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A phylogenetic overview of the lamprologine cichlids of Africa (Teleostei, Cichlidae): A morphological perspective

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The phylogenetic relationship of the speciose and ecologically diverse lamprologine cichlids of Africa are investigated utilising a range of anatomical data. The monophyly of the group is firmly established and the basal position of Variabilichromis moorii, an hypothesis originally inferred from molecular data is supported. Within the lamprologine clade a large monophyletic subclade, the so-called 'ossified group', is recognised. As membership within the 'ossified group' includes species currently arrayed among three lamprologine 'genera', the present study poses a challenge to current taxonomic convention and highlights the need for continued study. The relationship of the lamprologine clade to other African cichlid lineages is investigated and while anatomical evidence is far from compelling, a case is made for a sistergroup relationship with the Zairean genus, Teleogramma and a more distal relationship to the west African / Zairean genus, Steatocranus, is tentatively posited.
... (1986) classification of the Lake Tanganyika cichlid assemblage. Most lamprologines are found in lacustrine habitats (Poll, 1986;Stiassny, 1997). About 90% of the species are restricted to Lake Tanganyika and associated rivers and streams, while 10% are found in the remaining Congo River drainage. ...
... Since 1959, only two Congo River species have been described, both based on very small numbers of specimens with narrowly restricted distributions: L. symoensi Poll, 1976, and L. lethops Roberts and Stewart, 1976, which is the only known blind cichlid. This history suggests, tantalizingly, that the sampling of Congo River lamprologine diversity is far from complete, and in the course of the present study two additional riverine species have been recognized, bringing the total of known species to eight. 3 Recently, the intrarelationships of lamprologines have been investigated, and with lamprologine monophyly well supported by both morphological (Stiassny, 1997) and molecular (Sturmbauer et al., 1994;Salzburger et al., 2002) evidence, speculation has turned to the nature and number of major evolutionary transitions within the clade. Some of the most intriguing of these questions are whether ancestral lamprologines arose in rivers or lakes, and the number of transitions between the two modalities in the history of the group. ...
... Poll's (1986) classification of his tribe Lamprologini restricted the genus Lamprologus to include the Congo River species and 11 Lake Tanganyika species on the basis of their all having the second or third pelvic fin ray the longest, as opposed to the condition seen in the remaining lamprologines in which the first ray is the longest. However, this scheme is undercut by Stiassny's (1997) labial ossification character. In members of several lamprologine genera, including 8 of the 11 Lake Tanganyika Lamprologus, a fully ossified sesamoid bone is suspended in the labial ligament, but no such bone occurs in any of the Congo River species. ...
... The cichlid tribe Lamprologini forms a major component of the endemic fish fauna of Lake Tanganyika, with about 80 species distributed in seven (Poll, 1986), eight, or possibly nine (Stiassny, 1997) genera. An additional eight species are known only from the Congo River, and one spe-cies only from the Malagarasi River (Schelly & Stiassny, 2004;Schelly et al., 2003). ...
... They are also absent in Chalinochromis, a genus not examined by Colombé & Allgayer, and in Altolamprologus Poll (1986), species of which were included in Neolamprologus by Colombé & Allgayer. In the remaining genera at least the dermosphenotic or other infraorbital ossicles are present (Stiassny, 1997;Schelly, 2007). The type species of Neolamprologus is N. tetracanthus (Boulenger, 1899a). ...
... Poll (1986) synonymized the monotypic Variabilichromis and Paleolamprologus, in which infraorbitals are present. Stiassny (1997) resurrected Variabilichromis with reference to the presence of infraorbital ossicles and basal position in the tree of Sturmbauer et al. (1994). Paleolamprologus has remained in synonymy of Neolamprologus, but Stiassny (1997) pointed out that in the only species, P. toae, there are six or seven infraorbital ossicles, contrasting with the other African cichlids, in which there are typically five when not reduced or co-ossified. ...
