanganyika
2.1. Paleoclimate and Geologic History of Lake Tanganyika.
Lake Tanganyika sits within the annual migration path of the
ITCZ [76] and thus experiences both a rainy season (Septem-
ber–May) and a dry season (June–August), as well as chang-
ing wind direction and strength throughout the year
[77]. Mean annual precipitation (MAP) in the region is
∼1200 mm/yr [78] across most of the lake except on the east-
ern margins near the Mahale Mountains where orographic
effects increase MAP to ∼1800 mm/yr [76].
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.
2.1.1. Tectonic History of Lake Tanganyika. 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 base-
ment terrain and the remnants of a preexisting Permian-aged
ancientrift[79,80]. The series of half-grabens are ∼160–
180 km long by 30–60 km wide [79]. The half-grabens alter-
nate east and west along the length of the lake and are deepest
along the border faults and slope upwards towards the
opposite shore via a series of faults and folds [79]. They are
separated by bathymetric highs known as “high-relief ” and
“low-relief” accommodation zones forming intra- and inter-
basinal ridges that separate the lake into three subbasins [81].
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

6 International Journal of Evolutionary Biology
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 esti-
mates 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 [82]. Based on this
analog, it has been suggested that prior to the Miocene
until the onset of rifting, the area that would become Lake
Tanganyika might have been the site of an ancient river
system that drained primarily through a paleo-Congo river
system [5,83]. However, this potential river drainage pattern
is uncertain. Rifting probably began ≥9–12 Ma in the central
basin and extended northward, then southward [55,79].
The creation of the Kivu-Ruzizi dome on the north end of
modern Lake Tanganyika probably also occurred during this
time [18]. The central subbasin infilled first, followed by the
north basin, and finally the south basin as the rift opened
[13,55,84].
Detailed seismic studies of the early history of Lake
Tanganyika have been primarily focused on the north basin
[13,55,84]. Each subbasin in Lake Tanganyika is structurally
distinct, and the seismic record from the north basin cannot
necessarily be extrapolated to the central and southern
subbasins. However, significant tectonic changes and major
sequence boundaries documented in the north basin may
represent lakewide events. Much of the early tectonic and lake
level history presented here is based on data from the north
basin and thus must be cautiously interpreted until the events
are also documented in the central and southern basins.
The timing of the earliest deposition in the central basin
is difficult to resolve [20]. However, there is evidence that
during early stages of rifting within the north basin, roughly
7.5 Ma, deposition began as a small, swampy lake formed and
then expanded to fill the developing rift [13,55,84]. From
the onset of rifting until about a million years ago, extension
and faulting continued during which time the half-grabens
found in each subbasin formed [13,84]. The end of this
initial rifting and depositional phase is marked by a nearly
lakewide erosional surface [13,84].
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 [13,47,84]. The end of the
second period of tectonism and deposition is marked by an
erosional surface, which is thought to represent a lowstand
event in the northern basin [13]. Subsequently, the basin has
been largely inactive with only limited small-scale faulting
occurring, allowing the formation of Lake Tanganyika’s
modern subbasins [13].
2.1.2. Lake Level History of Lake Tanganyika. Lake level has
fluctuated dramatically throughout the history of Lake Tan-
ganyika. During the first phase of deposition from approx-
imately seven and a half million to one million years ago,
there is evidence for several major unconformities in the
northern basin [13,84,85]. The timing of these events is
difficult to resolve; however, they are most likely related to
both tectonic and climatic factors [13]. During the initial
phase of tectonism, proto-Lake Tanganyika grew to fill the
developing rift basin, and at approximately three and a half
million years ago, there is evidence for a dramatic expansion
in the size of proto-Lake Tanganyika in the north basin, either
as a result of downwarping or due to a transition to a wetter
climate across Africa [13]. Following this high stand at about
three and a half million years ago, there is a pronounced
aridification trend across Africa that is associated with
Northern Hemisphere glaciation [39,48,52,53,63,64,86],
which likely affected lake level.
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) [13]. The onset of this lowstand is unclear, but it
was likely prolonged and may have begun considerably
earlier than one million years ago [20,85]. Based on the
modern bathymetry of Lake Tanganyika, a reduction in lake
level this large could have split the lake into three hydro-
logically and biologically isolated basins [83] (Figure 3).
However, continued tectonism over the last one million years
suggests that the bathymetry of the Lake Tanganyika could
have significantly changed during that time. Further, no
estimates of lake level in the central and southern subbasins
have been made for this time interval. Until new data
from the central and southern basin are obtained for this
interval, this separation into three subbasins is somewhat
speculative.
Following this lowstand, lake level fluctuated dramati-
cally, 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 [13,15,20,47,87–
89]. These lowstand events were related to either tectonic
factors (∼390–∼360 and ∼190–∼160 ka) or major intervals
of aridity (∼290–∼260, ∼120–∼100, ∼40, and 32–14 ka).
During the first three lowstand events at ∼390–∼360, ∼290–
∼260, and ∼190–∼160 ka, the deepest areas in the lake may
have either been separated or have only been connected by
emergent, swampy areas [13]. Since 106 ka, Lake Tanganyika
has remained a single connected water body, even during
significant intervals of aridity [20]. All of these lowstand
events, except for the most recent events (younger than
∼150 ka), have been well documented mainly in the lake’s
northern basin, and the exact ages of the events are somewhat
uncertain because they were made using RSRM. These RSRM
ages for the lake level change events must be corroborated
by direct dating methods before they can be considered
reliable enough for calibration purposes. Further research in
the central and southern basins is also needed to determine
whether all of the lowstand events were lake wide, which
would indicate a climatic, rather than a tectonic process.

International Journal of Evolutionary Biology 7
2.1.3. History of Connectivity. Uplift related to rifting pro-
cesses 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 [23].
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 [90]. The uplift of
the East African Plateau and the initiation of rifting in
the eastern arm of the EAR reversed the drainages west of
this propagating rift causing the rivers to flow from east
to west [90]. This suggests that as the central basin of
Lake Tanganyika formed, it was probably infilled by rivers
draining from the east. The most likely source was the
proto-Malagarasi River inflow and Lukuga River outflow
river system, which may be the only modern river system
that also existed prior to the formation of the Tanganyika
Rift [47,78]. Rifting propagated northward from the central
basin, and by about seven and a half million years ago,
the northern basin had begun to form and was being
infilled by a proto-Rusizi River [13]. This represents an early
connection between Lake Tanganyika and the Rusizi-Kivu
Basin, which was probably also forming at this time [91].
Variable rifting-related uplift has probably led to periodic
connections between the Rusizi-Kivu and Tanganyika Basins
[91]. These periodic connections may have also allowed for
a direction connection between Lakes Kivu and Tanganyika
after the formation of Lake Kivu ≥2Ma [91]. The pre-
Pleistocene history of this Kivu-Tanganyika connection is
poorly understood, however, as result of the general lack of
seismic data from Lake Kivu. Today the Rusizi River, which
flows from Lake Kivu, is one of Lake Tanganyika’s main
inlets. Most recently, this connection was likely open ∼13–
9.5 ka when volcanism in northern Lake Kivu blocked its
northern outlet to the Nile [92–94]. This inflow from the
Ruisizi River increased lake levels in Tanganyika, causing
renewed outflow via the Lukuga River [88]. Following these
openings, the Rusizi inlet and Lukuga outlet have closed
and reopened multiple times during the Holocene [47,88,
93,95]. It is possible that the Tanganyikan cichlids used
the connection to Lake Kivu via the proto-Rusizi River to
colonize northern bodies of water such as Lake Victoria.
Alternatively, the connection between Lake Victoria and Lake
Tanganyika may have been through the Malagarasi River,
which may have been connected to both Lakes Victoria and
Tanganyika during its geologic history.
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 [23]. Thus, fish from Lake
Tanganyika migrated to Malawi via an unknown riverine
connection.
2.2. Evolution and Diversification of Tanganyikan Cichlids.
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
[58,96]. Depending on how one groups these fish, the
cichlids of Lake Tanganyika span either 12 [97]or16different
tribes [59]. Within these tribes is a remarkable amount of
phenotypic diversity in body shape, trophic structures, and
behavioral and parental care strategies, making the cichlids
of Lake Tanganyika the most phenotypically variable species
assemblage in the East African Great Lakes [98]. The unique
geological features of the lake, along with the dynamic
evolutionary history of its cichlids, serve as an ideal model
to study origin of the cichlid diversity [99].
2.2.1. The Origin and Diversification of Lake Tanganyikan
Cichlids. Prior to rifting and the formation of any Tan-
ganyikan 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) [83].
This ancient connection between these two bodies of water
is further supported by the similarities of fish fauna found in
these systems. Eighteen of 24 fish families documented in the
Congo are found in tributaries and marshes around the lake.
Twelve of the 24 families from the Congo River system occur
in littoral and sublittoral zones of the lake. Seven Congolese
families are found in the benthic and four in the pelagic zone
of Lake Tanganyika [78]. However, recent immigration of
these families into this Lake Tanganyika cannot be ruled out.
Among the cichlids, it is clear that the Tanganyikan
radiation is nested within cichlids endemic to the Congo
River system [100]. According to Schwarzer et al. [100,101],
the East African cichlid radiation is a sister group to a
clade containing the substrate brooding genus Steatocranus
that is common in the Congo River system. Together with
the several species of tilapia ([100], clade “AII”), the genus
Steatocranus and the cichlids of Lakes Tanganyika, Malawi,
and Victoria form the Austrotilapiini. The Austrotilapiini are
further nested within the larger Haplotilapiini, which itself is
nested within a collection of taxa that are widespread across
the Congo River system and West Africa. The findings of
Schwarzer et al. [100] are largely consistent with those of
Farias et al. [74], both of which provide clear support for the
Congolese origin of the cichlids of Lake Tanganyika.
The relationship between Tanganyikan and Congolese
cichlids, however, is far from simple [24] (Figure 4). Poll
[97] originally identified 12 polyphyletic cichlid tribes in
Lake Tanganyika and concluded that the lake had been col-
onized multiple independent times. Since then, a number of
molecular phylogenetic studies, summarized by Koblm¨
uller
et al. [25], support the multiple invasion hypothesis, and
the 12 tribes that originated during the primary lacustrine
radiation have been identified: the Haplochromini (includ-
ing the Tropheini and the hyperdiverse haplochromines of
Lakes Victoria and Malawi), the “new tribe” consisting of
Ctenochromis species, the Cyphotilapiini, the Benthochro-
mini, the Limnochromini, the Perissodini, the Cyprichro-
mini, the Ectodini, the Lamprologini, the Eretmodini,
the Orthochromini, and the Bathybatini. After the initial

