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Similar Morphologies of Cichlid Fish in Lakes Tanganyika and Malawi Are Due to Convergence Thomas D

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Similar Morphologies of Cichlid Fish in Lakes Tanganyika and Malawi Are Due to Convergence Thomas D MOLECULAR PHYLOGENETICS AND EVOLUTION Vol. 2. No. 2, June. pp. 158-165. 1993 Similar Morphologies of Cichlid Fish in Lakes Tanganyika and Malawi Are Due to Convergence Thomas D. Kocher , * '1 Janet A. Conroy,* Kenneth R. McKaye,* and Jay R. Stauffer* * Department of Zoology, University of New Hampshire, Durham, New Hampshire 03824; t Appalachian Environmental Laboratory, University of Maryland, Frostburg, Maryland 21532; t School of Forest Resources, Pennsylvania State University, University Park, Pennsylvania 16802 Received March 22, 1993; revised June 29, 1993 ancestor for the Lake Victoria cichlid flock (Sage et al., The species flocks of cichlid fishes in the lakes of East 1984; Meyer et al., 1990). The mechanisms by which Africa are the most spectacular example of adaptive so many species have arisen in such a short time, radiation among living vertebrates. Similar highly de­ within closed lake basins, are a fascinating subject for rived morphologies are found among species in differ­ research. ent lakes. These similarities have been variously inter­ A separate, monophyletic origin for the species flock preted either as evidence for migration of ancestral in each lake has often been assumed, partly because species between the lakes, or of striking convergence of the high levels of endemicity found in the cichlid of morphology. To distinguish among these competing fauna, and partly because of the ancient and isolated hypotheses we sequenced a portion of the mitochon­ history of each lake (Fryer and lies, 1972). The lake drial UNA control region from six pairs of morphologi­ basins have arisen separately by a gradual lengthen­ cally similar taxa from Lakes Malawi and Tanganyika. ing and deepening of the East African rift (Malawi Our results clearly indicate a separate origin of these and Tanganyika) or by tilting of the Tanzanian shield morphologies in the two lakes. They also suggest that (Victoria). Each lake now drains through a separate the Tanganyikan radiation is relatively old, and that the species flocks in lakes Malawi and Victoria are de­ river, which effectively isolates extant lacustrine rived from one of the ancient lineages found in Lake forms. Suggestions persist, however, that some lakes Tanganyika. These findings have important implica­ may have been connected at various times through in­ tions for understanding the pattern of morphological termediate lakes (e.g., the connection of lakes Malawi and behavioral evolution in these fish, e 1993 Academ ic and Tanganyika through Lake Rukwa; Banister and ProsH. Inc. Clarke, 1980), or by stream capture (Greenwood, 1974). All of this leads to the conclusion that geologic evidence is not sufficient to determine whether the INTRODUCTION flocks evolved separately in each lake. Morphological taxonomists have failed to reach a The explosive speciation of cichlid fish in the lakes consensus concerning relationships of fish in different of East Africa has long been a focus for controversy lakes. Regan (1920) created a basal dichotomy between among evolutionary theorists (Mayr, 1963; Fryer and “haplochromine” and “tilapiine” lineages based on the lies, 1972). Lake Malawi, with over 400 species of en­ shape of the neurocranial apophysis. Implied in this demic cichlid, has more species of fish than any other distinction were numerous instances of morphological lake in the world. Lakes Victoria 0200 species) and convergence between certain tilapiine species from Tanganyika 0 1 7 0 species) run a close second and Lake Tanganyika with haplochromine species from third. These species probably arose in a relatively lakes Malawi and Victoria. Myers (1936), while gener­ short period of time. Recent geological studies suggest ally accepting the idea of a separate origin of the fishes that Lake Tanganyika is no more than 12 MY old (Co­ in each flock, suggested that the Tanganyikan genus hen et al., 1993), while Lake Malawi is thought to be Petrochromis and Lake Malawi Pseudotropheus were considerably more recent, probably less than 2 MY old so similar that the genera should be merged. Trewavas (Banister and Clarke, 1980). Several authors have sug­ (1949), while studying the Malawi flock, reaffirmed Re­ gested an extremely recent (<200,000 years) common gan’s hypothesis of a separate origin of the fish in dif­ ferent lakes and this view has been promulgated by ‘ To whom correspondence should be addressed. Fax: (603) 862- most workers since (Fryer and lies, 1972). 