Article
Neolamprologus timidus, new species, is described from Ulwile Island and adjacent localities on the Tanzanian coast of Lake Tanganyika. The species was observed or collected along about 100 km of coastline from Kolwe Point, Cape Mpimbwe, south to Kisi Island. It is distinguished from the most similar species, N. furcifer, by presence of scales on most of the cheek, long pectoral fin and pelvic fin with the second ray longer than the first. Neolamprologus timidus is sympatric with N. furcifer at Kolwe Point and south to Kampempa Point, and at Lupita and Ulwile Islands south to Kisi Island, but N. furcifer is otherwise absent from the range of N. timidus. Two morphologically distinct forms are recognized in N. furcifer. Samples of N. furcifer from Ulwile Island and slightly more southern localities possess a caudal fin with rounded lobes and long middle rays, appearing only slightly emarginate. Samples of N. furcifer from Udachi and nearby localities possess pointed caudal-fin lobes with greatly elongated streamers, similar to N. timidus and to N. furcifer from other parts of Lake Tanganyika, including the type specimens from the southern part of the lake. The variation in caudal-fin shape may be an expression of character displacement as it occurs in the area of sympatry between N. timidus and N. furcifer. Mitochondrial DNA sequences are nearly identical in samples of N. furcifer with pointed or rounded caudal fin. A molecular phylogenetic analysis of a large set of lamprologin cichlids using two mitochondrial genes corroborates earlier analyses and places N. furcifer and N. timidus in different clades with different species of Neolamprologus, Julidochromis, Chalinochromis, and Telmatochromis despite sharing a unique combination of fin and body shape, and colour pattern. A 4648 base-pair multiloci analysis of a smaller number of species using fragments of three mitochondrial and two nuclear genes resolves N. furcifer and N. timidus in sister clades, but the N. timidus clade also includes Telmatochromis brachygnathus, and N. furcifer is sister species of Chalinochromis brichardi.
... One of these lineages, the tribe Lamprologini, comprises almost half of the entire cichlid diversity in Lake Tanganyika (Gante & Salzburger 2012;Wagner et al. 2012). Lamprologines show complex ecological, morphological, trophic and behavioural attributes, representing a radiation within the cichlid radiation (Stiassny 1997). Unlike other highly diverse cichlid lineages that display extreme levels of sexual dichromatism thought to promote their diversification, such as the radiations of haplochromine cichlids in lakes Malawi and Victoria (Wagner et al. 2012), most lamprologines are sexually monochromatic substrate spawners in which sexes share territorial defence and broodcare (Gante & Salzburger 2012). ...
... The tribe Lamprologini, to which Neolamprologus belongs, is the most species rich and also one of the most phenotypically diverse (in morphology, behaviour, life history) lineages of cichlids in Lake Tanganyika (Stiassny 1997;Gante & Salzburger 2012). We are just starting to acknowledge the various trophic adaptations (Muschick et al. 2012) and behaviours (Heg & Bachar 2006) that likely contributed to the lineage's evolutionary success. ...
Article
How variation in the genome translates into biological diversity and new species originate has endured as the mystery of mysteries in evolutionary biology. African cichlid fishes are prime model systems to address speciation-related questions for their remarkable taxonomic and phenotypic diversity, and the possible role of gene flow in this process. Here, we capitalize on genome sequencing and phylogenomic analyses to address the relative impacts of incomplete lineage sorting, introgression, and hybrid speciation in the Neolamprologus savoryi-complex (the ‘Princess cichlids’) from Lake Tanganyika. We present a time-calibrated species tree based on whole genome sequences, and provide strong evidence for incomplete lineage sorting in the early phases of diversification and multiple introgression events affecting different stages. Importantly, we find that the Neolamprologus chromosomes show center-to-periphery biases in nucleotide diversity, sequence divergence, GC content, incomplete lineage sorting, and rates of introgression, which are likely modulated by recombination density and linked selection. The detection of heterogeneous genomic landscapes has strong implications on the genomic mechanisms involved in speciation. Collinear chromosomal regions can be protected from gene flow and harbor incompatibility genes if they reside in lowly recombining regions, and coupling can evolve between non-physically linked genomic regions (chromosome centers in particular). Simultaneously, higher recombination toward chromosome peripheries makes these more dynamic, evolvable regions where adaptation polymorphisms have a fertile ground. Hence, differences in genome architecture could explain the levels of taxonomic and phenotypic diversity seen in taxa with collinear genomes, and might have contributed to the spectacular cichlid diversity observed today. This article is protected by copyright. All rights reserved.
