Journal o f Biology (1998) 53, 752-766 Article No.jb980740

Phylogenetic study of in : a lepidological approach

E. L ip p its c h Steingrabenweg 26, A-8044 Graz, Austria

(Received 13 February 1998, Accepted 15 M a y 1998)

The phylogeny of the various cichlid lineages in Lake Tanganyika has been investigated applying scale morphology and squamation characters. The monophyly of the established tribes is assessed and evidence is given for their interrelationships as well as their phyletic position within the family Cichlidae. © 1998 The Fisheries Society of the British Isles

Key words: scale morphology; squamation; cladistic analysis; .

INTRODUCTION Lake Tanganyika has played a key role in the history of Cichlid and systematics since J. E. S. Moore’s collection of fish from the lake reached Europe in 1898 (Boulenger, 1899a). Before this only four Lake Tanganyika species were known (Gunther, 1894), which were placed in the Chromis Cuvier, 1814. In the first part of his Revision of the African and Syrian Fishes of the Family Cichlidae prepared in 1897, G. A. Boulenger (1898) recognized nine cichlid genera. After having inspected the Moore collection he raised this number to 19 in the second part of the revision (Boulenger, 1899b). This was the first appreciation of the astonishing diversity of cichlid fish in this East African lake. In 1920, Regan based his idea of two main divisions within the family, one related to Tilapia, the other to Haplochromis, on anatomical peculiarities discovered in Lake Tanganyika species. This idea dominated cichlid systematics for the next 50 years. It was challenged by Wickler (1963) using morphological and ethological arguments, again based on observations of Lake Tanganyika fish. The only suprageneric taxa that were proposed formally and made available for cichlids were the 12 tribes erected by Poll (1986) to express his view on the relationships between the Lake Tanganyika cichlid genera. The interest in Lake Tanganyika cichlids has increased considerably over the last few years. Partly this is due to the aquarium trade, which has provided a strong motivation to search for new species (Brichard, 1989; Konings, 1989). In addition, a number of ecological projects have been launched (e.g. Lake Tanganyika Biodiversity Project, UNDP; Management of the Fisheries of Lake Tanganyika, FAO), driven by the concern about conservation of this marvellous ecosystem as well as about the possibilities of building up a sustainable fishery to the advantage of the people around the lake. Despite the interest in Lake Tanganyika cichlids, the systematics of this group of fishes is still rather incomplete. The classification attempted by Regan (1920), 752 0022-1112/98/100752+15 $30.00/0 © 1998 The Fisheries Society of the British Isles PHYLOGENY OF LAKE TANGANYIKA CICHLIDS 753

Fryer & Iles (1972) and Poll (1986) were not based on cladistic principles and hence no longer meet present-day methodological standards. For two of Poll’s tribes, the and the Perissodini, phylogenetic studies based on morpho­ logical characters have been conducted (Liem & Stewart, 1976; Liem, 1981; Greenwood, 1983), but monophyly of the other tribes is not established and the interrelationships between the tribes have not been investigated. Recently a number of investigations applying molecular methods have been published, dealing either with the phylogeny of certain tribes (Verheyen et al., 1991; Sturmbauer & Meyer, 1993; Sturmbauer et al., 1994) or of the whole group (Nishida, 1991, 1997). No assessment of the results applying morphological methods has been undertaken so far. The main reason is the well-known and much-deplored scarcity in cichlids of useful morphological characters and synapomorphic character states. Recently it has been shown that this difficulty can be overcome by using lepidological characters (scale morphology and squamation patterns) for phylogenetic purposes (Lippitsch, 1989, 1990, 1991, 1993, 1995, 1997). A large-scale comparative study has been performed, so far covering about 500 cichlid species from all parts of their distribution. About 100 characters with about 350 character states are provided by the squamation and these characters are well suited for constructing phylogenetic trees. The method has been applied successfully on various levels of universality, from the gross division of the family (Lippitsch, 1995) to the systematics of closely related species in young species flocks (Lippitsch, 1993). In the present work the lepidological method was applied to assess the monophyly of the presumed lineages in Lake Tanganyika, to clarify their interrelationships and their phyletic position within the whole family.

