Synodontis Multipunctatus Research Articles

Revised taxonomy of Synodontis catfishes (Siluriformes: Mochokidae) from the Lake Tanganyika basin reveals lower species diversity than expected

Abstract Synodontis Cuvier, 1816 is a species-rich group of African catfishes. Prior to this analysis, 13 species of Synodontis were recognized from Lake Tanganyika and its tributaries, composing the only extant lacustrine radiation of the genus, with a unique origin of obligate brood parasitism among all fishes. Species differentiation and phylogenetic relationships of this group remained largely unresolved. Herein, the taxonomy of Synodontis in the Lake Tanganyika basin is revised, including redescriptions of all species and an updated identification key. Genetic (mitochondrial and nuclear genomic markers) and morphological data suggest a lower species diversity than previously recognized, supporting the distinction of 10 Synodontis species in the lake basin. Based on our findings, we recognize Synodontis grandiops, Synodontis ilebrevis, and Synodontis lucipinnis as junior synonyms of Synodontis multipunctatus, Synodontis polli, and Synodontis petricola, respectively. No recent material of Synodontis dhonti and Synodontis tanganyicae (with Synodontis lacustricolus as a synonym) was available. Morphometric/meristic data suggest their close relationship to Synodontis granulosus. Sequencing of historical specimens inferred S. tanganyicae as sister to S. granulosus but with a 1.7% divergence based on mitochondrial data. In contrast to previous studies, phylogenomic data support the lacustrine assemblage of Synodontis in Lake Tanganyika as monophyletic.

The evolution of brood parasitism from host egg predation

Abstract Obligate brood parasites pass all their parental duties to foster parents of a host species. While best understood in birds and hymenopteran insects, obligate brood parasitism has evolved independently at least 59 times across many lineages. The ancestors of brood parasites often provided no parental care to their offspring. Instead, a trophic association with their eventual hosts commonly appears to precede the origin of a brood parasitic strategy. Here, we used a game theoretical model to explore the conditions under which brood parasitism can evolve from predation and be maintained in the population. Our model was inspired by the relationship between the cuckoo catfish (Synodontis multipunctatus) parasitizing mouthbrooding cichlid fishes in the African Lake Tanganyika. Our model demonstrates the facilitatory role of host egg predation on the origin and evolutionary maintenance of brood parasitism through the exploitation of the host response to egg predation by brood parasites. We found no conditions under which brood parasitism as a pure strategy is evolutionarily stable, but we describe a range of evolutionarily stable equilibria when predators and parasites coexist. While our model is tailored to the cuckoo catfish, it generally applies to other systems where brood parasitism has evolved from other antagonistic behavior.

Lack of host specialization despite selective host use in brood parasitic cuckoo catfish.

Host-parasite dynamics involve coevolutionary arms races, which may lead to host specialization and ensuing diversification. Our general understanding of the evolution of host specialization in brood parasites is compromised by a restricted focus on bird and insect lineages. The cuckoo catfish (Synodontis multipunctatus) is an obligate parasite of parental care of mouthbrooding cichlids in Lake Tanganyika. Given the ecological and taxonomic diversity of mouthbrooding cichlids in the lake, we hypothesized the existence of sympatric host-specific lineages in the cuckoo catfish. In a sample of 779 broods from 20 cichlid species, we found four species parasitized by cuckoo catfish (with prevalence of parasitism of 2%-18%). All parasitized cichlids were from the tribe Tropheini, maternal mouthbrooders that spawn over a substrate (rather than in open water). Phylogenetic analysis based on genomic (ddRAD sequencing) and mitochondrial (Dloop) data from cuckoo catfish embryos showed an absence of host-specific lineages. This was corroborated by analyses of genetic structure and co-ancestry matrix. Within host species, parasitism was not associated with any individual characteristic we recorded (parent size, water depth), but was costly as parasitized parents carried smaller clutches of their own offspring. We conclude that the cuckoo catfish is an intermediate generalist and discuss costs, benefits and constraints of host specialization in this species and brood parasites in general.

Low incidence of cannibalism among brood parasitic cuckoo catfish embryos.