... Members of the family Cichlidae, particularly those of the African Rift Valley lakes, are recognized as model systems for evolutionary studies in tropical freshwaters (e.g., Kocher, 2004;Salzburger, 2018;Santos & Salzburger, 2012). In Lake Tanganyika, within the Congo basin, cichlid diversity is dominated by members of the tribe Lamprologini and a number of species of Lamprologus are also distributed in the main channel of the Congo River (Schelly & Stiassny, 2004;Stiassny, 1997). Of the riverine Lamprologus, at least four species are endemic to the LCR: L. tigripictilis (Schelly & Stiassny, 2004), L. werneri (Poll, 1959), L. markerti (Tougas & Stiassny, 2014), and L. lethops (Roberts & Stewart, 1976). ...
Article
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Freshwater fishes are notably diverse, given that freshwater habitat represents a tiny fraction of the earth’s surface, but the mechanisms generating this diversity remain poorly understood. Rivers provide excellent models to understand how freshwater diversity is generated and maintained across heterogeneous habitats. In particular, the lower Congo River (LCR) consists of a dynamic hydroscape exhibiting extraordinary aquatic biodiversity, endemicity, morphological and ecological specialization. Previous studies have suggested that the numerous high‐energy rapids throughout the LCR form physical barriers to gene flow, thus facilitating diversification and speciation, generating ichthyofaunal diversity. However, this hypothesis has not been fully explored using genome‐wide SNPs for fish species distributed across the LCR. Here, we examined four lamprologine cichlids endemic to the LCR that are distributed along the river without range overlap. Using genome‐wide SNP data, we tested the hypotheses that high‐energy rapids serve as physical barriers to gene flow that generate genetic divergence at inter‐ and intraspecific levels, and that gene flow occurs primarily in a downstream direction. Our results are consistent with the prediction that powerful rapids sometimes act as a barrier to gene flow but also suggest that, at certain temporal and spatial scales, they may provide multidirectional dispersal opportunities for riverine rheophilic cichlid fishes. These results highlight the complexity of diversification processes in rivers and the importance of assessing such processes across different riverscapes.
... slender, unexpanded dorsal process). (3) Lamprologini: according to Stiassny (1997) characterized by a notched head of the hyomandibula (vs. not notched in †Rebekkachromis); more than three anal fin spines (see also Takahashi, 2003a) (vs. ...
Article
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The African Cichlidae Oreochromis (Alcolapia) and Oreochromis amphimelas can survive in extremely alkaline environments and represent the only known modern alkaliphilic cichlid fish found in Africa. The presence of fossil cichlids from the Miocene of central Kenya (Tugen Hills) that are morphologically similar to Oreochromis (Alcolapia) has been noted in previous works, but the conclusions remained tentative. The purpose of this study is to examine newly discovered fossil cichlids from the Tugen Hills and to compare their osteology with that of extant Oreochromis (Alcolapia). This is performed based on a comprehensive collection of comparative material, using microscopy and computed microtomography (μCT). We provide a revised diagnosis for the genus †Rebekkachromis, and revise its systematic relationships by assigning it to the Oreochromini (rather than to the Etiini). Two new species of †Rebekkachromis are described, i.e., †R. valyricus, sp. nov., and †R. vancouveringae, sp. nov., and a morphologically diverse assemblage of co-occurring †Rebekkachromis specimens is documented. Moreover, we found that †Rebekkachromis had three sensory canal pores (instead of four) on the lower arm of the preopercle, a feature that distinguishes both the modern Oreochromis (Alcolapia) and our fossil specimens from almost all other modern African cichlid fish. Our new data indicate that alkaliphile cichlids similar to Oreochromis (Alcolapia) were present in Central Kenya about 10-13 Ma ago and that the ability of African cichlid fishes to thrive in highly alkaline waters had already developed by that time. http://zoobank.org/urn:lsid:zoobank.
... Both features suggest that the new fossil does not exhibit the condition characteristic of the Trematocarini. Finally, †Warilochromis possesses only three anal fin spines (Fig. 4), and therefore differs from all members of the Lamprologini, which have more than three of these elements (Stiassny,[190]). ...