8 International Journal of Evolutionary Biology
invasion of the lake, many of these lineages experienced
a secondary radiation, which formed the modern cichlid
diversity found in Lake Tanganyika [99]. Following these
radiations, species from several of the radiating lineages
recolonized the rivers surrounding Lake Tanganyika [24,
75]. The lineages that secondarily invaded the surrounding
rivers include two species rich tribes, the Lamprologini and
Haplochromini, and one lineage currently found exclusively
in rivers, the Orthochromini. Two additional lineages, the
Tilapiini and the Tylochromini, recently invaded the lake
[102,103].
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 [23]. Thus Lake
Tanganyika is not only a sink for ancient African cichlid
lineages, but also a source of recent cichlid diversity in East
Africa.
In contrast to a predominately intralacustrine radiation,
Lake Tanganyika could have been colonized by a larger
number of more diverse taxa [75]. When the molecular
clock is calibrated to the breakup of Gondwana, molecular
clock estimates of divergence times suggest that nearly all
Tanganyikan lineages began to diverge prior to the estimated
onset of deep lake conditions [75]. In this model, the
divergence of Lake Tanganyika’s cichlid fishes did not occur
in Lake Tanganyika, but rather these lineages began to
diversify in the surrounding rivers prior to the formation
of the lake. Though novel, this much older estimate of the
diversification of Lake Tanganyikan cichlids conflicts with
long-held assumptions concerning the habitats suitable for
cichlid radiations, the evolution of resource partitioning, and
the biogeographic patterns of species distributions [25]. In
addition, it is well known that estimating recent diversifi-
cation events with ancient calibration points may produce
unreliable age estimates with large variances [104].
2.2.2. Ages of the Lake Tanganyikan Cichlid Radiations. 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.
[23] suggested that Lake Tanganyika’s cichlids evolved since
the formation of the lake basin 6–12 Ma and that the species-
rich haplochromines originated approximately 2.4 Ma.
While this estimate is widely accepted within the cichlid
community, this calibration method relies on assumptions
that are still debated within the geologic literature. For
example, this calibration method ignores the fact that the
timing of Lake Malawi’s formation is poorly constrained.
Genner et al. [75] generated age estimates using two
calibration methods. One method relied on the cichlid
fossil record, while the other relied on the breakup of
Gondwana. The cichlid fossil record calibration suggests that
Lake Tanganyika’s cichlids began diversifying coincident with
deep lake conditions (6–12 Ma), a finding that is consistent
with previous estimates [23]. Genner et al. [75] favor instead
the Gondwana calibration. This calibration suggests that
the diversification of Lake Tanganyika’s cichlids had begun
prior to the creation of Lake Tanganyika’s basin, possibly
in a now extinct paleolake. However, there is no geologic
evidence to support this paleolake hypothesis. Genner et al.’s
[75] conclusions were supported by estimates produced by
Schwarzer et al. [100] who used the fossil record of Ore-
ochromis lorenzoi (5.98 Ma), the divergence of Tylochromis,
and the remaining East African cichlids (53–89 Ma) as
calibration points. However, as was noted by Koblm¨
uller
et al. [25], Genner et al.’s [75] Gondwana calibration lacks
constraints on the more shallow bifurcations which may lead
to the incorrect assignment of divergence times. Koblm¨
uller
et al. [105]producedmodelscalibratedtoanumberof
geologic points including the occurrence of deep water
conditions in the Great Lakes and Genner et al.’s [75]
Gondwana calibration. From this analysis, Koblm¨
uller et al.
[105] conclude that the most parsimonious age estimate for
the divergence of Lake Tanganyika’s cichlids is ∼6Ma with
the most recent common ancestor of the haplochromines
occurring 5.3–4.4 Ma [105].
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 superconti-
nents, the formation of lake basins) [25,104]. Thus, the con-
tinued analysis of the geologic history of this dynamic region
is needed to accurately quantify the divergence times of the
East African cichlids [106]. It is clear that the divergence
times of Lake Tanganyika’s cichlid and the haplochromines
have yet to be resolved.
Incomplete taxon sampling is another major limitation
of the current dating estimates [105]. In most studies, one or
several of the major lineages are not included in the phyloge-
netic reconstruction. Further, based on recent publications,
not all of haplochromines lineages in the region have been
identified [26]. Dating estimates are further limited by the
lack of good calibration points. Estimates from molecular
clocks become more reliable when multiple geological and
fossil calibration points are used [105,107,108]incom-
bination with reliable rates of sequence evolution [109],
estimates of sequence saturation [110], and a posteriori
evaluation of estimated divergence times [108,110]. Few of
these requirements have been satisfied in previous analyses,
and the necessary data are just now becoming available
[106]. Thus, caution is necessary when considering the dates
provided here.

International Journal of Evolutionary Biology 9
2.2.3. Impact of Lake Level Fluctuations. The dynamic geo-
logical 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 pop-
ulations.
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 [13,20], Lake Tanganyika
would have been a refugium for ancient cichlid lineages,
which is reflected in age estimates of the diversification of
Tanganyikan cichlids [23,75].
Though these periods of aridity apparently did not extir-
pate 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. [111]ofmtDNA
regions from several Trop he us populations identified 6 phylo-
geographically unique haplotype clusters in three regions
of the lake: the northern basin, the central basin, and the
southern basin. Remarkably, in the central and southern
parts of the lake, individuals from one side of the lake
had mitochondrial haplotype identical to those found at
the opposite shoreline. It is possible that during one of the
major regressive events, Lake Tanganyika was separated into
three near-distinct lakes (Figure 3), and populations that are
currently separated by deep water were connected through
the shorelines of these three separate lakes. Alternatively,
during times of lake level fall, water levels at topographic
highs that separate the subbasins may have become shallow
enough to allow species to migrate from one side of the lake
to the other. Given that there are discrete haplotypes clusters
for each of the three subbasins and that their mitochondrial
haplotype are shared by individuals on opposite sides of the
lake in each subbasin, the separation into three near-distinct
lakes seems to be the more likely scenario.
While the cross-lake affinities of mitochondrial haplo-
types reflect the impact of major regressive events on the dis-
tribution 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 Trophe us m oorii populations, Koblm¨
uller
et al. [112] detected the effect that changes in lake level
have had on the genetic diversity over extremely limited
geographical distances. In this study, two distinct collections
of populations were identified. One collection was located on
the steeply sloping shores of the eastern side of the Chituta
Bay, while the other was located on the more gently sloping
shores west of the bay. Within the eastern populations, three
distinct populations which corresponded to geographic loca-
tions were identified. In contrast, the western populations
show greater degree of admixture. The authors conclude that
this pattern is consistent with the horizontal displacement of
the western shore populations as the lake regressed, causing
those populations to admix as the available habitat shrank.
The eastern populations migrated vertically along the steeply
sloping habitat, were not forced into secondary contact and
retained their accumulated genetic differences. In both the
eastern and western populations, the authors detect the
signature of population expansion that coincided with the
end of the Last Glacial Maximum. Population expansion was
greater in the western populations likely as a consequence
of this area having relatively greater area of available habitat
with a rise in lake level. The authors conclude that rapid,
dramatic, and relatively recent climatic changes in East Africa
drive both population divergence and population admixture.
3. Lake Malawi
3.1. Paleoclimate and Geologic History of Lake Malawi. 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 [6,7,56,85,91,113–116]. The two
northernmost drainage basins are deeper and steeper sided,
while the southern basin is shallower with a muddy bottom
[19,116]. The age of the formation of Lake Malawi is very
uncertain. Geologic evidence from deposits surrounding the
lake suggests that a deep lake may have first existed between
∼4.5 and 8 Ma [6,7,56,57,114,115]; however, it is possible
that a lake was present even earlier during the earliest phases
of rifting, 8–12 Ma [57,117]. Since formation, the lake has
undergone dramatic fluctuations in lake level during its
history [15,17,85,118].
The climate of Lake Malawi is strongly influenced by the
seasonal migration of the ITCZ producing a wet-dry mon-
soonal 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 [119].
The lake is close to the southern extent of the modern ITCZ
path (Figure 2), and thus changes in the position of the ITCZ
and its intensity considerably affect dry season length and
have been linked to periods of aridity and drops in lake level
during the Pleistocene [15,17,32].
Lake Malawi is permanently stratified with a chemocline
depth of ∼250 m [120], and today the lake is hydrologically
open. Several large drainage systems enter the lake across dif-
ferent structural settings in the three drainage basins [121],
and the sole outlet is the Shire River. Although outflow to the
Shire is continuous, more than 90% of water loss in the lake
is due to evaporation [119,122,123]. Because precipitation
is seasonal and evaporation is the main contributor to water
loss, lake level seasonally fluctuates up to a few meters.
Variability in lake level has caused disruption of the outflow
during historical times [72] and frequently throughout the
geologic history of the lake. Considerable reductions in lake
level during the lake’s geologic history have caused the outlet
to be disrupted, and the lake has become closed and more
saline [18,22].
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

10 International Journal of Evolutionary Biology
species. Below we review the geologic and paleoclimatic
history of Lake Malawi and discuss their influences on the
divergence of its haplochromine flock.
3.1.1. Tectonic History of Lake Malawi. 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
[114,116]. Each half-graben is bounded by a steep border
fault with high rift mountains (>1500 m above lake level)
along the lake shore on one side and a shallower flexural or
shoaling margin on the opposite side [121]. The border faults
link across “transfer zones” [85] which strongly influence
drainage and deposition patterns in each of the basins
[124,125]. The long-lived half-graben basins and associated
deep subsidence have resulted in the development of a long-
lived lake basin [95,116]. As a result, the lake is underlain
by >4000 m of lacustrine sediment that thins from the far
north to the south, indicating that rifting has propagated
from north to south [2,113–116]. The northern and central
basins, which are up to ∼700 m deep, are each ∼150 km
long and are characterized by very steep offshore slopes
at the border faults [116,125]. In these basins, sediment
is primarily transported downslope within channels and
canyons and out onto well-developed fan complexes [125,
126]. The offshore slopes in the shallower southern basin
(maximum depth =450 m) are less steep than the northern
and central basins, and the basin is primarily covered by fine-
grained, muddy sediments [125,126].
The exact timing of the onset of rifting is unknown; how-
ever, 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 [7,56]. The sediments are not directly
correlative with sediments in the subsiding Malawi Rift; thus,
8.6 Ma is a minimum age for the onset of rifting. Age models
based on sedimentation rates suggest that rifting commenced
between 8 and 12 Ma [117]. The earliest interval of rifting
and subsidence in the Malawi Rift probably occurred con-
temporaneously with two pulses of volcanism in the Rungwe
volcanic province between 8.6 and 1.7 Ma during which most
faulting occurred parallel or subparallel to the bounding
faults [7,56,57,117]. This was then followed by an ∼1Ma
interval of quiescence until the latest phase of rifting begin-
ning at ∼500–400 ka when there was a shift in rifting style to
oblique rifting and strike-slip deformation [117,127].
3.1.2. Lake Level History of Lake Malawi. The early history
of Lake Malawi is somewhat difficult to resolve. Radiometric
dates from lavas and tuffs surrounding Lake Malawi [7,
56] and sedimentological evidence suggest that a small,
shallow lake may have periodically existed after the onset of
rifting [57]. Lacustrine deposits, structural evidence, and an
increase in the rate of subsidence of the lake floor between
4.5 and 1.6 Ma suggest that a deep lake formed by ∼4.5 Ma,
if not earlier [57,128,129].
Sedimentation in the Malawi Rift occurred contempora-
neously with two of the early pulses of the Rungwe Volcanic
province to the north of the lake between 8.6 and 1.7 Ma
[7,56,57]. During this period of volcanism, rifting, and
deposition, there is evidence for multiple depositional hia-
tuses that likely correlate with significant reductions in lake
level [57]. The age of the early hiatuses is poorly constrained.
Two of them may be contemporaneous with onshore
unconformities that have been dated to 2.3 and 1.6Ma [56];
however, it is uncertain to which offshore unconformity
the lake events correlate. This onshore evidence indicates a
pronounced unconformity from 1.6 to 1.0 Ma during which
time Lake Malawi was probably significantly reduced in
size and possibly even completely desiccated [56,57,127]
(Figure 3). Preliminary evidence from drill core records also
suggests that Lake Malawi was a significantly reduced, saline
lake at ∼1.2 Ma [22]. Following this lowstand, lake level rose
towards deeper lake conditions [22]; however, the history of
lake level change is poorly resolved from 1.2 to ∼0.15 Ma.
Between ∼150 and 60 ka, there were dramatic fluctu-
ations in lake level [15,17–19]. During this time period,
there were two intervals of pronounced lake level drops up to
550 m bpll: one from 135 to 124ka and the other from 117 to
85 ka [15,17,19]. These two megadrought events would have
severely restricted Lake Malawi, and lake level may have been
reduced to as little as 2% of modern lake levels [19]. Between
the two megadroughts was an interval of relatively high lake
levels where the lake was stratified and the bottom water
was anoxic [18,19]. Beginning at ∼60 ka, the lake rose to
much higher levels, and changes in lake level were much less
dramatic than during the preceding 90 ka. There have been
modest fluctuations in lake level (100 m or less) since 60 ka,
including during the LGM [19]. However, in general lake
conditions during the last 60 ka have been relatively stable
and similar to those at present.
3.2. Evolution and Diversification of Malawian Cichlids. 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 hap-
lochromine cichlids. The tilapia are represented by two dis-
tantly related lineages [102]: Tilapia rendalli, asubstrate
spawning species common throughout the region, and an
endemic species flock, the chambo, containing three species
(Oreochromis karongae, Oreochromis lidole, and Oreochromis
squamipinnis)[130]. Given the paucity of endemic tilapiine
species, this section will focus on the more diverse hap-
lochromine lineage.
3.2.1. Origin and Diversification of Lake Malawi’s Haplochro-
mine Cichlids. With over 700 endemic species [58] most,
if not all of which appear to have descended from a single
common ancestor [131], the haplochromine cichlids of
Lake Malawi are the largest monophyletic species flock of
cichlid fishes. This species flock is nested within the Lake
Tanganyikan haplochromine group and is sister to the clade
containing the haplochromine cichlids of the Lake Victoria
superflock [23].