MATERIALS AND METHODS The present study is based on 80 of the about 180 cichlid species of Lake Tanganyika, covering 55 of the 56 genera (Poll, 1986), missing only the monotypic Baileychromis Poll, 1986. From every endemic genus at least the type species was included. For all but four of the non-monotypic genera at least a second species was studied. The study material is listed in the Appendix. Over 400 additional species from the whole distribution range of the family Cichlidae were used for comparative investigations. Much of that material has been listed in previous publications. The methods applied and the characters used have been described extensively in previous publications (Lippitsch, 1990, 1993, 1995). Nearly 100 characters with over 300 character states have been used. Numbering of the characters and states is the same as listed by Lippitsch (1993) and is presented in the form N/n, N standing for the number of the character and n for the number of that character’s state. A few more character states not included in the published list have been established since then. They are explained in the text. The mutual independence of the character states has been tested by correlation analysis using STATISTlCA 5.1. For phylogenetic analysis PAUP 3.0b (Swofford, 1989) and McClade 3.0 (Maddison & Maddison, 1992) were applied.

RESULTS AND DISCUSSION ASSESSMENT OF MAJOR LINEAGES The 12 tribes introduced by Poll (1986) are analysed applying lepidological methods. The tribes are dealt with in the same order as given by Poll (1986). 754 E. LIPPITSCH

Synapomorphies of the tribes are described and, as far as possible, their monophyly is assessed. The respective plesiomorphic conditions are as deter­ mined in Lippitsch (1995). Sometimes the tribal synapomorphies are not present in every presumed member of a lineage, the species showing a reversal to the plesiomorphic state or an autapomorphy. A few necessary reassignments of species are discussed.

Tribe Tilapiini This tribe had been defined by Trewavas (1983) and was adapted by Poll (1986) to include the genus Boulengerochromis Pellegrin, 1903. The tribe is not endemic to Lake Tanganyika but distributed all over Africa and beyond. In this study, the species endemic to Lake Tanganyika of the genera Oreochromis and Tilapia were not investigated, but many species of those genera from other regions have been analysed. No synapomorphies uniting all genera could be found. Especially noteable, the inclusion of Boulengerochromis into this tribe could not be substantiated at all.

Tribe Haplochromini This again is a non-endemic tribe. Its distribution extends over most parts of Africa and includes also Lakes Victoria and Malawi. Lake Tanganyika is inhabited by only a few of its very numerous species. The tribe is part of the cternoid assemblage as defined by Lippitsch (1995). Analyses of large parts of that tribe have been presented elsewhere (Lippitsch, 1993, 1997).

Tribe Tylochromini This tribe contains only one genus, Tylochromis Regan, 1920, which extends over large parts of Africa. It is now well accepted that it is the sister taxon to the whole African assemblage of taxa (Stiassny, 1989, 1990; Lippitsch, 1993).

Tribe Lamprologini This tribe is not strictly endemic, but most of its constituent species live in the lake. The type species, Lamprologus congoensis Schilthuis, is from the Congo river. The tribe is a member of the ctenoid assemblage as defined by Lippitsch (1995). A suite of character states that are synapomorphic with respect to the plesiomorphic states of that assemblage demonstrates clearly monophyly of the lineage: the operculum is scaled only partially to sparingly (1/2; this state is also found in various unrelated taxa all over the family, however); there is an abrupt transition between small scales extending from the occiput onto the rostral part of the dorsum and large scales on the caudal part of the dorsum (85/2); strongly ctenoid flank scales (24/4); an abrupt transition from the small ventral scales to the large flank scales (56/2); scales on the in rows directed obliquely across the membranes (62/4, this character state was not listed previously); anal fin scaly in the spiny part (68/2); scales on the anal fin in rows directed obliquely across the membranes (70/4; this character state was not yet listed in Lippitsch, 1993). Some other apomorphies are present and shared with the tribe Eretmodini (see below). Stiassny (1991) has suggested including the fluviatile genus Teleogramma in this tribe. This suggestion was based on similarities in the buccal dentition. The PHYLOGENY OF LAKE TANGANYIKA CICHLIDS 755 lepidological characters do not support that assignment at all. Teleogramma shares with the Lamprologini only a single apomorphy, the sparingly scaled operculum. This state, however, can be regarded as a homoplasy, since it is found in various unrelated taxa and seems to be correlated with rapid- dwelling habits. The scale surface morphology is of the same type as in the Hemichromines, and the buccal dentition with its large canines may also be regarded as derived from the tooth type found in Hemichromis. Partial dis­ section of a single specimen of Teleogramma brichardi Poll revealed some anatomical resemblance between this genus and the Hemichromines. It shares with Hemichromis, for example, the absence of a calyx in the suspensorium (cf. Greenwood, 1985a). With all Hemichromines it has in common a very low coronoid process of the dentary. It does not share, however, the single synapomorphy of the Hemichromines, the absence of a foramen for the passage of the preopercular sensory canal into the dentary (see Greenwood, 1985a, b).