Article
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Background: The diversification process known as the Lake Tanganyika Radiation has given rise to the most speciose clade of African cichlids. Almost all cichlid species found in the lakes Tanganyika, Malawi and Victoria, comprising a total of 12-16 tribes, belong to this clade. Strikingly, all the species in the latter two lakes are members of the tribe Haplochromini, whose origin remains unclear. The 'out of Tanganyika' hypothesis argues that the Haplochromini emerged simultaneously with other cichlid tribes and lineages in Lake Tanganyika, presumably about 5-6 million years ago (MYA), and that their presence in the lakes Malawi and Victoria and elsewhere in Africa today is due to later migrations. In contrast, the 'melting pot Tanganyika hypothesis' postulates that Haplochromini emerged in Africa prior to the formation of Lake Tanganyika, and that their divergence could have begun about 17 MYA. Haplochromine fossils could potentially resolve this debate, but such fossils are extremely rare. Results: Here we present a new fossil haplochromine from the upper Miocene site Waril (9-10 million years) in Central Kenya. Comparative morphology, supported by Micro-CT imaging, reveals that it bears a unique combination of characters relating to dentition, cranial bones, caudal skeleton and meristic traits. Its most prominent feature is the presence of exclusively unicuspid teeth, with canines in the outer tooth row. †Warilochromis unicuspidatus gen. et sp. nov. shares this combination of characters solely with members of the Haplochromini and its lacrimal morphology indicates a possible relation to the riverine genus Pseudocrenilabrus. Due to its fang-like dentition and non-fusiform body, †W. unicuspidatus gen. et sp. nov. might have employed either a sit-and-pursue or sit-and-wait hunting strategy, which has not been reported for any other fossil haplochromine cichlid. Conclusions: The age of the fossil (9-10 MYA) is incompatible with the 'out of Tanganyika' hypothesis, which postulates that the divergence of the Haplochromini began only 5-6 MYA. The presence of this fossil in an upper Miocene palaeolake in the Central Kenya Rift, as well as its predatory lifestyle, indicate that Haplochromini were already an important component of freshwater drainages in East Africa at that time.
... Here, we investigate the phylogeographic structure in two closely related species of the Lake Tanganyika cichlid genus Altolamprologus, a member of the 'ossified group' within the tribe Lamprologini (Stiassny, 1997). The genus diverged from its sister group [1 MYA and includes only two described species, Altolamprologus compressiceps and A. calvus. ...
Article
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Stenotopic specialization to a fragmented habitat promotes the evolution of genetic structure. It is not yet clear whether small-scale population structure generally translates into large-scale intraspecific divergence. In the present survey of mitochondrial genetic structure in the Lake Tanganyika endemic Altolamprologus (Teleostei, Cichlidae), a rock-dwelling cichlid genus comprising A. compressiceps and A. calvus, habitat-induced population fragmentation contrasts with weak phylogeographic structure and recent divergence among genetic clades. Low rates of dispersal, perhaps along gastropod shell beds that connect patches of rocky habitat, and periodic secondary contact during lake level fluctuations are apparently sufficient to maintain genetic connectivity within each of the two Altolamprologus species. The picture of genetic cohesion was interrupted by a single highly divergent haplotype clade in A. compressiceps restricted to the northern part of the lake. Comparisons between mitochondrial and nuclear phylogenetic reconstructions suggested that the divergent mitochondrial clade originated from ancient interspecific introgression. Finally, ‘isolation-with-migration’ models indicated that divergence between the two Altolamprologus species was recent (67–142 KYA) and proceeded with little if any gene flow. As in other rock-dwelling cichlids, recent population expansions were inferred in both Altolamprologus species, which may be connected with drastic lake level fluctuations.
... Note on generic assignment. The generic-level classification of lamprologine cichlids is in need of thorough revision (Stiassny, 1997). Pending the results of a wide-ranging phylogenetic analysis (Schelly, in prep.), the new species described herein is provisionally placed in the genus Neolamprologus Colombe & Allgayer, 1985. ...
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Neolamprologus devosi sp. n., a new species of riverine lamprologine cichlid is described from the lower Malagarasi River, Tanzania. The new species is tentatively placed within the poorly defined genus Neolamprologus, though generic reassignment may be necessary once ongoing work on the phylo-geny and classification of lamprologines is completed. Notably, Neolamprologus devosi sp. n. does not present characters diagnostic of Congo (ex-Zaire) River lamprologines, and contrary to previous suggestions appears to be phylogenetically distinct from those taxa. This raises questions regarding the number of putative riverine colonizations of lamprologines from a lacustrine source.
... due in part to their highly autapomorphic morphology, determination of the interrelationships of Teleogramma within the Cichlidae has proven elusive in morphological analyses (e.g., Stiassny, 1997;takahashi and nakaya, 2001). however, a recent multilocus phylogeny (Schwarzer et al., 2014) provides conclusive support for the placement of Teleogramma as nested within the chromidotilapiine lineage of African cichlids. ...