International Journal of Evolutionary Biology 11
The age of Lake Malawi’s species flock, like the ages of
other East African cichlid flocks, is debated. Sturmbauer
et al. [111] calibrated the age of Lake Malawi’s cichlids
to the geologic history of the lake [57]andestimatedthe
divergence of Lake Malawi’s cichlids at 0.93–1.64 Ma. In
contrast, Genner et al. [75] using two calibration methods
(see above) suggested that Lake Malawi’s cichlid flock orig-
inated either 4.6 Ma (Gondwanan calibration) or 2.4 Ma
(fossil calibration). Genner et al.’s [75] estimate suggests
that Lake Malawi’s cichlids began to diversify prior to
deep water conditions in the lake and/or persisted through
multiple megadroughts that either desiccated the lake or
dramatically altered the water chemistry thereby making the
lake uninhabitable. Genner et al.’s [75] estimates were not
supported by the work of Koblm¨
uller and colleagues [25].
In Koblm¨
uller et al.’s [25] analysis, the estimated age of the
Lake Malawi’s cichlids ranged between 0.72 and 1.80 Ma
for five of the seven calibration methods used. Though the
estimated age of Lake Malawi’s cichlid flock is not known, an
abundance of data suggests that this flock originated ∼1Ma.
If or how Lake Malawi’s haplochromine cichlids persisted
through the megadroughts of 135 ka and 117 ka is unknown.
Assuming an origination age of ∼1 Ma for the Malawi
cichlid flock, a riverine generalist similar to Astatotilapia
calliptera or Astatotilapia bloyeti [105]migratedfromLake
Tanganyika to Lake Malawi during that time [23] (Figure 4).
The cichlids of Lake Malawi then diverged into two large
clades plus several oligotypic lineages. The two large clades,
each containing ∼250–300 species, are reciprocally mono-
phyletic and consist of the rock-dwelling cichlids, or mbuna,
and the sand-dwelling cichlids [132]. Genner et al. [75]
suggest that the mbuna emerged 0.486 Ma (Gondwanan)
or 0.313 Ma (fossil), while the more diverse sand-dwelling
cichlids emerged 1.447 Ma (Gondwanan) or 0.855 Ma (fos-
sil). Given the large variances of these estimates and lack of
multiple calibration points [25], the reliability of these diver-
gence estimates is unknown. Future research utilizing a broad
sampling of taxa and multiple calibration points is needed to
accurately estimate the ages of these highly diverse clades.
3.2.2. Impact of Lake level Fluctuations. Regressive events
probably played an important role in shaping the evolution-
ary history of Lake Malawi cichlids. For example, Genner and
Turn er [133] recently discovered that one of Lake Malawi’s
most diverse clades evolved in response to a major regression
event. Between ∼75 and 135 ka, lake level dropped as much
as 580 m bpll [15,17]. As a consequence, the shallow benthic
habitats of southern Lake Malawi completely desiccated,
thereby reducing the proportion of shallow rock and sand
habitats relative to deep benthic and pelagic habitats. In
addition, this lowstand facilitated the hybridization of two
diverging lineages: the rock dwellers and the sand dwellers.
As a consequence of this event, this new hybrid lineage
rapidly adapted to the now plentiful deep benthic habitats
and gave rise to as many as one-third of all the species in
Lake Malawi’s haplochromine radiation.
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 [134] and species diversity [135]. This
period that reestablished littoral habitats and permitted the
rapid expansion of populations is likely synchronized with
similar phenomenon in other East African lakes [111,136].
Within historical times, Lake Malawi has experienced
meaningful but less dramatic regressive/transgressive events.
For example, Owen et al. [72] found that much of southern
Lake Malawi was exposed land as recently as 300 years ago.
Given the large number of species endemic to this area
[135,137,138], a regressive event of this magnitude would
suggest an exceptionally rapid diversification of southern
Lake Malawi endemics. These rapid and recent regres-
sive/transgressive events are believed to have disrupted and
permitted gene flow between mbuna populations and
thereby contributed to the high cichlid diversity in Lake
Malawi [139].
4. Lake Victoria
4.1. Paleoclimate and Geologic History of the Lake Victoria
Region. 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 1), giving it a
rectangular-shaped coastline. The timing of the formation of
Lake Victoria is uncertain. The lake has been suggested to
have formed between 1.6 and ∼0.40 Ma due to backponding
associated with the damming of westward flowing rivers by
the uplifting of the western arm of the EARS [7–12]. Unlike
the other African Great Lakes, Lake Victoria is not within
a rift basin, and as a result, it is relatively shallow with a
maximum depth of less than 100 m.
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)
[140]. The mean annual precipitation of the Lake Victoria
region is ∼1600 mm/yr [141].Thelakeismonomictic,and
mixing by the trade winds occurs during the dry season
between May and August [142]. However, in modern times,
the lake’s water column has become more stable, so that as
much as 40% of the lake’s bottom waters are anoxic [143].
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.Asmuchas90%ofwaterlossisfromevaporation
and 80% of the input is from direct precipitation on the
lake surface [141,144]. Because evaporation is consistent,
whereas precipitation in the Lake Victoria region is variable,
changes in precipitation have profound impacts on lake
level [145]. Due to its shallow depth (<100 m) and strong
dependence on precipitation to maintain lake level, Lake
Victoria has desiccated completely multiple times, probably
in response to increased aridity [10,14,16,21,70].
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

12 International Journal of Evolutionary Biology
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 [27,28]. Below we describe
the geologic and paleoclimatic history of Lake Victoria and
its surrounding waters and discuss how the geologic and
paleoclimatic history has influenced the extensive radiation
of the Lake Victoria cichlid superflock.
4.1.1. Evolution of Lake Victoria 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 [12,146]. Eventually rifting in the
western EARS completely truncated this network during the
Pleistocene, causing the rivers to flow eastward [7]. This
eastward flow from the western branch of the EARS, coupled
with the westward flow of rivers draining the western flank
of the eastern EARS [147], formed Lake Victoria as the low-
relief areas between the two arms of the EARS filled with
water. The timing of this formation is poorly constrained,
and the maximum estimate for the timing of formation is ∼
1.6 Ma [9–11], but because the lake formed by backponding
between the two arms of the EARS, it is possible that Lake
Victoria, or a “proto-Lake Victoria,” formed earlier than
1.6 Ma.
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 [11,143]. These sediments are exposed in
the Kagera River Valley 100 km to the west and 130 m above
present lake level. Doornkamp and Temple [11] used these
sediments to suggest that Lake Victoria was younger than
0.8 Ma. Mid-Pleistocene lacustrine sediments identified in
Kenya near the Kavirondo Gulf have been used to suggest
that Lake Victoria may be as old as 1.6Ma [9]. However, it
is important to note that these dates (0.8 Ma and 1.6 Ma) are
very imprecise and poorly constrained. Additional work is
needed to better constrain the age of these lacustrine sedi-
ments surrounding modern Lake Victoria. RSRM estimates
for the 60 m thick package of sediment in Lake Victoria
suggestatleast0.4Maofdeposition[10]. However, there are
multiple hiatuses in the succession, and their durations are
not possible to estimate, indicating that 0.4 Ma is a minimum
estimate for the formation of the lake [10].
The original outflow of Lake Victoria was probably to the
west directly into Lake Albert [148]. Uplift associated with
continued rifting of the EARS likely blocked this connection
and established the modern outflow through Lake Kyoga by
∼35–25 ka [148]. The first connection of Lake Victoria to the
White Nile may have been as early as ∼0.4 Ma [149]. The
timing of the modern connection of Lake Victoria to the
White Nile via the Victoria Nile is uncertain though it has
probably occurred in the last 13 ka [8].
4.1.2. Paleoclimate and Paleoenvironment. Lake Victoria is
extremely dependent on precipitation because as much as
80% of water input is from direct precipitation on the lake
surface [118,141,144]. Seismic data indicates that lake
level has fluctuated significantly during the Pleistocene and
Holocene and that there were multiple intervals when the
lake completely desiccated [10]. Coring of the uppermost
sediments provides evidence for the most recent desiccation
events. Near the base of the core is a 16-17ka paleosol that
represents drying at the end of the LGM [10,14,16]. This
paleosol has shrink-swell features that identify it as a paleo-
Ve r t i so l [ 10]. In order to form a Vertisol, the soil must be
completely desiccated for at least one month per year [150].
Seismic data indicate that the paleo-Vertisol can be traced
continuously across the entire lake basin [10,14,16,143].
The bathymetry of Lake Victoria does not allow for the
formation of separate basins where smaller lakes could have
persisted [10,14,16,143], leaving no refugium for cichlids.
Following this desiccation event during the LGM, the lake
dried up again between 14 and 15 ka [14,16,21]. Thus, Lake
Victoria was completely desiccated for at least two intervals
from the LGM to ∼14 ka, and it is highly unlikely that the lake
could have supported any cichlid populations during these
events. Following these desiccation events, the lake probably
filled relatively quickly [21].
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 [151].
Other evidence from the Burundi Highlands and from the
Congo River Basin also suggests that the late Pleistocene in
equatorial East Africa was arid [152,153]. This evidence for
aridity coupled with the roughly contemporaneous paleosol
horizons in Lakes Victoria and Albert suggests that many
of the lakes in which the Lake Victoria superflock currently
persists (e.g., Lakes Victoria, Albert, George, and Kyoga) were
probably completely dry for at least some period of time
during the LGM and the subsequent arid interval during the
latest Pleistocene.
Across Africa, the early- to mid-Holocene was generally
much wetter [86], and by ∼12 to 13 ka lake levels in Lake
Victoria and other surrounding lakes began to fill to their
current level [21,143,154]. Throughout the Holocene, Lake
Victoria experienced changes in lake levels, but no other
complete desiccations [21]. During the last 4 ka, climate
has become more seasonal, and precipitation has decreased,
which has likely caused lake level to decrease such that Lake
Nabugabo separated from Lake Victoria [21,155–157].
4.2. Evolution and Diversification of the Lake Victoria Super-
flock. 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) [27]. The
superflock consists of over 600 species of haplochromine
cichlids spread across nearby lakes such as Lakes Albert,
Edward, George, Kyoga, Kivu, and the rivers of the region
[27], in addition to more distant locations such as the more
southern Lake Rukwa and its drainage [27], Lake Turkana
[105], smaller North-Eastern Tanzanian lakes [26], and water
bodies as far north as Egypt, Tunisia, and Israel [29,30,105].

