*Department of Zoology and Limnology, University of Innsbruck, Austria;
National Museum of Natural History, Madrid, Spain; and
Section of Taxonomy and Biochemical Systematics, Department of Vertebrates, Royal Belgian Institute of Natural Sciences, Brussels, Belgium
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Abstract |
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Introduction |
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The age of a species flock may not correspond to the geological age of a lake, since climatic or geological events may have caused a temporary dry-up, such that preexisting species flocks may have gone extinct. Moreover, it was also shown by recent molecular studies that the dynamics of diversification events in African cichlid fishes are likely to be connected to fluctuations in the lake level (Sturmbauer and Meyer 1992
; Johnson et al. 1996
; Sturmbauer et al. 1997
; Rüber et al. 1998
; Nagl et al. 2000
). The evolutionary consequences of such severe environmental changes are well known for European terrestrial faunas (Hewitt 1996
) but are much less understood for tropical ecosystems. Lakes Malawi and Tanganyika were severely affected by the change to a drier climate in the late Pliocene/early Pleistocene, resulting in a drop of the lake level by 650700 m about 1.1 MYA in Lake Tanganyika (Lezzar et al. 1996
; Cohen et al. 1997
) and an almost complete dry-up of Lake Malawi from 1.6 MYA until 1.00.57 MYA (Delvaux 1995
). After that minimum, both lakes rose until about 400,000 years ago. New regressions started about 390,000 years ago in Lake Tanganyika (Cohen et al. 1997
) and 420,000 years ago in Lake Malawi (Delvaux 1995
), followed by a period of fluctuating lake level in both lakes. In Lake Tanganyika, the minima were dated at 390,000360,000 years ago, 290,000260,000 years ago, and 190,000170,000 years ago; those of Lake Malawi were not precisely dated by Delvaux (1995). Lake Tanganyika rose to its present level 170,00040,000 years ago, and the rise of Lake Malawi to its present level was estimated at about 250,000120,000 years ago. Concerning their most recent history, several studies agree that the lake levels of all three lakes were substantially lower during the late Pleistocene ice ages, when the climate in much of north and equatorial Africa became progressively more arid. Two recent studies carried out in the north part of Lake Tanganyika demonstrated three periods of low lake level for Lake Tanganyika in its recent past, the first 40,00035,000 years ago, the second 23,000 years ago, and the third 18,000 years ago (Lezzar et al. 1996
; Cohen et al. 1997
). The lowstands at 23,000 and 18,000 years ago were also found in a sediment study in the very south part of the lake by Gasse et al. (1989)
. A minimum water level of about 400 m below the present level was reached 18,000 years ago, and the lake was lower until 13,000 years ago abruptly rising in two steps 13,000 and 10,600 years ago (Gasse et al. 1989
). An earlier study tentatively dated the latest major lowstand for Lakes Malawi (250500 m) and Tanganyika (600 m) at about 25,000 years ago (Scholz and Rosendahl 1988
; C. A. Scholz, personal communication). This age estimate has been obtained by extrapolating sedimentation rates and may correspond to the minimum at 18,000 years ago found in the more recent studies (Gasse et al. 1989
; Lezzar et al. 1996
; Cohen et al. 1997
). As suggested for Lake Tanganyika, Lake Malawi was also at least 400 m lower 18,00010,700 years ago (Brooks and Robertshaw 1990
; Owen et al. 1990
; Finney and Johnson 1991
), and seismic reflection profile and piston core analyses from Lake Victoria suggest that Lake Victoria was (almost) dry from 17,300 years ago until 12,400 years ago (Johnson et al. 1996
; see also and Stager, Reinthal, and Livingstone 1986
; Talbot and Livingstone 1989). In summary, the lake levels of all three Great East African Lakes seem to have been influenced in a similar way by the same global climatic changes. They were generally low 18,00012,000 years ago, quickly rising to present levels with few and less severe fluctuations, with a maximum of 150 m in the Holocene and in historic times (Owen et al. 1990
).