Brood parasites have demanding needs of host resources. Brood parasitic offspring are highly competitive and frequently cause the failure of host broods and the survival of a single parasitic offspring. Accordingly, virulent brood parasites lay a single egg in the same host nest to avoid sibling competition. In the cuckoo catfish (Synodontis multipunctatus), which parasitize mouthbrooding cichlid fishes in Lake Tanganyika, the modes of host and parasite oviposition lead to frequent cases of multiple parasitism. We experimentally tested the prediction that multiple parasitism leads to frequent cannibalism among offspring. Cuckoo catfish embryos prey upon host offspring to obtain nourishment during their 3-week development in the host buccal cavity and may also consume conspecific embryos. The potential benefits of cannibalism in the system are, therefore, twofold; to decrease competition for limited resources (i.e., host brood with rich yolk sacs) and to directly obtain nourishment by consuming rivals. We found that cannibalism indeed provided measurable benefits in terms of increased growth of the cannibals, but cannibalism was rare and typically occurred once all host offspring had been consumed. This implies that cannibalism among cuckoo catfish embryos emerges to mitigate starvation rather than eliminate competition.

Individual experience as a key to success for the cuckoo catfish brood parasitism

Brood parasites are involved in coevolutionary arms races with their hosts, whereby adaptations of one partner elicit the rapid evolution of counter-adaptations in the other partner. Hosts can also mitigate fitness costs of brood parasitism by learning from individual or social experience. In brood parasites, however, the role of learning can be obscured by their stealthy behaviour. Cuckoo catfish (Synodontis multipunctatus) parasitise clutches of mouthbrooding cichlids in Lake Tanganyika and are the only non-avian obligate brood parasites among vertebrates. We experimentally demonstrate that cuckoo catfish greatly enhance their efficiency in parasitising their hosts as they learn to overcome host defences. With increasing experience, cuckoo catfish increased their parasitism success by greater efficiency through improved timing and coordination of intrusions of host spawnings. Hence, within the coevolutionary arms races, brood parasites learn to overcome host defences during their lifetime.

Group intrusions by a brood parasitic fish are not cooperative

Abstract Brood parasites relegate all parental duties to unrelated hosts. Host resistance against brood parasitism is most effective during egg laying and is best countered by surreptitious oviposition. This may be aided through distraction of host attention by the male partner or a larger cooperative group. Cuckoo catfish (Synodontis multipunctatus) parasitize the broods of mouthbrooding cichlids, which collect their eggs immediately after oviposition. Cuckoo catfish must time their intrusion precisely, as the temporal window for parasitism lasts only a few seconds. As the cuckoo catfish typically intrude host spawning as a group, we tested whether groups of catfish distract spawning cichlid pairs more successfully than a single catfish pair. We found that larger catfish groups were not more effective in parasitism, as parasitism success by groups of three catfish pairs increased only proportionally to single catfish pairs. The number of cichlid eggs in host clutches decreased at high catfish abundance, apparently due to elevated cuckoo catfish predation on the eggs. Hence, group intrusions do not represent cooperative actions, but incur an increased cost to the host cichlid from greater egg predation by cuckoo catfish.

Brood parasitism of an open-water spawning cichlid by the cuckoo catfish.

The cuckoo catfish Synodontis multipunctatus and S. grandiops are endemic to Lake Tanganyika and the only known nonavian vertebrates that exhibit obligate interspecific brood parasitism. Seven maternal mouth-brooding cichlid fish species are reported to be natural hosts of the parasitic catfish and share a common reproductive behaviour that the catfish exploits: cichlid females spawn eggs on the bottom, allowing the catfish female to place her eggs near the cichlid eggs, and the cichlid females collect the catfish eggs by mouth together with their own eggs. However, so far it has not been reported that the cuckoo catfish exploit different spawning behaviours. The genus Cyprichromis consists of five maternal mouth-brooding species endemic to Lake Tanganyika, most of which spawn and collect eggs in open water. This study reports that the cuckoo catfish also parasitizes the open-water spawning Cyprichromis coloratus, although it may not be a regular host.

Cuckoo catfish

Martin Reichard introduces the cuckoo catfish, the only obligatory brood parasite among vertebrates that is not a bird.

This cuckoo catfish tricks other fish into raising its head-chomping young

This cuckoo catfish tricks other fish into raising its head-chomping young

Early life-history features associated with brood parasitism in the cuckoo catfish, Synodontis multipunctatus (Siluriformes: Mochokidae).