International Journal of Evolutionary Biology 13
Thus, the LVSF has a geographic distribution far larger than
those of Lakes Tanganyika and Malawi [28,158].
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 [26,28,105]. Below we examine
these patterns with special attention given to identifying the
geographic origin of the superflock, its age, and how its
members persisted through recent periods of extreme aridity
in East Africa.
4.2.1. Age and Origin of the Lake Victoria Superflock. Molec-
ular 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 [159]
with major diversification of lineages between 98 and 132 ka
[28]. Similar patterns in which genetic lineages predate the
refilling of the Lake Victoria basin were found in cyprinid
fish [160], catfish [161], and snails [162,163]. However,
all of these estimated ages rely on the estimated timing of
geological events which themselves may be revised through
future research (see above).
On the basis of these estimates of lineage divergence,
several authors suggested that the lake never completely
desiccated [164,165]. Yet, the geological evidence is unam-
biguous. Lake Victoria and its surrounding waters were
completely dry at least once, and possibly twice, between
∼14 and 20 ka [10,14,16,143,151]. This conclusion is
consistent with phylogenetic analysis of the superflock. Based
on estimates of speciation rates for all cichlid lineages in
the Lake Victoria region, Seehausen [166] did not reject the
Pleistocene desiccation event and concluded that the lake
was colonized from a source outside of the basin rather than
persisting in small refugia within the basin itself. Hence, the
major diversification of the modern cichlid superflock in the
Lake Victoria region coincides with the Holocene refilling
of the lake when large areas of habitat became available
again. This conclusion is supported by the apparent severe
bottleneck [136] and subsequent range expansion [111] that
occurred in this lineage. Together these studies support the
conclusion that the present cichlid diversity endemic to Lake
Victoria must be the result of recent colonization followed by
intralacustrine speciation.
The rapid diversification of the LVSF has been attributed
by some [167] to the formation of a hybrid clade leading
to morphological novelty. Such hybridization events at the
base of highly diverse clades have been documented in Lakes
Tanganyika [168] and Malawi [60]. A similar event may have
influenced the origin of Lake Victoria’s cichlids [169].
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 [170] and the Congo [171]. Another
possible source for the ancestral lineages could have been
paleo-Lake Obweruka that formed 8 Ma but desiccated
during the late Pliocene [1]. Paleo-Lake Obweruka matched
Lake Tanganyika in size and depth and hence provided a large
area of habitat [1]. Such paleo-lakes have been implicated
in the diversification of related cichlid taxa. Joyce et al.
[172], for example, showed that much of the riverine cichlid
diversity in southern Africa can be traced back to paleo-
Lake Makgadikgadi, where the group radiated before the lake
desiccated and the species dispersed into the surrounding
waters. However, geological estimates of the desiccation of
paleo-Lake Obweruka indicate that it likely did not play a
role in seeding the modern constituents of the LVSF because
it disappeared before the formation of modern Lake Victoria.
Yet another hypothesis suggests that the LVSF arose out of a
lineage that persisted in refugia in Tanzania. The lakes in the
Eastern Arc region of Tanzania did not desiccate during the
Pleistocene and have been suggested to have served as refugia
for the Lake Victoria species flock [25,173]. This, however,
seems unlikely. Hermann et al. [26] demonstrated that the
cichlids found in that region represent an ancient lineage
which is not closely related to the LVSF. There now seems
to be general agreement that the Lake Victoria superflock
arose more recently in the much smaller Lake Kivu [28,136]
(Figure 4).
4.2.2. The “Out of Kivu Hypothesis”. Lake Kivu harbors 15
endemic haplochromine species in addition to three tilapiine
species one of which is native (Oreochromis niloticus) while
the remaining two (Oreochromis macrochir, Tilapia rendalli)
were introduced [174]). Among the haplochromine species,
two phylogenetically distinct lineages can be distinguished
both genetically and phenotypically [175]. Interestingly,
these two groups correspond to the two lineages of hap-
lochromines found in Lake Victoria [175]. Furthermore,
phylogenetic and population genetic evidence clearly indi-
cates that the ancestors of the superflock are derived from
Lake Kivu’s haplochromines [28,136]. Molecular clock
estimates suggest that the split between the Lake Victoria and
Kivu lineages occurred less than 41.5–30.5 ka. This estimate
roughly coincides with the eruptions of Virunga volcanoes
(25–11 ka), which disrupted the connection between Kivu
and the northern lakes in the Lake Victoria region (Lakes
Albert,Edward,George,andKyoga)[28]. However, a
causative relationship between the split of Lake Kivu’s and
Lake Victoria’s cichlids and the eruptions of the Virunga vol-
canoes is speculative. The apparent similarities in the timing
of these events depends on a geologic calibration point, the
origin of lacustrine conditions in Lake Malawi [57], which is
relatively poorly constrained.
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 diversi-
fied, it appears that a third lineage left Lake Kivu earlier and
seeded a smaller radiation in North Eastern Tanzania [26].
The lineage might have been separated from the western
cichlids during the formation of the Kenyan-Tanzanian rift
system formation [26].
4.2.3. Relationships within the LVSF and between the Other
Lakes. While most researchers agree on the postdesiccation
colonization and diversification of Lake Victoria’s endemic

14 International Journal of Evolutionary Biology
cichlids, the number of invading lineages appears to be less
clear. Nagl et al. [27] suggested that the lake has been invaded
at least twice, which is consistent with the results of Verheyen
et al. [28]. Additionally, this study found evidence that Lakes
Albert, George, and Edward have been seeded at least four
times. It appears, however, that only one of the four invading
lineages radiated extensively, while the others are rare relicts.
Although the number of colonizers remains unclear, some
phylogenetic patterns can be found within the LVSF.
Nagl et al. [27] found seven haplogroups within the Lake
Victoria superflock. Two lineages (II, IV) are found only at
and around Lake Rukwa. A third lineage is restricted to Lake
Manyara and Tanzanian rivers (VI). A fourth lineage is found
in these same rivers (III), while a fifth lineage is restricted
to the Malagarasi River east of Lake Tanganyika (I). A sixth
lineage (VII) is found in the Malagarasi River, the Kazinga
Channel, and Lake George. However, all species endemic to
Lake Victoria and its surrounding lakes and rivers fell into a
single haplogroup (V). Within this haplogroup V, four sub-
groups were distinguished: one is endemic to Lake Victoria
(VD), one is found in the rivers close to Lake Rukwa (VA),
and the other two lineages have a wider distribution within
the Lake Victoria region and can be found in Lakes Victoria,
Albert, Edward, and George and adjacent rivers (VB, VC).
While these relationships within the lake and the region
are fairly complex, the phylogeography of the superflock
becomes even more complicated when one considers mem-
bers 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 [27], in the North Eastern Lake Turkana [25],
and as far North as Egypt and Israel [25,29,30]. These
distributional patterns are interesting from a biogeographical
as well as from a paleogeographical standpoint since they
inform on past connectivity and colonization events. For
example, the presence of members of the superflock in
Lake Rukwa has been explained by a series of river capture
events that might have enabled the colonization of Lake
Rukwa from the Lake Victoria region [25]. Lake Turkana
was probably colonized fairly recently in the early Holocene,
when Turkana spilled over into the Nilotic system and a
connection between the Turkana and the Nile was established
[176]. This is supported by a fairly young age of the Lake
Turkana endemic species H. rudolfianus which groups with
the LV species flock [25]. Northern African locations in turn
were likely colonized ∼11 ka via the Nile [25].
5. Biogeographic Implications
The cyclical periods of aridity/humidity and the resulting
contraction, diversification, and expansion of species resem-
ble the classic biogeographic theory formulated by Bush
[177] to explain Amazonian diversity [177]. In Bush’s [177]
diversity-instability hypothesis, species become fragmented
due to climatic changes associated with glacial/postglacial
environmental conditions [177]. While fragmented, these
species undergo allopatric speciation. Repeated bouts of
climatic change through the Pleistocene would act as species
pumps that increase the species diversity in the tropics.
It is clear that similar climatic cycles have influenced the
diversification of East African cichlids [60,111,112,134,
136,166]. In East Africa, periods of humidity facilitated the
dispersal and fragmentation of species [23,134,136]. Periods
of aridity may either have led to further fragmentation due
to basin geomorphology [111] or facilitated admixture as
the lake levels dropped, and the available area to cichlids
dwindled [60,168]. Populations and species diverged during
these repeated climatic cycles at both the regional [23]and
within-lake scales [112]. Thus, climatically driven cycles of
desiccation and inundation may have acted as species pumps
within East African cichlids [98].
The diversification of East African cichlids also informs
on the “cradle” versus “museum” dichotomy in biogeo-
graphic theory. In attempting to explain higher diversity
found at lower latitudes, Stebbins [178] suggested that trop-
ical regions may act as either “cradles,” areas with high rates
of diversification, or “museums,” areas supporting diversity
with low extinction rates. Given the extraordinary diversifi-
cation of East African cichlids, the East African Great Lakes
are clearly cradles of diversity [58]. However, the great depths
of Lakes Tanganyika, Malawi, and Kivu allowed for the per-
sistence of cichlid lineages through prolong periods of aridity
[25,28,75,100,105,136,175]. In this way, East African lakes
also conform to the “museum” hypothesis. As with a growing
list of tropical species [179,180], East African cichlids split
the false dichotomy of “cradle” versus “museum” because
their habitats act as both cradles and museums.
6. Conclusions
Fundamental to the extraordinary diversification of East
African cichlids is the geologically, climatically, and ecologi-
cally dynamic environment in which they arose. Beginning at
least 10–12 Ma, the western East African rift opened and cre-
ated 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