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The lower Congo River and nearby habitats harbor numerous endemic lineages of cichlid fishes, including some with highly specialized morphologies. based on morphological and molecular data, we herein describe a new species of Teleogramma, a member of the chromi-dotilapiine clade found on rocky outcrops in the lower reaches of the middle Congo River. The new species, T. obamaorum, is distinguished from congeners by numerous morphological and ecological attributes, including the lack of dorsoventral head and body depression, absence of sexual dichromatism, and features of laterosensory anatomy, pharyngeal and gut morphology, and dietary preference. Phylogenetic analyses of two nuclear and two mitochondrial loci using bayesian and maximum-likelihood inference lend strong support for the taxonomic validity of T. obamaorum and provide preliminary estimates of species relationships within the genus. The discovery of a new, ecomorphologically distinctive cichlid species in the Congo River suggests that additional research focus on riverine clades has the potential to greatly contribute to our understanding of evolutionary dynamics in this hyperdiverse group of teleost fishes.
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Dentatherina merceri was compared with representatives of the superfamilies Phallostethoidea and Atherinoidea to determine whether Dentatherinidae is a sister group of the phallostethids. Histological examination of the labial nodules in D. merceri reveals that they have calcified cores with an outer cartilagenous rim. Fibrous connective tissue is known to change to hyaline or calcified cartilage or bone in response to stress in vertebrates. The nodules therefore, in the light of distinct histological morphological differences as well as from knowledge of morphogenetic processes, are not regarded as homologues of the paradentary in phallostethid fishes. It is believed that the presence of submaxillary bones in both of the above groups is a case of character convergence. Since parietals are absent in all Atherininae and most Australian atherinoids, this character is not unique to the phallostethids and Dentatherina. Absence of the dorsal postcleithrum is not unique to Dentatherina and the phallostethids and is therefore not regarded as a derived character establishing relationship. On the basis of the overall similarities of the first dorsal fin, interdorsal pterygiophores, the pelvic girdle, the supracleithrum, dorsal and ventral hypohyals, infraorbitals, and temporal canal, Dentatherina appears to share greater affinities with the Old World atherinoids than phallostethoids. As there is presently no evidence available to distinguish Taeniomembradinae from Atherininae, any affinities implied by Parenti (1984) between Dentatherina and the former, can also be regarded as affinities with the latter. Parenti's (1984) elevation of Dentatherininae to Dentatherinidae is accepted since this family can be distinguished from all other atherinoids by the presence of large lateral wings of the parasphenoid; maxilla with large spatulate process; anteriorly directed basal spine of the parhypural; one epural; and elongated ventral postcleithrum. The relationships of the phallostethoids may lie with fishes which are currently recognized as members of the family Melanotaeniidae. Further work is required to establish if this is so.
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This chapter focuses on the cichlid fauna of Lake Tanganyika, the least studied of the African Great Lakes. It places particular emphasis on the faunas of the rocky shore habitats, and explores the great species diversity that may have arisen. The chapter describes the evolutionary scenarios within the lake and the biology of these fishes. Several of the more parsimonious explanations as to how the extant species diversity is maintained are considered, and examples of resource partitioning among coexisting species along a variety of resources axes, the most likely mechanism of coexistence, are given. It also illustrates several examples of the diversity of feeding and breeding habits seen both within groups and within species. Moreover, the cichlids of Lake Tanganyika offer splendid, perhaps unique, opportunities for studies of ecology, behavior and evolution, yet there is a paucity of quantitative information concerning the ecology and evolution of its species flocks, such that our present level of knowledge is insufficient on which to form comprehensive theories regarding factors structuring these communities.
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Hunting behaviour is described for 18 individually identified fish of the piscivorous cichlid Lepidiolamprologus profundicola in Lake Tanganyika. When hunting, individuals of this species aim at, dash at and try to capture various kinds of prey fish. Most individuals exhibited only a few of nine documented hunting techniques, each of which was related to a particular microhabitat. These specializations were consistent during periods of more than 4 months. The hunting specializations of each fish were not a simple reflection of the relative abundance of the potential hunting places that each predator encountered; they were not always ascribable to intraspecific competition or phenotypes (size, sex, colour patterns); nor were they associated with specific prey species. Capture success rate was low, and failures to capture were due to rapid flight of the prey fish. It is suggested that individual specialized foraging behaviour was developed mainly through learning.
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