The cuckoo catfish, Synodontis multipunctatus, is the only known obligate brood parasite among fishes, exploiting the parental care of mouthbrooding cichlids endemic to Lake Tanganyika. Comparisons of this system to brood parasitism in birds may reveal broader principles that underlie the evolution of this life-history strategy in vertebrates. However, little is known about the features of the cuckoo catfish that enable this species to successfully parasitize cichlids. Here, we examine early ontogeny of the cuckoo catfish and compare it to that of its cichlid hosts as well as a non-parasitic congener. We found that cuckoo catfish embryos develop and hatch in advance of host embryos, and begin feeding on cichlid young just as they start to hatch. Overall timing of ontogeny in the cuckoo catfish was found to be similar to that of the substrate-spawning congener Synodontis lucipinnis, suggesting that more rapid development of the cuckoo catfish relative to cichlids is not a unique adaptation to brood parasitism. However, we found that cuckoo catfish progeny exhibit extensive morphological differences from S. lucipinnis, which may represent adaptations to brood parasitism. These life-history observations reveal both similarities and differences between the cuckoo catfish system and brood parasitism in other lineages. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

Parasitic cuckoo catfish exploit parental responses to stray offspring.

Interspecific brood parasitism occurs in several independent lineages of birds and social insects, putatively evolving from intraspecific brood parasitism. The cuckoo catfish, Synodontis multipunctatus, the only known obligatory non-avian brood parasite, exploits mouthbrooding cichlid fishes in Lake Tanganyika, despite the absence of parental care in its evolutionary lineage (family Mochokidae). Cuckoo catfish participate in host spawning events, with their eggs subsequently collected and brooded by parental cichlids, though they can later be selectively rejected by the host. One scenario for the origin of brood parasitism in cuckoo catfish is through predation of cichlid eggs during spawning, eventually resulting in a spatial and temporal match in oviposition by host and parasite. Here we demonstrate experimentally that, uniquely among all known brood parasites, cuckoo catfish have the capacity to re-infect their hosts at a late developmental stage following egg rejection. We show that cuckoo catfish offspring can survive outside the host buccal cavity and re-infect parental hosts at a later incubation phase by exploiting the strong parental instinct of hosts to collect stray offspring. This finding implies an alternative evolutionary origin for cuckoo catfish brood parasitism, with the parental response of host cichlids facilitating its evolution. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

A laboratory study of host use by the cuckoo catfish Synodontis multipunctatus

The only known non-avian vertebrate obligate brood parasite is the cuckoo catfish (Synodontis multipunctatus), a Lake Tanganyikan endemic. The cuckoo catfish parasitizes Tanganyikan mouthbrooding cichlids, and under captive conditions, will also parasitize cichlids from other Rift Valley lakes. Here we examine the frequency of parasitism by the cuckoo catfish of Ctenochromis horei from Lake Tanganyika and three species from Lake Malawi and the greater Lake Victorian system in a laboratory setting. C. horei was parasitized significantly less (17%) than the allopatric species Haplochromis latifasciatus, Haplochromis nubilus, and Metriaclima estherae (combined parasitism rate of 28%). The lower rates of parasitism in C. horei may be due to differences in the mating ritual, oviposition (e.g., long periods of pseudo-spawning before actual oviposition), and behavioral adaptations (e.g., increased aggression towards the cuckoo catfish). The number of catfish eggs per parasitized brood was similar between C. horei, H. latifasciatus, H. nubilus, and M. estherae. Our results are comparable to findings from the field for C. horei parasitism frequency and number of cuckoo catfish per brood. We also analyzed the parasitism rate of the albino morph of Metriaclima zebra, a domestic strain. Parasitism rates and number of catfish per brood were the highest in the albino morphotype suggesting that the higher levels of parasitism may be related to lower aggressive behavior, lower visual acuity, or captive influence. Cuckoo catfish and mouthbrooding cichlids provide a model system for testing brood parasitism in a laboratory setting.

Success of cuckoo catfish brood parasitism reflects coevolutionary history and individual experience of their cichlid hosts.