International Journal of Evolutionary Biology 15
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.
Acknowledgments
The authors would like to thank S. Koblm¨
uller as well as three
anonymous reviewers whose comments greatly improved
this paper.
References
[1] R. G. Taylor and K. W. F. Howard, “Post-Palaeozoic evo-
lution of weathered landsurfaces in Uganda by tectonically
controlled deep weathering and stripping,” Geomorphology,
vol. 25, no. 3-4, pp. 173–192, 1998.
[2] B. R. Rosendahl, “Architecture of continental rifts with spe-
cial reference to East Africa,” Annual Rev iew of Earth and
Planetary Sciences, vol. 15, pp. 445–503, 1987.
[3] J. Chorowicz, “The East African rift system,” Journal of Afri-
can Earth Sciences, vol. 43, no. 1–3, pp. 379–410, 2005.
[4] A. A. Nyblade and R. A. Brazier, “Precambrian lithospheric
controls on the development of the East African rift system,”
Geology, vol. 30, no. 8, pp. 755–758, 2002.
[5] E. M. Roberts, N. J. Stevens, P. M. O’Connor et al., “Initiation
of the western branch of the East African Rift coeval with the
eastern branch,” Nature Geoscience, vol. 5, no. 4, pp. 289–294,
2012.
[6]C.J.Ebinger,A.L.Deino,R.E.Drake,andA.L.Tesha,
“Chronology of volcanism and rift basin propagation: rung-
we volcanic province, East Africa,” Journal of Geophysical
Research, vol. 94, no. 11, pp. 15785–15803, 1989.
[7] C. J. Ebinger, “Tectonic development of the western branch
of the East African rift system,” Geological Society of America
Bulletin, vol. 101, no. 7, pp. 885–903, 1989.
[8] M. R. Talbot and M. A. J. Williams, “Cenozoic evolution of
theNileBasin,”inThe Nile: Origin, Environments, Limnology
and Human Use, H. J. Dumont, Ed., pp. 37–60, Springer
Science + Business Media B.V., 2009.
[9] P. E. Kent, “The Miocene beds of Kavirondo, Kenya,” Quar-
terly Journal of the Geological Society of London, vol. 100, no.
1–4, pp. 85–118, 1944.
[10] T. C. Johnson, C. A. Scholz, M. R. Talbot et al., “Late pleis-
tocene desiccation of Lake Victoria and rapid evolution of
cichlid fishes,” Science, vol. 273, no. 5278, pp. 1091–1093,
1996.
[11] J. C. Doornkamp and P. H. Temple, “Surface, drainage and
tectonic instability in part of southern uganda,” The Geo-
graphical Journal, vol. 132, no. 2, pp. 238–252, 1966.
[12] W. W. Bishop and A. F. Trendall, “Erosion-surfaces, tectonics
and volcanic activity in Uganda,” Quarterly Journal of the
Geological Society, vol. 122, no. 1–4, pp. 385–420, 1967.
[13] A. S. Cohen, K. E. Lezzar, J. J. Tiercelin A, and M. Soreghan,
“New palaeogeographic and lake-level reconstructions of
Lake Tanganyika: implications for tectonic, climatic and bio-
logical evolution in a rift lake,” Basin Research, vol. 9, no. 2,
pp. 107–132, 1997.
[14]J.C.Stager,D.B.Ryves,B.M.Chase,andF.S.R.Pausata,
“Catastrophic drought in the Afro-Asian monsoon region
during Heinrich event 1,” Science, vol. 331, no. 6022, pp.
1299–1302, 2011.
[15] C. A. Scholz, T. C. Johnson, A. S. Cohen et al., “East African
megadroughts between 135 and 75 thousand years ago and
bearing on early-modern human origins,” Proceedings of the
National Academy of Sciences of the United States of America,
vol. 104, no. 42, pp. 16416–16421, 2007.
[16] J. C. Stager, P. A. Mayewski, and L. D. Meeker, “Cooling
cycles, Heinrich event 1, and the desiccation of Lake Victo-
ria,” Palaeogeography, Palaeoclimatology, Palaeoecology, vol.
183, no. 1-2, pp. 169–178, 2002.
[17] R. P. Lyons, C. A. Scholz, M. R. Buoniconti, and M. R.
Martin, “Late Quaternary stratigraphic analysis of the Lake
Malawi Rift, East Africa: an integration of drill-core and
seismic-reflection data,” Palaeogeography, Palaeoclimatology,
Palaeoecology, vol. 303, no. 1–4, pp. 20–37, 2011.
[18] A. S. Cohen, J. R. Stone, K. R. M. Beuning et al., “Ecological
consequences of early Late Pleistocene megadroughts in
tropical Africa,” Proceedings of the National Academy of
Sciences of the United States of America, vol. 104, no. 42, pp.
16422–16427, 2007.
[19]C.A.Scholz,A.S.Cohen,T.C.Johnson,J.King,M.R.
Talbot, and E. T. Brown, “Scientific drilling in the Great Rift
Valley: the 2005 Lake Malawi Scientific Drilling Project—an
overview of the past 145,000years of climate variability in
Southern Hemisphere East Africa,” Palaeogeography, Palae o-
climatology, Palaeoecology, vol. 303, no. 1–4, pp. 3–19, 2011.
[20] M. M. McGlue, K. E. Lezzar, A. S. Cohen et al., “Seismic
records of late Pleistocene aridity in Lake Tanganyika, tropi-
cal East Africa,” Journal of Paleolimnology,vol.40,no.2,pp.
635–653, 2008.
[21] M. R. Talbot and T. Lærdal, “The Late Pleistocene—
Holocene Palaeolimnology of Lake Victoria, East Africa,
based upon selemental and isotopic analyses of sedimentary
organic matter,” Journal of Paleolimnology,vol.23,no.2,pp.
141–164, 2000.
[22] M. W. Blome, A. S. Cohen, and M. J. Lopez, “A 1,200,000
year paleoecological record from ostracodes, charcoal, and
other paleoclimate indicators from lake malawi, East Africa,”
in Proceedings of the GSA Annual Meeting in Minneapolis,
October 2011.
[23] W. Salzburger, T. Mack, E. Verheyen, and A. Meyer, “Out
of Tanganyika: genesis, explosive speciation, key-innovations
and phylogeography of the haplochromine cichlid fishes,”
BMC Evolutionary Biology, vol. 5, no. 1, article 17, 2005.
[24] W.Salzburger,A.Meyer,S.Baric,E.Verheyen,andC.Sturm-
bauer, “Phylogeny of the Lake Tanganyika cichlid species
flock and its relationship to the Central and East African
haplochromine cichlid fish faunas,” Systematic Biology, vol.
51, no. 1, pp. 113–135, 2002.
[25] S. Koblm¨
uller, K. M. Sefc, and C. Sturmbauer, “The Lake
Tanganyika cichlid species assemblage: recent advances in
molecular phylogenetics,” Hydrobiologia, vol. 615, no. 1, pp.
5–20, 2008.
[26] C. M. Hermann, K. M. Sefc, and S. Koblm¨
uller, “Ancient
origin and recent divergence of a haplochromine cichlid
lineage from isolated water bodies in the East African Rift
system,” Journal of Fish Biology, vol. 79, no. 5, pp. 1356–1369,
2011.

16 International Journal of Evolutionary Biology
[27] S. Nagl, H. Tichy, W. E. Mayer, N. Takezaki, N. Takahata, and
J. Klein, “The origin and age of haplochromine fishes in Lake
Victoria, East Africa,” Proceedings of the Royal Society B, vol.
267, no. 1447, pp. 1049–1061, 2000.
[28] E. Verheyen, W. Salzburger, J. Snoeks, and A. Meyer, “Origin
of the superflock of cichlid fishes from Lake Victoria, East
Africa,” Science, vol. 300, no. 5617, pp. 325–329, 2003.
[29] M. J. Genner and M. P. Haesler, “Pliocene isolation of a
north-west Saharan cichlid fish,” Journal of Fish Biology, vol.
76, no. 2, pp. 435–441, 2010.
[30] N. Y. Werner and O. Mokady, “Swimming out of Africa:
mitochondrial DNA evidence for late Pliocene dispersal of a
cichlid from Central Africa to the Levant,” Biological Journal
of the Linnean Society, vol. 82, no. 1, pp. 103–109, 2004.
[31] A. S. Cohen, K. E. Lezzar, J. Cole et al., “Late Holocene link-
ages between decade–century scale climate variability and
productivity at Lake Tanganyika, Africa,” Journal of Paleolim-
nology, vol. 36, no. 2, pp. 189–209, 2006.
[32] T.C.Johnson,E.T.Brown,J.McManus,S.Barry,P.Barker,
and F. Gasse, “A high-resolution paleoclimate record span-
ning the past 25,000 years in Southern East Africa,” Science,
vol. 296, no. 5565, pp. 113–132, 2002.
[33] S. E. Nicholson, “A review of climate dynamics and climate
variability in Eastern Africa,” in The Limnology, Climatology
and Paleoclimatology of the East African Lakes,T.Johnsonand
E. Odada, Eds., OPA, Amsterdam, The Netherlands, 1996.
[34] J. D. Kingston, B. Fine Jacobs, A. Hill, and A. Deino,
“Stratigraphy, age environments of the late Miocene Mpesida
Beds, Tugen Hills, Kenya,” Journal of Human Evolution, vol.
42, no. 1-2, pp. 95–116, 2002.
[35] J. P. Kennett, “Cenozoic evolution of antarctic glaciation, the
Circum-Antarctic ocean, and their impact on global paleo-
ceanography,” Journal of Geophysical Research, vol. 82, no. 27,
pp. 3843–3860, 1977.
[36] J. B. Anderson, S. Warny, R. A. Askin et al., “Progres-
sive Cenozoic cooling and the demise of Antarctica’s last
refugium,” Proceedings of the National Academy of Sciences
of the United States of America, vol. 108, no. 28, pp. 11356–
11360, 2011.
[37] E. M. van Zinderen Bakker and J. H. Mercer, “Major late cain-
ozoic climatic events and palaeoenvironmental changes in
Africa viewed in a world wide context,” Palaeo geography, Pal-
aeoclimatology, Palaeoecology, vol. 56, no. 3-4, pp. 217–235,
1986.
[38] J. H. Mercer, “Cenozoic glaciation in the southern hemi-
sphere,” Annual Review of Earth and Planetary Sciences, vol.
11, pp. 99–132, 1983.
[39] T. E. Cerling, J. G. Wynn, S. A. Andanje et al., “Woody
cover and hominin environments in the past 6-million years,”
Nature, vol. 476, no. 7358, pp. 51–56, 2011.
[40] T. E. Cerling, J. M. Harris, B. J. MacFadden et al., “Global
vegetation change through the Miocene/Pliocene boundary,”
Nature, vol. 389, no. 6647, pp. 153–158, 1997.
[41] P. Molnar, P. England, and J. Martinod, “Mantle dynamics,
uplift of the Tibetan Plateau, and the Indian monsoon,”
Reviews of Geophysics, vol. 31, no. 4, pp. 357–396, 1993.
[42] N. J. Shackleton and J. P. Kennett, “Paleotemperature history
of the Cenozoic and the initiation of Antarctic glaciation:
oxygen and carbon isotope analyses in DSDP Sites 277, 279,
and 281,” in Initial Reports of the Deep Sea Drilling Project,J.
P. Kennett and R. E. Houtz, Eds., vol. 29, pp. 743–755, U.S.
Government Printing Office, Washington, DC, USA, 1975.
[43] M. E. Raymo, B. Grant, M. Horowitz, and G. H. Rau, “Mid-
Pliocene warmth: stronger greenhouse and stronger con-
veyor,” Marine Micropaleontology, vol. 27, no. 1–4, pp. 313–
326, 1996.
[44] M. Pickford, “Uplift of the Roof of Africa and its bearing on
the evolution of mankind,” Human Evolution, vol. 5, no. 1,
pp. 1–20, 1990.
[45] S. LeRoy and L. Dupont, “Upper Pliocene history of the
Sahara by high resolution marine palynology; ODP Site 658,”
in Abstracts of the Proceedings of the Twenty-sixth Annual
Meeting of the American Association of Stratigraphic Palynol-
ogists, vol. 18, p. 252, American Association of Stratigraphic
Palynologists, Dallas, Tex, USA, 1994.
[46] A. M. Haywood, P. J. Valdes, and B. W. Sellwood, “Global
scale palaeoclimate reconstruction of the middle Pliocene
climate using the UKMO GCM: initial results,” Global and
Planetary Change, vol. 25, no. 3-4, pp. 239–256, 2000.
[47]A.S.Cohen,M.R.Talbot,S.M.Awramik,D.L.Dettman,
and P. Abell, “Lake level and paleoenvironmental history of
Lake Tanganyika, Africa, as inferred from late Holocene and
modern stromatolites,” Bulletin of the Geological Society of
America, vol. 109, no. 4, pp. 444–460, 1997.
[48] N. J. Shackleton, “New data on the evolution of Pliocene
climatic variability,” in Paleoclimate and Evolution: With an
Emphasis on Human Origins,E.Vrba,G.Denton,L.Burckle
et al., Eds., pp. 242–248, Yale University Press, 1995.
[49] A.C.Ravelo,D.H.Andreasen,M.Lyle,A.O.Lyle,andM.
W. Wara, “Regional climate shifts caused by gradual global
cooling in the Pliocene epoch,” Nature, vol. 429, no. 6989,
pp. 263–267, 2004.
[50] A. Meyer, “Phylogenetic relationships and evolutionary pro-
cesses in East African cichlid fishes,” Tr en ds i n Ec ol og y and
Evolution, vol. 8, no. 8, pp. 279–284, 1993.
[51] M. E. Raymo, “The initiation of Northern Hemisphere
glaciation,” Annual Review of Earth & Planetary Sciences, vol.
22, pp. 353–383, 1994.
[52] P. B. deMenocal, “African climate change and faunal evolu-
tion during the Pliocene-Pleistocene,” Earth and Planetary
Science Letters, vol. 220, no. 1-2, pp. 3–24, 2004.
[53] P. B. deMenocal, “Plio-Pleistocene African climate,” Science,
vol. 270, no. 5233, pp. 53–59, 1995.
[54] H. A. Bootsma and R. E. Hecky, “A comparative introduction
to the biology and limnology of the African Great Lakes,”
Journal of Great Lakes Research, vol. 29, no. 2, pp. 3–18, 2003.
[55] A. S. Cohen, M. J. Soreghan, and C. A. Scholz, “Estimating
the age of formation of lakes: an example from Lake
Tanganyika, East African Rift system,” Geology, vol. 21, no.
6, pp. 511–514, 1993.
[56] C. J. Ebinger, A. L. Deino, A. L. Tesha, T. Becker, and U.
Ring, “Tectonic controls on rift basin morphology: evolution
of the northern Malawi (Nyasa) Rift,” Journal of Geophysical
Research, vol. 98, no. B10, pp. 17821–17836, 1993.
[57] D. Delvau, “Age of Lake Malawi (Nyasa) and water level
fluctuations,” Mus´
ee Royal de l’Afrique Centrale Tervuren
(Belgium). D´
epartement de G´
eologie et Min´
eralogie. Rapport
Annuel, vol. 1993-1994, pp. 99–108, 1995.
[58] G. F. Turner, O. Seehausen, M. E. Knight, C. J. Allender, and
R. L. Robinson, “How many species of cichlid fishes are there
in African lakes?” Molecular Ecology, vol. 10, no. 3, pp. 793–
806, 2001.
[59] T. Takahashi, “Systematics of Tanganyikan cichlid fishes
(Teleostei: Perciformes),” Ichthyological Research, vol. 50, no.
4, pp. 367–382, 2003.

