* Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Midori-ku, Yokohama, Japan
Division of Molecular Marine Biology, Ocean Research Institute, University of Tokyo, Nakano, Tokyo, Japan
Conservation Division, WWF Japan, Minato-ku, Tokyo, Japan
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Abstract |
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Key Words: exclusive speciation incomplete lineage sorting African Great Lakes cichlid retroposon SINE AFC family
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Introduction |
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Another topic of interest is whether the evolution of pan- and west African cichlids was accompanied by incomplete lineage sorting and/or interspecific hybridization, which appears to have occurred multiple times during the evolution of cichlids in the African Great Lakes (Moran and Kornfield 1993, 1995; Parker and Kornfield 1997; Nagl et al. 1998; Van Oppen et al. 2000; Takahashi et al. 2001a, 2001b). If this was indeed the case for the pan- and west African cichlids, then caution must be exercised when attempting to elucidate their phylogeny, given that the genealogies of individual loci may not coincide with their phylogeny (Nei 1987; Pamilo and Nei 1988; Takahata 1989; Avise 2000).
Recently, a series of successful phylogenetic analyses was conducted for African Great Lakes cichlids by investigating insertions of the AFC (rican
ichlid) family (Takahashi et al. 1998, 2001a, 2001b) of short interspersed elements (SINEs) into orthologous loci in the nuclear genome (for reviews of the SINE method see Okada 1991; Cook and Tristem 1997; Miyamoto 1999; Shedlock, Milinkovitch, and Okada 2000; Shedlock and Okada 2000). Short interspersed elements multiply via retroposition, and their choice of insertion sites is nearly random (Weiner, Deininger, and Efstratiadis 1986). In the absence of any known specific excision mechanism, SINEs remain at the integration locus indefinitely. These characteristics of SINEs make them advantageous for elucidating phylogenetic relationships; the sharing of a SINE sequence at a specific site can be regarded essentially as a synapomorphy. Short interspersed elements have also been useful for detection of both recent (Hamada et al. 1998; Takahashi et al. 2001a) and ancient (Takahashi et al. 2001b) rapid speciation accompanied by incomplete lineage sorting of alleles. In this article we report use of the SINE method to elucidate the phylogenetic relationships among the ancient cichlid lineages in Africa, as well as testing for the existence of incomplete lineage sorting among these lineages to gain insights into their mode of speciation.
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Materials and Methods |
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Results and Discussion |
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On the basis of the above results, a phylogenetic tree for the cichlids was constructed (fig. 2). Monophyly of the east African clade was suggested by earlier studies using nuclear DNA and/or mitochondrial sequences. However, these studies involved only a limited number of genera from pan- and west Africa (36 genera; Sültmann et al. 1995; Zardoya et al. 1996; Streelman and Karl 1997; Mayer, Tichy, and Klein 1998; Streelman et al. 1998; Farias, Orti, and Meyer 2000; Farias et al. 2001). Our data from 11 pan- and west African genera for two loci (241 and 504) as well as from 3 to 10 genera for the other five loci (255, 450, 509, 1240, and 1708; table 3) provide the most comprehensive support for monophyly of the east African clade. The sister group relationship between Tilapia/Steatocranus and the east African clade is consistent with the phylogeny proposed by a sequence analysis of the noncoding nuclear locus DXTU1, in which Oreochromis, Tylochromis, Pelvicachromis, and Hemichromis were included as well (bootstrap value of 75%; Mayer, Tichy, and Klein 1998). That study also suggested (bootstrap value of 66%) that the clade consisting of 7 species of Oreochromis is the sister group to the clade corresponding to our east clade. The results obtained for locus 906 are also consistent with this hypothesis (table 3). Our results support the hypothesis that the ancestral stock, which may formerly have populated west Africa, gave rise to lineages that were the forebears of Anomalochromis, Chromidotilapia, Hemichromis, Nanochromis, Oreochromis, Pelvicachromis, Sarotherodon, Teleogramma, and Tylochromis. The divergence of Tilapia, Steatocranus, and the ancestor of the east African clade then followed this event (see Mayer, Tichy, and Klein 1998, Discussion). Clarification of the detailed relationships among the west African lineages will require further characterization of other loci into which the AFC SINE has inserted.
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Under what circumstances could the speciation of the ancestral lineages of Tilapia, Steatocranus, and the east African clade have accompanied incomplete lineage sorting? Lineage sorting tends to be incomplete when successive speciation events occur rapidly (Nei 1987; Pamilo and Nei 1988; Takahata 1989). All previous examples of incomplete lineage sorting in cichlids (Moran and Kornfield 1993, 1995; Parker and Kornfield 1997; Nagl et al. 1998; Van Oppen et al. 2000; Takahashi et al. 2001a, 2001b) occurred in the African Great Lakes which are known to exhibit explosive rates of speciation. The speciation events that are the focus of the present study, however, preceded the divergence of the oldest lineages in Lake Tanganyika, which corresponds to the basal node of the east African clade (fig. 2). Thus, it is possible that rapid speciation occurred in riverine ecosystems before Lake Tanganyika was formed. An alternate explanation is that speciation may have taken place in a putative ancient lake that existed prior to the formation of Lake Tanganyika. Phylogenetic analysis of central and east African riverine and lacustrine cichlids using mitochondrial DNA sequences (Salzburger et al. 2002) suggests that some lineages that diverged during the primary lacustrine radiation of Tanganyikan cichlids may have been capable of colonizing surrounding rivers secondarily. If a similar process was involved in the more ancient lacustrine radiation hypothesized in the present study, then the ancestors of Tilapia, Steatocranus, and the east African clade might have been the lineages that fled the ancient lake for the riverine habitat prior to the lake's disappearance. Inclusion of more species into future analyses would be helpful to gain greater insight into how extensively the assumed incomplete lineage sorting or interspecific hybridization event occurred, and thus to test the above hypotheses. Especially, analyses of various lineages of tilapiines may be important, either for this purpose or for reconstruction of a more detailed phylogeny, given that they may consist of diverse lineages (Nagl et al. 2001).
Our work demonstrates that the analysis of SINE insertions is capable of detecting possible ancient incomplete lineage sorting (or interspecific hybridization) that took place even before the divergence of the major cichlid lineages of Lake Tanganyika, during an event that occurred 14 MYA, as estimated by an earlier allozyme analysis (Nishida 1997). Previous analyses of nuclear and/or mitochondrial markers (Sültmann et al. 1995; Zardoya et al. 1996; Streelman and Karl 1997; Mayer, Tichy, and Klein 1998; Streelman et al. 1998; Farias, Orti, and Meyer 2000, Farias et al. 2001) did not recognize this phenomenon. Given that ancient incomplete lineage sorting (or interspecific hybridization) can be detected only by analyzing genealogic discordance among multiple loci, the failure of several of these studies to recognize the phenomenon can be explained by the fact that only a single locus (or two, in the case of Farias et al. [2000]) was analyzed. Even if multiple loci are analyzed, conventional methods of sequence analysis tend to produce relatively large statistical errors when the subjects are ancient lineages that diverged over a relatively short period (e.g., 30% of the bootstrap support for the sister group relationship between Steatocranus and Tilapia; see fig. 2 in Mayer, Tichy, and Klein 1998). Thus, it may often be difficult to discern such statistical errors from bona fide incomplete lineage sorting in analyses of discordance among topologies obtained from multiple loci. Our data suggest that SINEs could be useful as probes for the analysis of explosive speciation, including events that were "ancient."
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Acknowledgements |
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Footnotes |
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1 These two authors contributed equally to this work.
E-mail: nokada{at}bio.titech.ac.jp.
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