Tribe Tropheini This tribe is part of the ctenoid assemblage as defined by Lippitsch (1995). If it is taken in its composition as conceived by Poll (1986), no synapomorphies for all taxa can be found. If Cyphotilapia frontosa (Boulenger) is excluded, as also suggested by a recent molecular study (Nishida, 1997), at least a single synapomorphy is present in all taxa, a reduced or, more often, completely missing interopercular squamation (6/1). Thus, from the lepidological point of view monophyly of the tribe cannot be proven, but there is also no indication of a polyphyletic origin. The overall similarity is greatest with members of the tribe Haplochromini (see below). The excluded species, Cyphotilapia frontosa, is not assigned easily to any of the lineages. It is only clear that it belongs to the cternoid assemblage. Within that assemblage, the species shares apomorphies with the Tropheini, the Ectodini, the Haplochromini and the Limnochromini. Molecular data (Nishida, 1997) suggest the species to be at the basis of Nishida’s (1991) H-lineage (i.e. the ctenoid assemblage minus the Lamprologini and Ectodini). This could be in agreement with the lepidological characters, but the results are ambiguous.

Tribe Eretmodini This small tribe, consisting of only four described species assigned currently to three different genera, is part of the ctenoid assemblage as defined by Lippitsch (1995). It is clearly monophyletic, as indicated by the following synapomorphies: the operculum is scaleless (1/1); the suboperculum is scaleless (4/1); the interoperculum is scaleless (6/1); the cheek is scaleless (10/1); there is a vestigial scale sheath on the base of the dorsal fin (63/4). Some other apomorphies are present and shared with the tribe Lamprologini (see below).

Tribe Ectodini

This tribe is part of the ctenoid assemblage as defined by Lippitsch (1995). Its monophyly has been established convincingly (Liem, 1981; Greenwood, 1983; 756 E. LIPPITSCH

Sturmbauer et al., 1994). A number of apomorphies are present, but none are found only in the Ectodini. Most of them are shared with the Limnochromini (see below).

Tribe Trematocarini This tribe consists of only two rather closely related genera with about 10 species. They are rather plesiomorphic in their lepidological characters and certainly do not belong to the ctenoid assemblage as defined by Lippitsch (1995). Nevertheless, there are a few synapomorphies indicating monophyly of the tribe. Most notably, there is no opercular blotch in this tribe (3/5), a feature that is rare among African taxa, but is shared with the (otherwise very different) Cyprichromini; the squamation of the operculum is reduced (1/2); the interperculum is scaleless (6/1), but this apomorphy also occurs in other, not closely related, lineages (Lamprologini and Eretmodini); there is no postorbital squamation (12/5). Some other apomorphies are present and shared with the tribe (see below).

Tribe Bathybatini This tribe also is not a member of the ctenoid assemblage. According to Poll (1986) it comprises the genera and Hemibates. In contrast, Stiassny (1981) postulates a closer relationship of Hemibates to the Trematocarini. The lepidological characters favour Poll's classification, in agreement with a recent molecular study (Nishida, 1997), since both Bathybates and Hemibates share the following synapomorphies, which are not shared by the Trematocarini: the cheek squamation shows a distinct rostral embayment (10/4; this character state is found, however, also scattered among taxa from other tribes); the squamation pattern along the lower median of the caudal peduncle is irregular (41/4). There are three character states that are apomorphic with respect to the plesiomorphic African condition and that are shared by the Bathybatini and the Trematocarini, possibly indicating a sister taxon relationship between the two tribes (see below).

Tribe Limnochromini This tribe is part of the ctenoid assemblage as defined by Lippitsch (1995). A number of lepidological apomorphies is present, but all of them are shared with the Ectodini. Hence only monophyly of the Ectodini and Limnochromini combined can be substantiated (see below). It remains unclear whether the Limnochromini are a monophyletic lineage or a paraphyletic grade. One species that had been included with the Limnochromini by Poll (1986) does not show any of the synapomorphies characterizing the Limnochromini/ Ectodini assemblage: Paratilapia pfefferi Boulenger, 1898, which had been assigned to the genus Gnathochromis Poll, 1981. This species resembles more closely the members of the tribe Tropheini, but it cannot be assigned to any one of the available genera.