International Journal of Evolutionary Biology 17
[60] M. J. Genner and G. F. Turner, “Ancient hybridization and
phenotypic novelty within lake Malawi’s cichlid fish radia-
tion,” Molecular Biology and Evolution, vol. 29, no. 1, pp. 195–
206, 2012.
[61] M. H. Trauth, M. A. Maslin, A. Deino, and M. R. Strecker,
“Climate change: late cenozoic moisture history of east
Africa,” Science, vol. 309, no. 5743, pp. 2051–2053, 2005.
[62] R. Stein, “Late neogene changes of paleoclimate and pale-
oproductivity offnorthwest africa (D.S.D.P. Site 397),”
Palaeogeography, Palaeoclimatology, Palaeoecology, vol. 49, no.
1-2, pp. 47–59, 1985.
[63] L. Dupont and S. Leroy, “Steps towards drier climatic con-
ditions in Northwestern Africa during the Upper Pliocene,”
in Paleoclimate and Evolution: With Emphasis on Human
Origins, E. Vrba, G. Denton, T. Partridge et al., Eds., pp. 289–
297, Yale University Press, 1995.
[64] T.E.Cerling,J.R.Bowman,andJ.R.O’Neil,“Anisotopic
study of a fluvial-lacustrine sequence: the Plio-Pleistocene
koobi fora sequence, East Africa,” Palaeo geography, Palaeocli-
matology, Palaeoecology, vol. 63, no. 4, pp. 335–356, 1988.
[65] N. C. Sturchio, P. N. Dunkley, and M. Smith, “Climate-driven
variations in geothermal activity in the northern Kenya rift
valley,” Nature, vol. 362, no. 6417, pp. 233–234, 1993.
[66] J. H. F. Jansen, T. C. E. van Weering, R. Gieles, and J.
van Iperen, “Middle and late quaternary oceanography and
climatology of the Zaire-Congo fan and the adjacent Eastern
Angola basin,” Netherlands Journal of Sea Research, vol. 17,
no. 2–4, pp. 201–249, 1984.
[67] C. Hillaire-Marcel, O. Carro, and J. Casanova, “C-14 and
Th/U dating of Pleistocene and Holocene stromatolites from
East African paleolakes,” Quaternary Research, vol. 25, no. 3,
pp. 312–329, 1986.
[68] F. Gasse, V. L´
ed´
ee, M. Massault, and J. C. Fontes, “Water-
level fluctuations of Lake Tanganyika in phase with oceanic
changes during the last glaciation and deglaciation,” Nature,
vol. 342, no. 6245, pp. 57–59, 1989.
[69] P. B. deMenocal and D. Rind, “Sensitivity of Asian and
African climate to variations in seasonal insolation, glacial ice
cover, sea surface temperature, and Asian orography,” Journal
of Geophysical Research, vol. 98, no. 4, pp. 7265–7287, 1993.
[70] K. W. Butzer, F. W. Brown, and D. L. Thurher, “Horizontal
sediments of the lower Omo Valley. The Kibish Formation,”
Quaternaria, vol. 11, pp. 15–29, 1969.
[71] D. M. Anderson and W. L. Prell, “A 300 Kyr record of
upwelling offOman during the late Quaternary: evidence of
the Asian southwest monsoon,” Paleoceanography, vol. 8, no.
2, pp. 193–208, 1993.
[72] R. B. Owen, R. Crossley, T. C. Johnson et al., “Major low-
levels of Lake Malawi and their implications for speciation
rates in cichlid fishes,” Proceedings of the Royal Society B, vol.
240, no. 1299, pp. 519–553, 1990.
[73] J. S. Sparks and W. L. Smith, “Freshwater fishes, dispersal
ability, and nonevidence: “Gondwana life rafts” to the
rescue,” Systematic Biology, vol. 54, no. 1, pp. 158–165, 2005.
[74] I. P. Farias, G. Ort´
ı, and A. Meyer, “Total evidence: molecules,
morphology, and the phylogenetics of cichlid fishes,” Journal
of Experimental Zoology, vol. 288, no. 1, pp. 76–92, 2000.
[75] M. J. Genner, O. Seehausen, D. H. Lunt et al., “Age of cichlids:
new dates for ancient lake fish radiations,” Molecular Biology
and Evolution, vol. 24, no. 5, pp. 1269–1282, 2007.
[76] S. E. Nicholson, “The nature of rainfall variability over Africa
on time scales of decades to millenia,” Global and Planetary
Change, vol. 26, no. 1–3, pp. 137–158, 2000.
[77] P. D. Plisnier, D. Chitamwebwa, L. Mwape, K. Tshibangu,
V. Langenberg, and E. Coenen, “Limnological annual cycle
inferred from physical-chemical fluctuations at three stations
of Lake Tanganyika,” Hydrobiologia, vol. 407, pp. 45–58, 1999.
[78] G. W. Coulter and R. H. Spiegel, “Hydrodynamics,” in Lake
Tanganyika and Its Life,G.W.Coulter,Ed.,pp.49–75,Oxford
University Press, London, UK, 1991.
[79] S. Sander and B. R. Rosendahl, “The geometry of rifting in
Lake Tanganyika, East Africa,” Journal of African Earth Sci-
ences, vol. 8, no. 2–4, pp. 323–354, 1989.
[80] C. F. Burgess, The Structure and Stratigraphic Evolution of
Lake Tanganyika: A Case Study of Continental Rifting, 1985.
[81] D. J. Reynolds, Structural and Dimensional Repetition in Con-
tinental Rifts, Duke University, Department of Geology, 1984.
[82] R. L. Gawthorpe and M. R. Leeder, “Tectono-sedimentary
evolution of active extensional basins,” Basin Research, vol.
12, no. 3-4, pp. 195–218, 2000.
[83] J. J. Tiercelin and A. Mondeguer, “The geology of the Tan-
ganyika trough,” in Lake Tanganyika and Its Life,G.W.Coul-
ter, Ed., Oxford University Press, London, UK, 1991.
[84] K. E. Lezzar, J. J. Tiercelin, M. DeBatist et al., “New seis-
mic stratigraphy and Late Tertiary history of the North
Tanganyika Basin, East African Rift system, deduced from
multichannel and high-resolution reflection seismic data and
piston core evidence,” Basin Research, vol. 8, no. 1, pp. 1–28,
1996.
[85] C. A. Scholz and B. R. Rosendahl, “Low lake stands in Lakes
Malawi and Tanganyika, East Africa, delineated with multi-
fold seismic data,” Science, vol. 240, no. 4859, pp. 1645–1648,
1988.
[86] S. J. Feakins and P. B. demenocal, “Cenozoic mammals
of africa,” in Global and African Regional Climate Change
During the Cenozoic,L.WerdelinandW.J.Sanders,Eds.,pp.
45–55, University of California Press, 2010.
[87] J. E. Tierney, J. M. Russell, and Y. Huang, “A molecular per-
spective on Late Quaternary climate and vegetation change in
the Lake Tanganyika basin, East Africa,” Quaternary Science
Reviews, vol. 29, no. 5-6, pp. 787–800, 2010.
[88] J. Casanova and C. Hillaire-Marcel, “Late Holocene hydro-
logical history of Lake Tanganyika, East Africa, from isotopic
data on fossil stromatolites,” Palaeogeography, Palaeoclimatol-
ogy, Palaeoecology, vol. 91, no. 1-2, pp. 35–48, 1992.
[89] A. P. Burnett, M. J. Soreghan, C. A. Scholz, and E. T. Brown,
“Tropical East African climate change and its relation to
global climate: a record from Lake Tanganyika, Tropical East
Africa, over the past 90+kyr,” Palaeogeography, Palaeoclima-
tology, Palaeoecology, vol. 303, no. 1–4, pp. 155–167, 2011.
[90] J. Stankiewicz and M. J. de Wit, “A proposed drainage evo-
lution model for Central Africa—did the Congo flow east?”
Journal of African Earth Sciences, vol. 44, no. 1, pp. 75–84,
2006.
[91] C. J. Ebinger, “Geometric and kinematic development of
border faults and accommodation zones, Kivu-Rusizi rift,
Africa,” Tectonics, vol. 8, no. 1, pp. 117–133, 1989.
[92] P. Stoffers and R. E. Hecky, “Late Pleistocene Holocene Evo-
lution of the Kivu-Tanganyika Basin,” in Modern and Ancient
Lake Sediments, pp. 43–55, Blackwell Publishing, 1978.
[93] A. A. Felton, J. M. Russell, A. S. Cohen et al., “Paleolimnolog-
ical evidence for the onset and termination of glacial aridity
from Lake Tanganyika, Tropical East Africa,” Palaeogeogra-
phy, Palaeoclimatology, Palaeoecology, vol. 252, no. 3-4, pp.
405–423, 2007.