Obligate brood parasites manipulate other species into raising their offspring. Avian and insect brood parasitic systems demonstrate how interacting species engage in reciprocal coevolutionary arms races through behavioral and morphological adaptations and counteradaptations. Mouthbrooding cichlid fishes are renowned for their remarkable evolutionary radiations and complex behaviors. In Lake Tanganyika, mouthbrooding cichlids are exploited by the only obligate nonavian vertebrate brood parasite, the cuckoo catfish Synodontis multipunctatus. We show that coevolutionary history and individual learning both have a major impact on the success of cuckoo catfish parasitism between coevolved sympatric and evolutionarily naïve allopatric cichlid species. The rate of cuckoo catfish parasitism in coevolved Tanganyikan hosts was 3 to 11 times lower than in evolutionarily naïve cichlids. Moreover, using experimental infections, we demonstrate that parasite egg rejection in sympatric hosts was much higher, leading to seven times greater parasite survival in evolutionarily naïve than sympatric hosts. However, a high rejection frequency of parasitic catfish eggs by coevolved sympatric hosts came at a cost of increased rejection of their own eggs. A significant cost of catfish parasitism was universal, except for coevolved sympatric cichlid species with previous experience of catfish parasitism, demonstrating that learning and individual experience both contribute to a successful host response.

Contrasting geographic structure in evolutionarily divergent Lake Tanganyika catfishes.

Geographic isolation is suggested to be among the most important processes in the generation of cichlid fish diversity in East Africa's Great Lakes, both through isolation by distance and fluctuating connectivity caused by changing lake levels. However, even broad scale phylogeographic patterns are currently unknown in many non‐cichlid littoral taxa from these systems. To begin to address this, we generated restriction‐site‐associated DNA sequence (RADseq) data to investigate phylogeographic structure throughout Lake Tanganyika (LT) in two broadly sympatric rocky shore catfish species from independent evolutionary radiations with differing behaviors: the mouthbrooding claroteine, Lophiobagrus cyclurus, and the brood‐parasite mochokid, Synodontis multipunctatus. Our results indicated contrasting patterns between these species, with strong lake‐wide phylogeographic signal in L. cyclurus including a deep divergence between the northern and southern lake basins. Further structuring of these populations was observed across a heterogeneous habitat over much smaller distances. Strong population growth was observed in L. cyclurus sampled from shallow shorelines, suggesting population growth associated with the colonization of new habitats following lake‐level rises. Conversely, S. multipunctatus, which occupies a broader depth range, showed little phylogeographic structure and lower rates of population growth. Our findings suggest that isolation by distance and/or habitat barriers may play a role in the divergence of non‐cichlid fishes in LT, but this effect varies by species.

Reproductive parasitism: male and female responses to conspecific and heterospecific intrusions at spawning in a mouth‐brooding cichlid Ophthalmotilapia ventralis

A rare form of alternative reproductive behaviour without simultaneous parasitic spawning was observed in Ophthalmotilapia ventralis, a lekking mouth-brooding cichlid from Lake Tanganyika. Floater males attempted to sneak opportunistically into the territory to actively court the female, while the owner (bourgeois male) defended the territory against other potential intruders. Floater males had more body fat than territory owners and generally higher condition factors. In field experiments, the response of bourgeois males and courted females was tested towards floaters and egg predators (a catfish Synodontis multipunctatus) present in the territories. Territory owners responded aggressively particularly to floaters, and female responsiveness to bourgeois male courtship tended to decline when floaters were present. The potential influence of reproductive parasitism on sexual selection in mouth-brooding cichlids is discussed.

Kinematics of benthic suction feeding in Callichthyidae and Mochokidae,with functional implications for the evolution of food scraping in catfishes

Food scraping has independently evolved twice from suction feeding in the evolution of catfishes: within neotropical Loricarioidea and paleotropical Mochokidae. To gain insight in the evolutionary transitions associated with the evolution towards scraping, we analyzed prey capture kinematics in two species of benthic suction feeders which belong to taxa that are closely related to the scraper lineages (respectively, Corydoras splendens and Synodontis multipunctatus), and compared it to prey capture in a more distantly related, generalist suction feeder (Clarias gariepinus). Simultaneous ventral and lateral view high-speed videos were recorded to quantify the movements of the lower jaw, hyoid, pectoral girdle and neurocranium. Additionally, ellipse modeling was applied to relate head shape differences to buccal expansion kinematics. Similarly to what has been observed in scrapers, rotations of the neurocranium are minimal in the benthic suction feeders, and may consequently have facilitated the evolution of a scraping feeding mechanism. The hypothesis that fish with a more laterally compressed head rely more heavily on lateral expansion of the buccal cavity to generate suction, was confirmed in our sample of catfish species. Since an important contribution of lateral expansion of the head to suction may avoid the need for a strong, ventral depression of the mouth floor during feeding, we hypothesized that this may have allowed a closer association with the substrate in the ancestors of scrapers. However, our hypothesis was not supported by an ancestral state reconstruction, which suggests that scraping probably evolved from sub-terminal mouthed ancestors with dorsoventrally flattened heads.

