Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes - PubMed (original) (raw)
Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes
Walter Salzburger et al. BMC Evol Biol. 2005.
Abstract
Background: The adaptive radiations of cichlid fishes in East Africa are well known for their spectacular diversity and their astonishingly fast rates of speciation. About 80% of all 2,500 cichlid species in East Africa, and virtually all cichlid species from Lakes Victoria (approximately 500 species) and Malawi (approximately 1,000 species) are haplochromines. Here, we present the most extensive phylogenetic and phylogeographic analysis so far that includes about 100 species and is based on about 2,000 bp of the mitochondrial DNA.
Results: Our analyses revealed that all haplochromine lineages are ultimately derived from Lake Tanganyika endemics. We find that the three most ancestral lineages of the haplochromines sensu lato are relatively species poor, albeit widely distributed in Africa, whereas a fourth newly defined lineage - the 'modern haplochromines' - contains an unparalleled diversity that makes up more than 7% of the worlds' approximately 25,000 teleost species. The modern haplochromines' ancestor, most likely a riverine generalist, repeatedly gave rise to similar ecomorphs now found in several of the species flocks. Also, the Tanganyikan Tropheini are derived from that riverine ancestor suggesting that they successfully re-colonized Lake Tanganyika and speciated in parallel to an already established cichlid adaptive radiation. In contrast to most other known examples of adaptive radiations, these generalist ancestors were derived from highly diverse and specialized endemics from Lake Tanganyika. A reconstruction of life-history traits revealed that in an ancestral lineage leading to the modern haplochromines the characteristic egg-spots on anal fins of male individuals evolved.
Conclusion: We conclude that Lake Tanganyika is the geographic and genetic cradle of all haplochromine lineages. In the ancestors of the replicate adaptive radiations of the 'modern haplochromines', behavioral (maternal mouthbrooding), morphological (egg-spots) and sexually selected (color polymorphism) key-innovations arose. These might be - together with the ecological opportunity that the habitat diversity of the large lakes provides - responsible for their evolutionary success and their propensity for explosive speciation.
Figures
Figure 1
Distribution of the major haplochromine lineages in Africa with special emphasis on the East African lakes (according to our phylogenetic and phylogeographic analyses and references [4, 12, 13, 34]). Note that the color scheme is carried throughout this publication.
Figure 2
50% majority-rule bootstrap consensus tree of 304 cichlid fish specimens based on 862 bp of the mitochondrial control region (neighbor-joining, HKY85 model with gamma substitution correction, 5,000 replicates). Relevant bootstrap values are depicted on the respective branches. The branches colored in red indicate the taxa that were chosen for the phylogenetic analyses combining the control region with sequences of the NADH dehydrogenase subunit II gene (see Fig. 3; for Ctenochromis oligacanthus from GenBank no control region sequence was available). The colors of the boxes that indicate the major clades refer to Figs. 1 and 3, the labels of the clades correspond to Table 1 [see Additional file 1]. Note that Haplochromis bloyeti (marked by an asterisks) had a control region sequence identical to H. sp. 1533 of [25], which was collected in the Malagarasi River, and grouped – together with other fishes from the Malagarasi area and from the Lake Edward/George region – into their group VII. Likewise, our H. sp. Tanzania I (marked by a circle) was identical to H. sp. 1738 of [25], which was collected in Lake Chala and clustered with other taxa from Tanzania into their group VI. In addition to Haplochromis gracilior (endemic to Lake Kivu), which was recently identified as close relative of the Lake Victoria superflock [4], we found another sister group to the superflock. This lineage includes Haplochromis paludinosus that occurs in the Malagarasi, as well as undescribed species from Tanzania and Lake Edward (see also Fig. 3). Like Haplochromis gracilior from Lake Kivu, all these taxa have the diagnostic character state 'Adenine' in position 630 of the control region alignment and root to the Lake Victoria superflock through the central rift valley haplotype [4], corroborating the view that Lake Kivu is the main reservoir from which the Lake Victoria superflock evolved [4].