18 International Journal of Evolutionary Biology
[94] K. W. Butzer, C. Washbourn-Kamau, J. L. Richardson, and
G. L. Isaac, “Radiocarbon dating of East African lake levels,”
Science, vol. 175, no. 4026, pp. 1069–1076, 1972.
[95] H. H. Lamb, “Climate in the 1960’s changes in the world’s
wind circulation reflected in prevailing temperatures, rainfall
patterns and the levels of the African lakes,” The Geographical
Journal, vol. 132, no. 2, pp. 183–212, 1966.
[96] R. H. Lowe-McConnell, “Fish faunas of the African Great
Lakes: origins, diversity, and vulnerability,” Conservation
Biology, vol. 7, no. 3, pp. 634–643, 1993.
[97] M. Poll, “Classification des cichlidae du lac Tanganika. Tibus,
genres, et aspeces,” Academie Royale de Belgique Mem. Classe
des Sciences M´
emoires, vol. 45, no. 2, pp. 1–163, 1986.
[98] A. Rossiter, “The cichlid fish assemblages of lake Tanganyika:
ecology, behaviour and evolution of its species flocks,” in
Advances in Ecological Research,M.BegonandA.H.Fitter,
Eds., pp. 187–252, Academic Press, 1995.
[99] C. Sturmbauer, M. Husemann, and P. D. Danley, “Explosive
speciation and adaptive radiation of East African Cichlid
Fishes,” in Biodiversity Hotspots: Distribution and Protection
of Conservation Priority Areas,F.E.ZachosandJ.C.Habel,
Eds., pp. 333–362, Springer, 2011.
[100] J. Schwarzer, B. Misof, D. Tautz, and U. K. Schliewen,
“The root of the East African cichlid radiations,” BMC
Evolutionary Biology, vol. 9, no. 1, article 186, 2009.
[101] J. Schwarzer, B. Misof, S. N. Ifuta, and U. K. Schliewen, “Time
and origin of cichlid colonization of the lower Congo rapids,”
PLoS ONE, vol. 6, no. 7, Article ID e22380, 2011.
[102] V. Klett and A. Meyer, “What, if anything, is a Tilapia?—
mitochondrial ND2 phylogeny of tilapiines and the evolution
of parental care systems in the African cichlid fishes,”
Molecular Biology and Evolution, vol. 19, no. 6, pp. 865–883,
2002.
[103] M. Koch, S. Koblm ¨
uller, K. M. Sefc, N. Duftner, C. Katongo,
and C. Sturmbauer, “Evolutionary history of the endemic
Lake Tanganyika cichlid fish Tylochromis polylepis: a recent
intruder to a mature adaptive radiation,” Journal of Zoological
Systematics and Evolutionary Research, vol. 45, no. 1, pp. 64–
71, 2007.
[104] F. Rodr´
ıguez-Trelles, R. Tarr´
ıo, and F. J. Ayala, “A method-
ological bias toward overestimation of molecular evolution-
ary time scales,” Proceedings of the National Academy of
Sciences of the United States of America, vol. 99, no. 12, pp.
8112–8115, 2002.
[105] S. Koblm¨
uller, U. K. Schliewen, N. Duftner, K. M. Sefc, C.
Katongo, and C. Sturmbauer, “Age and spread of the hap-
lochromine cichlid fishes in Africa,” Molecular Phylogenetics
and Evolution, vol. 49, no. 1, pp. 153–169, 2008.
[106] A. S. Cohen, “Scientific drilling and biological evolution in
ancient lakes: lessons learned and recommendations for the
future,” Hydrobiologia, vol. 682, no. 1, pp. 3–25, 2012.
[107] K. L. Sanders and M. S. Y. Lee, “Evaluating molecular
clock calibrations using Bayesian analyses with soft and hard
bounds,” Biology Letters, vol. 3, no. 3, pp. 275–279, 2007.
[108] R. C. M. Warnock, Z. Yang, and P. C. J. Donoghue,
“Exploring uncertainty in the calibration of the molecular
clock,” Biology Letters, vol. 8, no. 1, pp. 156–159, 2012.
[109] P. C. J. Donoghue and M. J. Benton, “Rocks and clocks:
calibrating the Tree of Life using fossils and molecules,”
Trends in Ecology and Evolution, vol. 22, no. 8, pp. 424–431,
2007.
[110] V. Lukoschek, J. Scott Keogh, and J. C. Avise, “Evaluating
fossil calibrations for dating phylogenies in light of rates
of molecular evolution: a comparison of three approaches,”
Systematic Biology, vol. 61, no. 1, pp. 22–43, 2012.
[111] C. Sturmbauer, S. Baric, W. Salzburger, L. R¨
uber, and
E. Verheyen, “Lake level fluctuations synchronize genetic
divergences of cichlid fishes in African Lakes,” Molecular
Biology and Evolution, vol. 18, no. 2, pp. 144–154, 2001.
[112] S. Koblm˜
aller, W. Salzburger, B. Oberm˜
aller, E. Eigner, C.
Sturmbauer, and K. M. Sefc, “Separated by sand, fused by
dropping water: habitat barriers and fluctuating water levels
steer the evolution of rock-dwelling cichlid populations in
Lake Tanganyika,” Molecular Ecology, vol. 20, no. 11, pp.
2272–2290, 2011.
[113] J. W. Flannery and B. R. Rosendahl, “The seismic stratigraphy
of Lake Malawi, Africa: implications for interpreting geo-
logical processes in lacustrine rifts,” Journal of African Earth
Sciences, vol. 10, no. 3, pp. 519–548, 1990.
[114] C. J. Ebinger, B. R. Rosendahl, and D. J. Reynolds, “Tectonic
model of the Mala ˆ
wi rift, Africa,” Tecton op hy sic s, vol. 141, no.
1–3, pp. 215–235, 1987.
[115] C. J. Ebinger, M. J. Crow, B. R. Rosendahl, D. A. Livingstone,
and J. Lefournier, “Structural evolution of Lake Mala ˆ
wi,
Africa,” Nature, vol. 308, no. 5960, pp. 627–629, 1984.
[116] T. D. Specht and B. R. Rosendahl, “Architecture of the Lake
Malawi Rift, East Africa,” Journal of African Earth Sciences,
vol. 8, no. 2–4, pp. 355–382, 1989.
[117] E. Mortimer, D. A. Paton, C. A. Scholz, M. R. Strecker, and
P. Blisniuk, “Orthogonal to oblique rifting: effect of rift basin
orientation in the evolution of the North basin, Malawi Rift,
East Africa,” Basin Research, vol. 19, no. 3, pp. 393–407, 2007.
[118] L. C. Beadle, The Inland Waters of Tropical Africa. An Intro-
duction to Tropical Limnology, Longman Group, London, UK,
1981.
[119] C. H. R. Kidd, “A water resources evaluation of Lake Malawi
and the Shire River,” UNDP Project MLW/77/012, World
Meteorological Organization, Geneva, Switzerland, 1983.
[120] G. Patterson and O. Kachinjika, Limnology and Phytoplankton
Ecology, edited by A. Menz, Natural Resources Institute, 1995.
[121] C. A. Scholz, “Deltas of the Lake Malawi Rift, East Africa:
seismic expression and exploration implications,” American
Association of Petroleum Geologists Bulletin, vol. 79, no. 11,
pp. 1679–1697, 1995.
[122] R. S. Drayton, “Variations in the level of Lake Malawi,”
Hydrological Sciences Journal, vol. 29, no. 1, pp. 1–12, 1984.
[123] M. J. Kingdon, H. A. Bootsma, J. Mwita et al., River Discharge
and Water Quality, Malawi, 1999.
[124] T. C. Johnson and P. Ng’ang’a, “Reflections on a rift lake,”
in Lacustrine Basin Exploration—Case Studies and Modern
Analogs, B. J. Katz, Ed., pp. 113–135, American Association
of Petroleum Geologists, 1990.
[125] C. A. Scholz, T. C. Johnson, and J. W. McGill, “Deltaic
sedimentation in a rift valley lake: new seismic reflection data
from Lake Malawi (Nyasa), East Africa,” Geology, vol. 21, no.
5, pp. 395–398, 1993.
[126] M. J. Soreghan, C. A. Scholz, and J. T. Wells, “Coarse-grained,
deep-water sedimentation along a border fault margin of
Lake Malawi, Africa; seismic stratigraphic analysis,” Journal
of Sedimentary Research, vol. 69, no. 4, pp. 832–846, 1999.
[127] D. Delvaux, K. Levi, R. Kajara, and J. Sarota, “Cenozoic
paleostress and kinematic evolution of the Rukwa-North
Malawi Rift Valley (East African Rift System),” Bulletin des
Centres de Recherche Exploration-Production Elf-Aquitaine,
vol. 16, no. 2, pp. 383–406, 1992.