In order to compare the evolutionary consequences of the most recent minima of the lake levels on the cichlid faunas of Lakes Tanganyika, Malawi, and Victoria, we investigated the geographic distribution of closely related genotypes. Therefore, we selected species and populations of littoral cichlid fishes in each of the three lakes that have been shown to be weak dispersers and thus likely to be greatly affected by lake level changes (Meyer et al. 1990
; Sturmbauer and Meyer 1992
; Moran and Kornfield 1993
; Verheyen et al. 1996
; Sturmbauer et al. 1997
; van Oppen et al. 1997
; Albertson et al. 1999
; Arnegard et al. 1999
; Markert et al. 1999). The samples included in our study were chosen according to the basin structure of the lakes. Our approach was based on the observation that lake level fluctuations temporarily form or break down barriers among habitats and thus either promote or prevent gene flow among adjacent populations and/or incipient species (Sturmbauer 1998
). The degree of habitat change enforced by water level fluctuations may range from small-scale effects to major vicariant events that affect species communities in most habitats. Any drop in the lake level will establish secondary contact and admixis among previously isolated populations in shallow regions of a lake, leading to an increase in genetic diversity in admixed populations. A rise in the lake level may promote population subdivision due to the colonization of new habitats. Newly formed ecological barriers interrupt gene flow, such that genetic differences can accumulate independently and lineage sorting can proceed. Populations of cichlid fishes specialized to particular habitats such as rocks in the littoral zone are likely to become isolated to a higher degree than less stenotopic and thus more mobile species. Only populations that have become isolated in the very recent past should share identical or closely related haplotypes, even if they are now separated by long distances or are situated on opposite shores. When the time of divergence between two populations is short, not many new mutations arise and lineage sorting is likely to be incomplete. In this case, any individual sampled from one population is expected to be as similar to individuals from different populations that were formed by the same founder event as it is to some individuals sampled from its own population. Any set of genetically heterogeneous populations is expected to contain several clusters of equally closely related genotypes, since lineage sorting is likely to be incomplete, as long as the number of generations after the split is equal to or less than twice the population size (Tajima 1983
).
It is important to note that our approach is not affected by ancient DNA sequence polymorphisms due to recent speciation events, because only gene trees referring to the geographic distribution of genotypes are used to derive relative time estimates for allopatric divergence. While most rock-dwelling cichlid species of Lake Tanganyika are easily distinguishable by means of mtDNA sequences, and incipient speciation mostly proceeds in absence of ecomorphological innovation, species of Lakes Victoria and Malawi are much younger and still tend to share mitochondrial haplotypes, even if they sometimes differ dramatically in terms of their trophic morphologies and are placed in different genera (Greenwood 1980, 1984
; Eccles and Trewavas 1989
; Meyer et al. 1990
; Moran and Kornfield 1993
; Kornfield and Parker 1997
; Parker and Kornfield 1997
; Nagl et al. 2000
). Thus, mtDNA-based phylogenies still represent gene trees and not species trees for Lake Victoria and Lake Malawi cichlids. Recent studies using more variable genetic markers or behavioral data, however, showed that these young species are genetically distinct and have evolved complete prezygotic isolation (Seehausen, van Alphen, and Witte 1997
; Seehausen and van Alphen 1998
; van Oppen et al. 1998, 2000
; Knight et al. 1999
).
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Materials and Methods |
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An absolute age estimate was attempted by calibrating the molecular divergences by a new age estimate for Lake Malawi using average genetic divergences of two basal lineages of the Lake Malawi cichlid species flock. The geological history of the Lake Malawi basin is complex, so the age of the lacustrine habitat can only be dated in the form of a minimum-maximum estimate. While the geological age is assumed to be 45 Myr, the lake was most likely almost or completely dry for several thousands of years in the late Pleistocene from 1.6 MYA until maximally 1 MYA and minimally 570,000 years ago. We thus estimated the age of its species flock to be between 570,000 years and 1 Myr (Delvaux 1995
), assuming that the emergence of the ecological diversity of Lake Malawi cichlids did not predate this period, because most suitable lacustrine habitats were lacking in a shallow and swampy lake.
To calibrate the mutation rate of the 359-bp segment of the control region, we calculated the average genetic distance among two ancient Lake Malawi cichlid lineages (Meyer et al. 1990
). We compared published DNA sequences of 26 mbuna (Kocher et al. 1993
; Bowers, Stauffer, and Kocher 1994
; Parker and Kornfield 1997
), 13 utaka (Meyer et al. 1990
; Lee et al. 1995
; Parker and Kornfield 1997
), and five additional species sequenced by us for this study: Aulonocara jacobfreibergi, Fossorchromis rostratus, Melanochromis caeruleus yellow, Nimbochromis livingstoni, and Nimbochromis venustus (table 1
). After performing a relative-rate test (Takezaki, Rzhetsky, and Nei 1995
), average pairwise Kimura distances were calculated among all taxa of each lineage. Two mbuna sequences and three utaka sequences were excluded because of different substitution rates.
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Results and Discussion |
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The DNA sequences of Lake Victoria haplochromines from seven localities in the lake and four localities from surrounding rivers and lakes contained 4 out of 38 haplotypes that were shared by up to eight species originating from opposite sides of the lake, again defining geographically informative clusters of genotypes (average genetic distance = 1.33 base substitutions; SD = 0.97; 212 pairwise comparisons; see fig. 3 and table 2 ).