Tribe Cyprichromini This tribe, which consists of only two genera with four described species, is part of the ctenoid assemblage as defined by Lippitsch (1995). Its constituent species are the only members of that assemblage that have the apomorphic PHYLOGENY OF LAKE TANGANYIKA CICHLIDS 757 condition of a completely scaled operculum (1/4) and lack the opercular blotch (3/5). The interoperculum has two rows of scales in its caudal part (84/2), and the preoperculum is partly scaly (8/2); there are ctenoid scales on the cheek (11/3), a condition found extremely rarely in cichlids; and the scales in the rostral part of the dorsum are strongly ctenoid (20/4), which is also very rare. These synapomorphies corrobrate the monophyly of the tribe.

Tribe Perissodini On a first inspection this tribe does not resemble the members of the ctenoid assemblage sensu Lippitsch (1995), since the predominant scale type in all of its members is the cycloid one. When analysing the whole suite of lepidological characters it turns out, however, that for every one of the investigated species the most similar species outside the tribe is from the ctenoid assemblage. This is not a cladistically sound argument, but the possibility has to be taken into account, that the Perissodini are members of the ctenoid assemblage despite sharing none of the constituent synapomorphies. If a cladistic analysis is performed with respect to the plesiomorphic conditions of the African assemblage, then the Perissodini share the synapomorphies of a suboperculum with scaleless caudoventral rim (5/3; but this state is not rare in other lineages of the ctenoid assemblage); and an interoperculum with naked ventral rim (6/3; this state is shared, however, with a few scattered species of the ctenoid assemblage, especially the Ectodini). If the plesiomorphic status of the ctenoid assemblage is used for the analysis, the Perissodini have in common the synapomorphies of the above-mentioned interopercular squamation pattern (6/3) and the predominant cycloidy on various parts of the body (22/1, 24/1, 38/1, 40/1, 54/1). In any case the synapomorphies indicate monophyly for the tribe, as suggested before by Liem & Stewart (1976).

PHYLETIC INTERRELATIONSHIPS OF THE LINEAGES The results of this analysis corroborate the monophyly of most of Poll’s (1986) tribes, at least after a few species have been removed and assigned to another lineage. Now it remains to establish the interrelationships between the tribes and their phyletic position within the family. All of the Lake Tanganyika tribes can be assigned to the monophyletic African radiation, which is characterized by at least four myological and osteological synapomorphies (see Stiassny, 1991) and is supported by molecular data (Zardoya et al., 1996). Within this radiation, Tylochromis is the sister taxon to all the others combined. This African assemblage is united by the synapo­ morphies of reduced number of predorsal bones (Cichocki, 1976) and the presence of an opercular blotch (3/1). This feature has been listed by Stiassny (1991) as ‘ a strongly pigmented opercular spot ’, but this expression is somewhat misleading. The opercular blotch is a scaleless spot in the dorsocaudal angle of the operculum and is strongly pigmented in some taxa, but may be completely without pigment in others. It may also vary in size and shape. But irrespective of its appearance it can be distinguished readily from the rest of the operculum by its characteristic polished surface, which is discernible in many cases even if the operculum is scaleless. The lack of an opercular blotch in the Cyprichromini and the Trematocarini has to be considered as due to independent reversals. 758 E. LIPPITSCH