International Journal of Evolutionary Biology 19
[128] R. Crossley, “Controls of sedimentation in the Malawi rift
valley, Central Africa,” Sedimentary Geology, vol. 40, no. 1–
3, pp. 33–50, 1984.
[129] R. Crossley and M. J. Crow, “The Malawi rift,” in Geodynamic
Evolution of the Afro-Arabian Rift System,A.Carelli,Ed.,pp.
78–87, Accademia Nazionale dei Lincei, 1980.
[130] P. K. Sodsuk, B. J. McAndrew, and G. F. Turner, “Evolutionary
relationships of the Lake Malawi Oreochromis species:
evidence from allozymes,” Journal of Fish Biology, vol. 47, no.
2, pp. 321–333, 1995.
[131] D. A. Joyce, D. H. Lunt, M. J. Genner, G. F. Turner, R. Bills,
and O. Seehausen, “Repeated colonization and hybridization
in Lake Malawi cichlids,” Current Biology,vol.21,no.3,pp.
R108–R109, 2011.
[132] R. C. Albertson, J. A. Markert, P. D. Danley, and T. D. Kocher,
“Phytogeny of a rapidly evolving clade: the cichlid fishes
of Lake Malawi, East Africa,” Proceedings of the National
Academy of Sciences of the United States of America, vol. 96,
no. 9, pp. 5107–5110, 1999.
[133] M. J. Genner and G. F. Turner, “Ancient hybridization and
phenotypic novelty within lake Malawi’s cichlid fish radia-
tion,” Molecular Biology and Evolution, vol. 29, no. 1, pp. 195–
206, 2012.
[134] M. J. Genner, M. E. Knight, M. P. Haesler, and G. F. Turner,
“Establishment and expansion of Lake Malawi rock fish
populations after a dramatic Late Pleistocene lake level rise,”
Molecular Ecology, vol. 19, no. 1, pp. 170–182, 2010.
[135] A. J. Ribbink, B. A. Marsh, A. C. Marsh, A. C. Ribbink, and B.
J. Sharp, “A preliminary survey of the cichlid fishes of rocky
habitats in Lake Malawi,” South African Journal of Zoology,
vol. 18, no. 3, pp. 149–310, 1983.
[136] K. R. Elmer, C. Reggio, T. Wirth, E. Verheyen, W. Salzburger,
and A. Meyer, “Pleistocene desiccation in East Africa bottle-
necked but did not extirpate the adaptive radiation of Lake
Victoria haplochromine cichlid fishes,” Proceedings of the
National Academy of Sciences of the United States of America,
vol. 106, no. 32, pp. 13404–13409, 2009.
[137] A. Konings, Malawi Cichlids in Their Natural Habitat, Cichlid
Press, 4th edition, 2007.
[138] J. R. Stauffer,N.J.Bowers,K.A.Kellogg,andK.R.Mckaye,
“A revision of the blue-black Pseudotropheus zebra (Tele-
ostei: Cichlidae) complex from Lake Mala ˆ
wi, Africa, with a
description of a new genus and ten new species,” Proceedings
of the Academy of Natural Sciences of Philadelphia, vol. 148,
pp. 189–230, 1997.
[139] K. A. Young, J. Snoeks, and O. Seehausen, “Morphological
diversity and the roles of contingency, chance and determin-
ism in African cichlid radiations,” PLoS ONE,vol.4,no.3,
Article ID e4740, 2009.
[140] Y. Song, F. H. M. Semazzi, L. Xie, and L. J. Ogallo, “A coupled
regional climate model for the Lake Victoria Basin of East
Africa,” International Journal of Climatology, vol. 24, no. 1,
pp. 57–75, 2004.
[141] R. C. M. Crul, Limnology and Hydrology of Lake Victoria,
UNESCO Publishing, 1995.
[142] J. F. Talling, “The incidence of vertical mixing, and some
biological and chemical consequences in tropical African
lakes,” Verhandlungen der Internationalen Vereinigung f¨
ur the-
oretische und angewandte Limnologie, vol. 17, pp. 998–1012,
1969.
[143] J. C. Stager and T. C. Johnson, “The late Pleistocene desic-
cation of Lake Victoria and the origin of its endemic biota,”
Hydrobiologia, vol. 596, no. 1, pp. 5–16, 2008.
[144] B. S. Piper, D. T. Plinston, and J. V. Sutcliffe, “The water
balance of Lake Victoria,” Hydrological Sciences Journal, vol.
31, no. 1, pp. 25–37, 1986.
[145] W. S. Broecker, D. Peteet, I. Hajdas, J. Lin, and E. Clark, “Anti-
phasing between rainfall in Africa’s Rift Valley and North
America’s Great Basin,” Quaternary Research, vol. 50, no. 1,
pp. 12–20, 1998.
[146] C. D. Ollier, “Morphotectonics of the Lake Albert Rift Valley
and its significance for continental margins,” Journal of Geo-
dynamics, vol. 11, no. 4, pp. 343–355, 1990.
[147] R. M. Shackleton, “A contributon to the geology of the Kavi-
rondon Rift Valley,” Quarterly Journal of the Geological Soci-
ety, vol. 106, no. 1–4, pp. 345–392, 1950.
[148] W. W. Bishop, Pleistocene Stratigraphy in Uganda: Geological
Survey of Uganda, 1969.
[149] M. A. J. Williams, D. Adamson, J. R. Prescott, and F. M. Willi-
ams, “New light on the age of the White Nile,” Geology, vol.
31, no. 11, pp. 1001–1004, 2003.
[150] S. W. Buol, R. J. Southard, R. C. Graham et al., “Vertisols:
shrinking and swelling dark clay soils,” in Soil Genesis and
Classification, pp. 385–395, Wiley-Blackwell, 2011.
[151] K. R. M. Beuning, M. R. Talbot, and K. Kelts, “A revised
30,000-year paleoclimatic and paleohydrologic history of
Lake Albert, East Africa,” Palaeogeography, Palaeoclimatology,
Palaeoecology, vol. 136, no. 1–4, pp. 259–279, 1997.
[152] J. W. H. Weijers, E. Schefuß, S. Schouten, and J. S. S. Damst´
e,
“Coupled thermal and hydrological evolution of tropical
Africa over the last deglaciation,” Science, vol. 315, no. 5819,
pp. 1701–1704, 2007.
[153] R. Bonnefille and F. Chali´
e, “Pollen-inferred precipitation
time-series from equatorial mountains, Africa, the last 40 kyr
BP,” Global and Planetary Change, vol. 26, no. 1–3, pp. 25–50,
2000.
[154] R. L. Kendall, “An ecological history of the lake victoria
basin,” Ecological Monographs, vol. 39, no. 2, pp. 121–176,
1969.
[155] J. C. Stager, J. Westwood, D. Grzesik, and B. F. Cumming, “A
5500-year environmental history of Lake Nabugabo, Ugan-
da,” Palaeogeography, Palaeoclimatology, Palaeoecology, vol.
218, no. 3-4, pp. 347–354, 2005.
[156] J. C. Stager and T. C. Johnson, “A 12,400 14C yr offshore
diatom record from east central Lake Victoria, East Africa,”
Journal of Paleolimnology, vol. 23, no. 4, pp. 373–383, 2000.
[157] J. C. Stager, B. F. Cumming, and L. D. Meeker, “A 10,000-year
high-resolution diatom record from Pilkington Bay, Lake
Victoria, East Africa,” Quaternary Research,vol.59,no.2,pp.
172–181, 2003.
[158] L. Kaufman, “Asynchronous taxon cycles in haplochromine
fishes of the greater Lake Victoria Region,” South African
Journal of Science, vol. 93, no. 11-12, pp. 601–606, 1997.
[159] A. Meyer, T. D. Kocher, P. Basasibwaki, and A. C. Wilson,
“Monophyletic origin of Lake Victoria cichlid fishes sug-
gested by mitochondrial DNA sequences,” Nature, vol. 347,
no. 6293, pp. 550–553, 1990.
[160] J. Rutaisire, A. J. Booth, C. Masembe, S. Nyakaana, and V.
B. Muwanika, “Evolution of Labeo victorianus predates the
Pleistocene desiccation of Lake Victoria: evidence from mito-
chondrial DNA sequence variation,” South African Journal of
Science, vol. 100, no. 11-12, pp. 607–608, 2004.
[161] C. J. Mwita and G. Nkwengulila, “Molecular phylogeny of
the clariid fishes of Lake Victoria, Tanzania, inferred from
cytochrome b DNA sequences,” Journal of Fish Biology, vol.
73, no. 5, pp. 1139–1148, 2008.

20 International Journal of Evolutionary Biology
[162] A. JØrgensen, T. K. Kristensen, and J. R. Stothard, “Phylogeny
and biogeography of African Biomphalaria (Gastropoda:
Planorbidae), with emphasis on endemic species of the great
East African lakes,” Zoological Journal of the Linnean Society,
vol. 151, no. 2, pp. 337–349, 2007.
[163] M. E. Sengupta, T. K. Kristensen, H. Madsen, and A.
Jørgensen, “Molecular phylogenetic investigations of the Vi-
viparidae (Gastropoda: Caenogastropoda) in the lakes of
the Rift Valley area of Africa,” Molecular Phylogenetics and
Evolution, vol. 53, no. 3, pp. 797–805, 2009.
[164] G. Fryer, “Biological implications of a suggested Late Pleis-
tocene desiccation of Lake Victoria,” Hydrobiologia, vol. 354,
no. 1–3, pp. 177–182, 1997.
[165] G. Fryer, “On the age and origin of the species flock of
haplochromine cichlid fishes of Lake Victoria,” Proceedings of
the Royal Society B, vol. 268, no. 1472, pp. 1147–1152, 2001.
[166] O. Seehausen, “Patterns in fish radiation are compatible with
Pleistocene desiccation of Lake Victoria and 14 600 year
history for its cichlid species flock,” Proceedings of the Royal
Society B, vol. 269, no. 1490, pp. 491–497, 2002.
[167] O. Seehausen, “Hybridization and adaptive radiation,” Tr en ds
in Ecology and Evolution, vol. 19, no. 4, pp. 198–207, 2004.
[168] S. Koblm¨
uller, B. Egger, C. Sturmbauer, and K. M. Sefc,
“Rapid radiation, ancient incomplete lineage sorting and
ancient hybridization in the endemic Lake Tanganyika cichlid
tribe Tropheini,” Molecular Phylogenetics and Evolution, vol.
55, no. 1, pp. 318–334, 2010.
[169] E. Bezault, S. Mwaiko, and O. Seehausen, “Population geno-
mic tests of models of adaptive radiation in Lake Victoria
region cichlid fish,” Evolution, vol. 65, no. 12, pp. 3381–3397,
2011.
[170] L. S. Kaufman, L. J. Chapman, and C. A. Chapman, “Evo-
lution in fast forward: haplochromine fishes of the Lake
Victoria region,” Endeavour, vol. 21, no. 1, pp. 23–30, 1997.
[171] O. Seehausen, E. Koetsier, M. V. Schneider et al., “Nuclear
markers reveal unexpected genetic variation and a Congo-
lese-Nilotic origin of the Lake Victoria cichlid species flock,”
Proceedings of the Royal Society B, vol. 270, no. 1533, pp.
2637–2638, 2003.
[172] D. A. Joyce, D. H. Lunt, R. Bills et al., “An extant cichlid fish
radiation emerged in an extinct Pleistocene lake,” Nature, vol.
435, no. 7038, pp. 90–95, 2005.
[173] N. D. Burgess, J. Fjelds ˚
a, and R. Botterweg, “Faunal impor-
tance of the eastern arc mountains of Kenya and Tanzania,”
Journal of East African Natural History, vol. 87, no. 1, pp. 37–
58, 1998.
[174] J. Snoeks, The Haplochromines (Teleostei, Cichlidae) of Lake
Kivu (East Africa): A Taxonomic Revision with Notes on Their
Ecology: Koninklijk Museum voor Midden-Afrika, 1994.
[175] E. Lippitsch, “Phylogenetic investigations on the hap-
lochromine cichlidae of Lake Kivu (East Africa), based on
lepidological characters,” Journal of Fish Biology, vol. 51, no.
2, pp. 284–299, 1997.
[176] H. J. Dumont, The Nile: Origin, Environments, Limnology and
Human Use, Springer, 2009.
[177] M. B. Bush, “Amazonian speciation: a necessarily complex
model,” Journal of Biogeography, vol. 21, no. 1, pp. 5–17, 1994.
[178] G. L. Stebbins, Flowering Plants: Evolution above the Species
Level, Belknap Press of Harvard University Press, 1974.
[179] D. Jablonski, K. Roy, and J. W. Valentine, “Out of the tropics:
evolutionary dynamics of the latitudinal diversity gradient,”
Science, vol. 314, no. 5796, pp. 102–106, 2006.
[180] D. D. McKenna and B. D. Farrell, “Tropical forests are both
evolutionary cradles and museums of leaf beetle diversity,”
Proceedings of the National Academy of Sciences of the United
States of America, vol. 103, no. 29, pp. 10947–10951, 2006.