3784. E-mail: t_ kocherft/ unhh.unh.edu. A series of papers by Greenwood (1978, 1979, 1980) 1055-7903 93 $5.00 158 Copyright £ 1993 by Academic Press. Inc. All rights of reproduction in any form reserved. HISTORY OK AFRICAN RIFT LAKE CICHLID FISH 159 and colleagues (Stiassny, 1981) exposed inconsisten­ idochromis (T) display a strong horizontal striping cies in the characters used by others to demonstrate reminiscent of Melanochromis auratus (M). the close relationship of fish within each lake. Neither Most specimens were collected by the authors the structure of the apophysis, squamation and shape directly from nature: Bathybates sp. Boulenger; Cyr- of the caudal fin, nor the structure of anal fin spots is tocara moorii Boulenger; Lobochilotes labiatus Bou­ consistent among the members of a single flock. Even­ lenger; Melanochromis auratus (Boulenger); Placido­ tually, Greenwood (1983, p. 209) concluded “that the chromis milomo (Oliver); Petrotilapia sp.; Rhampho­ species flocks of lakes Victoria, Malawi and Tangan­ chromis sp. Several Tanganyikan specimens were yika are each composed of several distinct lineages, provided by Mireille Shreyen (Fishes of Burundi, Bu­ and that members of at least some lineages occur in jumbura): Cyphotilapia frontosa (Boulenger); Petroch­ more than one lake.” The search for morphological romis orthognathus Matthes; Tropheus moorii var. characters useful for cladistic analyses has continued. Moba Boulenger. Two species common in the aquarium Despite the morphological diversity of these fishes, trade were purchased from dealers in the United however, few synapomorphic characters exist for re­ States: Julidochromis regani Poll and Pseudotropheus solving phylogeny (Stiassny, 1991). Repatterning of zebra (Boulenger). All vouchers will be deposited in cichlids has mostly occurred by changes in relative the Pennsylvania State University Museum. growth rate among structures (Strauss, 1984). In any case, construction of phylogenies from morphological DNA Methods characters creates a tautology for studies of the evolu­ DNA was extracted from tissues of frozen or ethanol- tion of these traits. An independent set of characters preserved specimens using standard proteinase K is required. digestion and phenol extraction protocols (Kocher Kornfield (1991), on the basis of allozyme characters, et al., 1989). Amplifications were performed in 50-iil suggested that Cyphotilapia frontosa of Lake Tangan­ volumes of 0.67 M Tris (pH 8.8), 2 m u MgCl2, 1 d im yika was more closely related to members of the Ma­ of each dNTP, 5 |a m of each primer, 1-1000 ng of tem­ lawi flock than to other Tanganyikan species tested. plate DNA and 1.5 units Taq polymerase (Perkin To date, this has been the only test of the relationship Elmer-Cetus). The primers used were THR between Malawi and Tanganyikan cichlids using mo­ (5-AGCTCAGCGCCAGAGCGCCGGTCTTGTAAA-3 lecular characters. and TDKD (5'-CCTGAAGTAGGAACCAGATG-3'). We have used the sequence of nucleotides in mito­ The temperature profile for 30-40 cycles of double­ chondrial DNA to test the independent origin hypothe­ stranded amplification was 93°C for 30 s, 50°C for 60 sis. These characters are expected to evolve indepen­ s and 72°C for 120 s. Amplified products were sepa­ dently from the genes which control the morphology of rated on a 1% LMP agarose gel. Desired fragments these fishes. The recency of the East African cichlid were purified from the gel by hot phenol extraction and radiations (Sage et al., 1984) led us to sequence a rap­ precipitation with isopropanol. The DNA (approxi­ idly evolving portion of the mitochondrial genome, the mately 0.5 (jLg) was resuspended in 20-40 nl of dH20 control or D-loop region. and 10-12 ji.1 sequenced using the TAQ DyeDeoxy Ter­ minator cycle sequencing protocol (Applied Biosys­ MATERIALS AND METHODS tems). Centri-Sep columns (Princeton Separations) were used to remove unincorporated nucleotides prior Sources of DNA to loading on an automated sequencer (373A, Applied We chose six pairs of morphologically similar fishes Biosystems). to illustrate the range of morphological and behavioral similarities of species in lakes Malawi and Tanganyika Phylogenetic Analyses (Fig. 1). Petrochromis (Tanganyika) and Petrotilapia Sequence alignment was performed using the se­ (Malawi) share a highly developed rasping jaw mor­ quential algorithm of the program PILEUP (Devereux phology and were considered by Fryer and lies (1972) et al., 1984). A gap penalty of 1 and a gap length pen­ to represent one of the most remarkable similarities alty of 0.3 were used, but the alignment was not partic­ in the two fauna. The morphology and ecology of the ularly sensitive to variations in these parameters. No elongate predator Bathybates (T) closely mimics that manual adjustments of the alignment were performed. of Rhamphochromis (M). The fleshy lips of Lobochilotes Minimum length networks relating the taxa were (T) closely resemble the fat lips of Placidochromis mi- found using the branch and bound algorithm of PAUP lomo (M). Tropheus (T) and Pseudotropheus (M) are (Swofford, 1992). Statistical significance of particu­ morphologically and behaviorally similar taxa which lar groupings was estimated by branch and bound live over rock substrates. Cyphotilapia frontosa (T) has searches of 2000 bootstrap samples from the original an enlarged nuchal hump which is also found in Cyrto- data set. For the tree relating 16 taxa, computational cara moorii (M). Some species of the rock-dwelling Jul- limitations prevented the examination of a large num­ 160 KOCHER ET AL. FIG. 1. Six pairs of morphologically similar cichlids from Lakes Tanganyika and Malawi. Tanganyikan fish are in the left column, Malawi fish in the right.
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