Both have a reduced number of predorsal bones, none to a single one in the Trematocarini (Cichocki, 1976) and a single one in the Cyprichromini (pers. obs.). Furthermore, the Cyprichromini share the synapomorphies of the ctenoid assemblage. Thus there is no reason to assume that these two tribes are not members of the African assemblage. The Bathybatini and Trematocarini retain a large number of plesiomorphic states of the African radiation. But they share three character states that may suggest the two tribes are sister taxa. The first one is the missing granulation on the caudal field of the flank scales (28/4). All other members of the African assemblage, even those with cycloid scales, have a distinct granulation. The absence in these two tribes could be interpreted in two different ways. It could be interpreted as a plesiomorphy, since the same condition is present in Tylochromis. Accepting this interpretation, the presence of granulation would become a synapomorphy of the remaining monophyletic African assemblage. The Bathybatini and Trematocarini, which are members of that assemblage, would represent a clade or grade at the base of, but not belonging to that monophyletic part. The alternative interpretation would be that absence of granulation shared with the Tylochromini is a homoplasy. In that case this state would be a synapomorphy of the Bathybatini and the Trematocarini, and the two tribes would be sister taxa. The second apomorphy is the presence of short, talon-shaped ctenii (33/1). The same form of ctenii is present in some species scattered over various lineages of the African assemblage. Hence its value in assessing relationships is some­ what dubious. Probably it has evolved independently several times and in two different ways, either de novo from cycloid ancestral scales, or as a reduction from long and straight ctenii. So far it cannot be decided if this state is a true synapomorphy of the Bathybatini and Trematocarini, indicating a sister-taxon relationship. The third apomorphy is a true synapomorphy, beyond every doubt. Among all the other cichlid taxa the circuli in the interradial spaces on the rostral field of the flank scales bear distinct denticles, anchoring the scale in the tissue. The Bathybatini and the Trematocarini have the unique condition of completely reduced denticles (34/4). The functional basis of that reduction is not clear, but the phyletic significance is obvious. This unique synapomorphy, together with the former two, rather ambiguous ones, establishes the sister-taxon relationship between the two tribes. This result is in agreement with the finding of Stiassny (1981) that both tribes share several apomorphic anatomical character states (Table I, states B, C). In view of the lepidological synapomorphies and the molecular data (Nishida, 1997) uniting Bathybates and Hemibates, the evolution of apomorphies has to be reinterpreted, however. No further relationships can be established for the joint Bathybatini/Trematocarini. The relationships of the Tilapiini are unclear. Since no uniting synapomorphy could be found it is not even clear if the tribe is really monophyletic. Interest­ ingly, the difference in scale granulation (26/2 or 26/3) does not coincide with the accepted genera (Tilapia, Sarotherodon, and Oreochromis as the most important ones), but cuts through the genus Oreochromis. All the other Lake Tanganyika taxa belong to the ctenoid assemblage, which is characterized by the synapomorphies (with respect to the plesiomorphic PHYLOGENY OF LAKE TANGANYIKA CICHLIDS 759

Table I. Data matrix used in the analysis of intertribal phyletic relationships

Character state Taxon ABCDEFGHI J KLMNOP Q RST

Bathybatini 1 1 1 100 1 0 00 1 1 0 0 0 1 1 0 00 Cyprichromini 1 0 0 0 1 1 0 1 11 1 1 0 0 0 0 0 0 0 0 Ectodini 1001110 111110 0000111 Eretmodini 100 1 110 11100 1 1 10 0 000 Haplochromini 1 0 0 1 1 1 0 1 11 1 1 0 0 0 0 0 0 0 0 Lamprologini 1 0 0 1 1 10 1 110 0 1 1 1 0 0 0 0 0 Limnochromini 1 0 0 1 1 1 0 1 11 1 1 0 0 0 0 0 1 1 1 Perissodini 100 1000 00011 0 0 0 0 0 000 Tilapiini 100 1000000110 0000000 Trematocarini 1 1 1 0 0 0 1 0 00 1 1 0 0 0 1 1 0 0 0 Tropheini 100 1110 111110 0 000000 Tylochromis 00000010001100000000

0 and 1 denote absence or presence of character state. Autopomorphies of the respective taxa are not given. Character list: A, reduced number of predorsals; B, ascending process of the anguloarticular expanded laterally. C, palatine-lateral ethmoid ligament present; D, opercular blotch present; E, ctenoid scales on caudal part of dorsum; F, ctenoid scales on flank; G, caudal field of flank scales without granulation; H, ctenoid scales close to base of pectoral fins; I, ctenoid scales on caudal peduncle; J, ctenoid scales on belly; K, interoperculum scaly; L, cheek scaly; M , flank scales of trapezoid from; N, rim of flank scales weakly ossified; O, dorsal fin scaly; P, presence of short, talon-shaped ctenii on flank scales; Q, denticles on interradial circuli missing; R, opercular blotch protracted rostrally; S, flank scale granulation type 28 (see text); T, granular area forming a circular arch; Character states A, B and C from Stiassny (1991), others from this work.