The presence of individuals having identical or very closely related mitochondrial haplotypes at distant localities in all three lakes, together with the remarkable degree of genetic heterogeneity found in many populations, consistently indicates an event of secondary admixis of previously isolated populations in the very recent past, followed by a range expansion. In each of the three lakes, this event was triggered by a major fluctuation of the lake level. Even though base substitutions occur stochastically, they can be taken as measures of divergence time when three criteria are met. First, all taxa have similar rates of base substitution in the analyzed gene segment. Second, the stochastic variation of mutation rates among individuals is homogenized by averaging multiple pairwise comparisons of taxa. Third, incomplete lineage sorting must be taken into account by comparing those individuals from a given population only to their counterparts from another population that are direct descendants of the same ancestral mitochondrial haplotype. All haplotype clusters that have diverged after the most recent admixis thus exhibit similar levels of genetic variation.
The strikingly similar average numbers of base substitutions in all phylogeographically informative haplotype clusters suggest that the latest periods of low lake level in Lakes Tanganyika, Malawi, and Victoria happened, or at least ended, roughly at the same time. The finding of identical genotypes of Tropheus at opposite shores in the central region of Lake Tanganyika (fig. 1A and B ) suggests a retreat of the lake level by a minimum of 550 m, which would be sufficient to shift a continuous band of rock bottom into the depth limit of Tropheus (about 50 m). The distribution of identical or very closely related genotypes in Lake Malawi, and particularly their occurrence at the edge of the deep basin at locality 1 (fig. 2 ), suggests a retreat of about 500 m, but certainly more than 400 m, below its present level.
Since all data sets were found to have similar evolutionary rates in the analyzed segment of the control region, the inference of relative age estimates seems justified. The published rate estimates for the control region on various organisms differ widely (Vigilant et al. 1991
; Quinn 1992
; Brown, Beckenbach, and Smith 1993
; Stewart and Baker 1994
). Since no calibration of the evolutionary rate was available for cichlid fishes, we used new evidence for the history of Lake Malawi (Delvaux 1995
) and the average genetic distance among two ancestral lineages of Lake Malawi cichlids to derive a rate estimate. Among 25 mbuna and 14 utaka haplotypes (350 pairwise comparisons), an average Kimura distance of 6.54% (SD = 0.98%) was found. Our rate estimate for the most variable section of the control region thus amounts to 6.5%8.8% per Myr, depending on which age is assumed for the Lake Malawi lacustrine ecosystem (fig. 4 ). The highly similar average genetic distances within clusters of closely related genotypes in cichlids of all three lakes (Lake Tanganyika, 1.33 mutations, 0.37%; Lake Malawi, 1.27 mutations, 0.35%; Lake Victoria, 1.33 mutations, 0.37%) would translate into an age range of between 57,000 and 40,000 years. This estimate would fit to a period of moderately low lake level (-160 m) in Lake Tanganyika 40,00035,000 years ago (Lezzar et al. 1996
; Cohen et al. 1997
) but is older than the dating of the most recent period of very low lake level in all three lakes (18,00012,000 years ago). This discrepancy may be due to the still relatively imprecise age estimate for Lake Malawi. Alternatively, it was repeatedly shown that mtDNA mutation rates seem faster when studied over relatively few generations, due to rapid accumulation of mutations at hypervariable sites. These mutation hot spots rapidly saturate after short periods of divergence, or genotypes may be quickly removed from populations due to selection against slightly deleterious mutations (Parsons et al. 1997
; Gibbons 1998
). We thus feel that the time estimate for the latest major dispersal event between 40,000 and 57,000 years ago is likely to be too old. To us, the most likely time for an almost synchronous spread in all three lakes would be their rise dated about 11,000 years ago by geological and sedimentological evidence, because the drop in the lake level 40,00035,000 years ago was not sufficiently large to allow for crossing of the lake at the central basin by individuals of Tropheus (Gasse et al. 1989
; Owen et al. 1990
; Finney and Johnson 1991
; Johnson et al. 1996
; Lezzar et al. 1996
; Cohen et al. 1997
). The fluctuation of Lake Malawi over, at most, 150 m between a.d. 1500 and a.d. 1840 (Owen et al. 1990
; but see Nicholson 1998
) is not likely to have resulted in the observed pattern of genotype distribution, because this would have not fused all studied populations.
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Acknowledgements |
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Footnotes |
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1 Keywords: mtDNA sequences
adaptive radiation
Lake Tanganyika
Lake Malawi
Lake Victoria
2 Address for correspondence and reprints: Christian Sturmbauer, Department of Zoology and Limnology, University of Innsbruck, Technikerstrasse 25, A-6020 Innsbruck, Austria. E-mail: christian.sturmbauer{at}uibk.ac.at
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