Figure 3
Maximum likelihood phylogeny of the haplochromine cichlids [general time-reversible model with gamma correction] based on 100 taxa. Numbers above the branches represent Bayesian posterior probabilities obtained with Mr. Bayes, numbers below the branches represent maximum-likelihood bootstraps (100 replicates, obtained with PAUP*). Boulengerochromis microlepis and Oreochromis tanganicae, two tilapiine cichlids in LT, were used as outgroup taxa [9, 15, 16, 63]. In accordance to previous studies [9, 15] we find that within the LT species flock the Eretmodini (Ere.) are placed as sister group to the Lamprologini (Lampr.) plus several LT tribes ("Tanganyika") including the Orthochromis assemblage from the Malagarasi plains, and the haplochromines sensu lato. The latter clade combines four distinct lineages, a Congolese/South-African- (CSA; ~150 species), the _Pseudocrenilabrus_- (3 species), the _Astatoreochromis_-lineage (3 species), and the modern haplochromines (~1,800 species). The modern haplochromines combine the LT Tropheini, the species flock of LM, several riverine lineages as well as the LV region superflock according to [4]. The haplochromines sensu lato are characterized by their breeding behavior; true egg-spots (ocelli) are likely to have evolved in the ancestor of the _Astatoreochromis_-lineage and the modern haplochromines. By contrast, the Malagarasi River Orthochromis are biparental caregivers [34] providing behavioral support for our molecular-based classification that excluded these fish from the haplochromines sensu lato. We note that several genera are polyphyletic and major taxonomic revisions will be required in the future to take our phylogenetic results into consideration. For example, Orthochromis of the Malagarasi River plains form a clade outside the remaining haplochromines in close affinity to the LT Ectodini (see also [9]) whereas Orthochromis polyacanthus and O. stormsi, which share derived features [12], fall – in accordance to their distribution – into the Congolese/South African clade. Other polyphyletic genera are Astatotilapia, Ctenochromis, and Haplochromis. The grey arrows next to some species names refer to the pictures on the right, the asterisk symbol marks the ancestor of the haplochromines sensu lato, the circle symbol marks a "piebald" ("orange blotched") form as found in the modern haplochromines only.
Figure 4
The "out of Tanganyika" scenario of haplochromine evolution in Africa. (a) Several haplochromine lineages independently left Lake Tanganyika and colonized large parts of Africa via past and present river connections. Some of these lineages seeded cichlid radiations in distant lakes. The phylogeographic scenario is in agreement with palaeo-geological reconstructions of the evolution of the East African Rift region. LT is the oldest of the rift lakes. Its central basin began to form between 9 and 12 MYA, the northern (8-7 MYA) and the southern basin (2–4 MYA) began to fill at later periods [76]; deepwater conditions exist since about 5–6 MYA [78]. LM (2–4 MYA) and LV (750,000 years) are considerably younger. (b) Proposed lake level of Lake Tanganyika during the last four million years [76, 77, 79] indicating major low- and high-stands. (c) Chronogram of the haplochromine evolution in Africa as reconstructed with r8s [72, 73] based on the maximum likelihood topology. The size of each clade represents its species number. The modern haplochromines are a recent and rapidly speciating lineage. Our molecular clock calibration suggested about 2 MYA (1.15 – 3.89 MYA) for the most recent common ancestor in the Congolese/Southern African lineage and ca. 2.4 MYA (1.22 – 4.02 MYA) for their split from the common ancestor with the _Pseudocrenilabrus_-, _Astatoreochromis_-, and modern haplochromine lineage. This lies in the range of the proposed high lake-level stand of LT between the minima at 3.5 MYA and 1.1 MYA (650–700 m below present level) [76, 77] making an overflow through the Lukuga valley possible, thus opening the connection between LT and the Congo drainage. The asterisks mark nodes with a significant burst of lineage diversification (p c < 0.01) [21]. Aa... Astatoreochromis alluaudi, CSA... Congolese/South African lineage, Hb... Haplochromis bloyeti, LMF... Lake Malawi species flock, LVS... Lake Victoria Region Superflock, MO... Malagarasi Orthochromis assemblage, Pm... Pseudocrenilabrus multicolor, Pp...Pseudocrenilabrus philander, Ps... _Pseudocrenilabrus-_lineage, Tr... Tropheini.
Figure 5
Maximum parsimony reconstruction of habitat type (lake versus river) using MacClade (the maximum likelihood reconstruction with Mesquite revealed analogous results) based on the maximum likelihood topology (see Fig. 3). The ancestor of the modern haplochromines (marked by a circle) is likely to have been a riverine species. This implies that also the Tanganyikan Tropheini originated from a riverine ancestor and re-colonized the lake where they presently form an abundant group in the rocky littoral zones.
References
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- Kornfield I, Smith PF. African Cichlid Fishes: Model systems for evolutionary biology. Annu Rev Ecol Syst. 2000;31:163–196. doi: 10.1146/annurev.ecolsys.31.1.163. -DOI
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