African condition) of ctenoid scales on the caudal part of the dorsum (22/3), on the flank (24/3), near the base of the pectoral fin (38/3), on the caudal peduncle (40/3), and on the belly (54/3). This assemblage is also strongly supported by molecular data (Nishida, 1991, 1997). The Lamprologini and the Eretmodini exhibit a suite of clear synapomorphies: the interoperculum is scaleless (6/1), the cheek squamation is highly reduced (10/1); the flank scales have a trapezoidal form (25/4) with a rather straight rostral rim, straight and nearly parallel dorsal and caudal rims, and a caudal rim forming an obtuse angle (see Fig. 1); the rim of the flank scales is only weakly ossified (32/3); the scales on the caudal peduncle are more strongly ctenoid than on the flanks (40/4); and the dorsal fin is scaly, with cycloid scales (61/1). From this suite it can be assumed that the two tribes are sister taxa. Molecular data (Nishida, 1997) had rendered ambiguous results, placing the Eretmodini near the Tropheini (using allozyme data) or the Lamprologini (from data of the NADH dehydrogenase subunit 2 gene). For the Perissodini no relationships could be established. The question of their belonging to the ctenoid assemblage has been discussed above. Molecular data suggest that they are near the Cyprichromini and Limnochromini (Nishida, 1991, 1997). Also for the Cyprichromini the nearest relatives within the ctenoid assemblage could not be established unequivocally. The Limnochromini and the Ectodini are united by three unique synapo- morphies: they have an opercular blotch that is large to extremely large and 760 E. LIPPITSCH

Fig. 1. Flank scale of Lepidiolamprologus profundicola (MRAC 78-25-P 354-355), to show trapezoidal overall form, a synapomorphy uniting the tribes Lamprologini and Eretmodini. Scale bar 1 mm.

Fig. 2. Dorsal part of operculum in Enantiopus melanogenys (unregistered) to show enlarged, rostrally protracted opercular blotch, synapomorphic for the tribes Ectodini and Limnochromini. Scale bar 1 mm. distinctly protracted rostally (3/7). This form of the opercular blotch is not found in any other cichlid taxon and is very conspicuous (Fig. 2). Furthermore, they exhibit a peculiar form of the granular area of the caudal field of the flank scales that is a circular arch (28/3; Fig. 3) rather than a sector. The granulation (numbered as type 28 in Lippitsch, 1995) is characterized by very regular radial rows of ctenii lying flat on the scale surface, the neighbouring rows being displaced with respect to each other by half the interctenial distance. Molecular studies (Nishida, 1991, 1997) had shown the two tribes of Eretmodini and Limnochromini to be near each other, but had suggested that they form a PHYLOGENY OF LAKE TANGANYIKA CICHLIDS 761

Fig. 3. Flank scale of Enantiopus melanogenys (unregistered) showing arch-like form of granular area and type of granulation. Scale bar 0-2 mm. paraphyletic grade rather than a monophyletic clade. Lepidological characters strongly support joining the two tribes in a monophyletic lineage. No convincing lepidological synapomorphies could be established for the two remaining tribes, the Tropheini and the Haplochromini. Their close mutual relationship is strongly supported, however, by molecular data (Nishida, 1997). Possibly they form, together with the monophyletic Limnochromini/Ectodini and the Cyprichromini, a superlineage within the ctenoid assemblage. These data are summarized in the data matrix (Table I). A phylogenetic analysis of the tribes was performed with PAUP 3.0b, regarding Tylochromis as the outgroup. A heuristic search yielded two shortest trees of length L =22, which had a nearly identical topography, but differed in leaving unresolved two polytomies in the first one while resolving them at least partly in the second. Bootstrapping with 100 replications yielded a tree in full agreement with the second one, again resolving the polytomies. Two character states (the reduced number of predorsal bones and the absence of denticles on the circuli in the rostral field) turned out to be uninformative in the present context. The overall consistency index was C =0 909, the retention index R =0 943. This tree is presented, together with the relevant synapomorphies and the bootstrap values of the branches, as the final phylogenetic hypothesis in Fig. 4.

CONCLUSION The results of this study provide a morphological basis for the monophyly of the presumed lineages as well as a hypothesis on the interrelationships of the tribes and their phyletic positions within the family Cichlidae. The agreement with other phylogenetic studies, as far as they are available, is rather satisfactory. In cases, where conflicting hypotheses existed, the lepidological approach may facilitate a choice between them. In addition, new evidence on certain phyletic relationships could be established. Eventually, this study proves that cichlid 762 E. LIPPITSCH

Fig. 4. Cladogram of the cichlid lineages present in Lake Tanganyika. Synapomorphies uniting tribes into monophyletic lineages are denoted by upper case letters attached to the branches, correspond­ ing to those given in the character matrix, Table I. Numbers on branches denote bootstrap values (PAUP, heuristic search, 100 replications). Support of a branch by molecular data (Nishida, 1991, 1997; Sturmbauer & Meyer, 1993) is indicated by an asterisk. Question marks (?) indicate absence of known synapomorphies and dashed lines denote possible relationships that are, how­ ever, only insufficiently supported by available data. See text for explanation. Overall consistency index C =0 909, retention index R=0943. morphology is far from having reached its ultimate borders, and that many new morphological characters can be found even from external investigation of the fishes alone. This finding should encourage morphological work to elucidate cichlid phylogeny, hand in hand with the novel molecular techniques established in recent years.

Most of this work is based on material from the rich collections in the Musee Royal de l’Afrique Centrale, Tervuren, Belgium and The Natural History Museum, London. The author is highly indebted to the authorities and the staff of the museums, especially to G. Teugels, J. Snoeks, Tervuren, and O. Crimmen, for the generous loan of specimens. Financial support of this work by the Austrian Science Foundation, grants no., P09935-BI0 and P12047-BI0, is gratefully acknowledged. PHYLOGENY OF LAKE TANGANYIKA CICHLIDS 763

References

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APPENDIX In the following, all specimens from Lake Tanganyika used in this study are listed. Specimens from a few additional species that were of special importance in the present context are included. Specimens from other cichlid species used for comparison have been listed in previous papers (Lippitsch, 1990, 1992, 1993, 1995, 1997). The following abbreviations are used for the museums, from which the specimens were borrowed: BMNH, The Natural History Museum London; MRAC, Musee royale de l’Afrique Centrale Tervuren; NMW, Naturhistorisches Museum Vienna. Other specimens are in the author’s collection.

Altolamprologus calvus (Poll, 1978) MRAC 78-25-P-180-193 Altolamprologus compressiceps (Poll, 1986) MRAC 84-09-P-352-353, MRAC 92-084-P-0002 PHYLOGENY OF LAKE TANGANYIKA CICHLIDS 765

Asprotilapia leptura Boulenger, 1901 MRAC 84-23-P-94, MRAC 84-23-P-82-88 Astatoreochromis straeleni (Poll, 1944) MRAC 73-68-P-171 Astatoreochromis vanderhorsti (Greenwood, 1954) BMNH 953.11.4.59-62 Bathybates ferox Boulenger, 1898 MRAC 14134, MRAC 14202, MRAC 112209 Bathybates leo Poll, 1956 MRAC 112492-496, MRAC 112502 Bathybates vittatus Boulenger, 1914 MRAC 112487-489 Benthochromis tricoti (Poll, 1948) MRAC 115121, MRAC 112546 Callochromis macrops (Boulenger, 1899) MRAC 108010-12 Callochromis pleurospilus (Boulenger, 1906) MRAC 108271-314 Cardiopharynx schoutedeni Poll, 1942 MRAC 85-12-P-77-90 Chalinochromis brichardi Poll, 1974 Ctenochromis benthicola (Matthes, 1962) MRAC 82-12-P-270 Ctenochromis horei (Gunther, 1893) NMW 24660 Cunningtonia longiventralis Boulenger, 1906 MRAC 107177 Cyathopharynx furcifer (Boulenger, 1899) MRAC 107023-027 Cyphotilapia frontosa (Boulenger, 1906) NMW 89983 Cyprichromis leptosoma (Boulenger, 1898) Cyprichromis microlepidotus (Poll, 1956) MRAC 126408-419 Ectodus descampsii Boulenger, 1899 MRAC 115378-79, 42678 Enantiopus melanogenys Boulenger, 1899 Eretmodus cyanostictus Boulenger, 1899 MRAC 77-11-P-59-147 Gnathochromis permaxillaris (David, 1936) MRAC 107260-262 Gnathochromis pfefferi (Boulenger, 1898) MRAC 129696, MRAC 107194, MRAC 77-35-P-28 Grammatotria lemairii Boulenger, 1899 MRAC 108510 Greenwoodochromis christyi (Trewavas, 1953) MRAC 94-031-P-0018-0019 Hemibates stenosoma (Boulenger, 1901) MRAC 112105, MRAC 112134-136 Julidochromis dickfeldi Staeck, 1975 NMW 90004: 1-4 Julidochromis ornatus Boulenger, 1899 MRAC 84-23-P-604-605 Julidochromis regani Poll, 1942 Julidochromis transcriptus Matthes, 1959 NMW 90005: 1-4 Lamprologus congoensis Schilthius, 1891 NMW 90008 Lamprologus werneri Poll, 1959 NMW 90009 Lepidiolamprologus elongatus (Boulenger, 1899) MRAC 63761-767 Lepidiolamprologus profundicola (Poll, 1949) MRAC 78-25-P-354-355 Lestradea perspicax Poll, 1943 MRAC 45036-037 Lestradea stappersii (Poll, 1943) MRAC 106659-699 Limnochromis abeelei Poll, 1949 MRAC 107283-284 Limnochromis auritus (Boulenger, 1901) MRAC 107215-217 Limnotilapia dardennii (Boulenger, 1899) MRAC 106014-020 Lobochilotes labiatus (Boulenger, 1898) MRAC 45736, MRAC 106278-284 Microdontochromis tenuidentatus Poll, 1951 MRAC 115445-466 Neolamprologus brevis (Boulenger, 1899) MRAC 81-62-P-77-117 Neolamprologus brichardi (poll, 1974) NMW90019 Neolamprologus longior (Staeck, 1980) NMW 90020: 1-2 Neolamprologus moorii (Boulenger, 1899) MRAC 190464-465 Neolamprologus ocellatus (Steindachner, 1909) Neolamprologus tetracanthus (Boulenger, 1899) NMW 90021: 1-5 Neolamprologus tretocephalus (Boulenger, 1899) MRAC 129085-086 Ophthalmotilapia boops (Boulenger, 1901) MRAC 107148-150 Ophthalmotilapia nasuta (Poll & Matthes, 1962) MRAC 78-25-P-586-589 Orthochromis malagaraziensis (David, 1936) MRAC 55783-824, BMNH 1953.11.4.46-58 Paleolamprologus toae (Poll, 1949) MRAC 83-33-P-221-224 766 E. LIPPITSCH

Paracyprichromis brieni Poll, 1981 MRAC 84-23-P-175-179 Paracyprichromis nigripinnis (Boulenger, 1901) Perissodus microlepis Boulenger, 1899 MRAC 76-4-P-256-258 Petrochromis polyodon Boulenger, 1898 MRAC 53086-088 Petrochromis trewavasae Poll, 1948 MRAC 78-25-P-639-648 Plecodus multidentatus Poll, 1952 MRAC 115687, MRAC 94-031P-0020 Plecodus paradoxus Boulenger, 1898 MRAC 112706-708 Pseudosimochromis curvifrons (Poll, 1942) MRAC 76-4-P-481, MRAC 78-25-P-691-692 Reganochromis calliurus (Boulenger, 1901) MRAC 84-44-P-443, MRAC 108658-659 Rhamphochromis macrophthalmus Regan, 1922 Simochromis diagramma (Gunther, 1893) MRAC 106388-393 Simochromis loocki (Poll, 1949) MRAC 106266, MRAC 106270 Spathodus erythrodon Boulenger, 1900 MRAC 76-9-P-195, MRAC 76-4-P-165-166 Tangachromis dhanisi (Poll, 1949) MRAC 94-068-P-0127, MRAC 107302 Tanganicodus irsacae Poll, 1950 MRAC 84-09-P-337-340 Teleogramma brichardi Poll, 1959 NMW 90041 Telmatochromis temporalis Boulenger, 1899 NMW 90042 Telmatochromis vittatus Boulenger, 1899 MRAC 78-25-P-717-719 Telotrematocara macrostoma (Poll, 1952) MRAC 74-22-P-1-3 Trematocara marginatum Boulenger, 1899 MRAC 110370-396 Trematocara variabile Poll, 1953 MRAC 93-152-P-82-91 Triglachromis otostigma (Regan, 1920) MRAC 115362-363 Tropheus duboisi Marlier, 1959 NMW 90045 Tropheus moorii Boulenger, 1899 NMW 90046 Tylochromis lateralis (Boulenger, 1898) NMW 24456 Xenochromis hecqui Boulenger, 1899 MRAC 112569-572 Xenotilapia ochrogenys (Boulenger, 1914) MRAC 76-28-P-124-126 Xenotilapia sima Boulenger, 1899 MRAC 80616-617