Developmental genetic mechanisms of evolutionary tooth loss in cypriniform fishes

The fossil record indicates that cypriniform fishes, a group including the zebrafish, lost oral teeth over 50 million years ago. Despite subsequent diversification of feeding modes, no cypriniform has regained oral teeth, suggesting the zebrafish as a model for studying the developmental genetic basis of evolutionary constraint. To investigate the mechanism of cypriniform tooth loss, we compared the oral expression of seven genes whose mammalian orthologs are involved in tooth initiation in the zebrafish and the Mexican tetra, Astyanax mexicanus, a related species retaining oral teeth. The most significant difference we found was an absence in zebrafish oral epithelium of expression of dlx2a and dlx2b, transcription factors that are expressed in early Astyanax odontogenic epithelium. Analysis of orthologous genes in the Japanese medaka (Oryzias latipes) and a catfish (Synodontis multipunctatus) suggests that expression was lost in cypriniforms, rather than gained in Astyanax. Treatment of Astyanax with an inhibitor of Fibroblast growth factor (Fgf) signaling produced a partial phenocopy of the zebrafish oral region, in that oral teeth, and expression of dlx2a and dlx2b, were lost, whereas shh and pitx2, genes whose expression is present in zebrafish oral epithelium, were unaffected. We hypothesize that a loss of Fgf signaling to oral epithelium was associated with cypriniform tooth loss.

Mitochondrial phylogeny and phylogeography of East African squeaker catfishes (Siluriformes: Synodontis)

BackgroundSqueaker catfishes (Pisces, Mochokidae, Synodontis) are widely distributed throughout Africa and inhabit a biogeographic range similar to that of the exceptionally diverse cichlid fishes, including the three East African Great Lakes and their surrounding rivers. Since squeaker catfishes also prefer the same types of habitats as many of the cichlid species, we hypothesized that the East African Synodontis species provide an excellent model group for comparative evolutionary and phylogeographic analyses.ResultsOur analyses reveal the existence of six major lineages of Synodontis in East Africa that diversified about 20 MYA from a Central and/or West African ancestor. The six lineages show a clear geographic patterning. Two lineages are endemic to Lake Tanganyika (plus one non-endemic representative), and these are the only two Synodontis lineages that diversified further into a small array of species. One of these species is the cuckoo catfish (S. multipunctatus), a unique brood parasite of mouthbrooding haplochromine cichlids, which seems to have evolved in parallel with the radiation of its cichlid host lineage, the Tropheini. We also detect an accelerated rate of molecular evolution in S. multipunctatus, which might be the consequence of co-evolutionary dynamics.ConclusionWe conclude that the ancestral lineage of today's East African squeaker catfish fauna has colonized the area before the Great Lakes have formed. This ancestor diversified rapidly into at least six lineages that inhabit lakes and rivers in East Africa. Lake Tanganyika is the only lake harboring a small species flock of squeaker catfishes.

Comparative study of otolith organs between two species of upside‐down swimming catfish Synodontis nigriventris showing converse swimming postures

AbstractTo clarify whether the unique postural control of the upside‐down swimming catfish (Synodontis nigriventris, family Mochokidae) is related to the histological characteristics of the otolith organs, we performed light microscopic observation of the utricle, the saccule and the lagena. The histological aspects of the otolith organs were compared between S. nigriventris and Synodontis multipunctatus, which belong to the same genus. S. multipunctatus usually shows upside‐up swimming posture except for feeding behaviour near water surface. As controls, we additionally used a miniature catfish, Corydoras paleatus and goldfish, Carassius auratus, which shows upside‐up swimming posture. We concluded that the structural aspects of the otolith organs did not cause the unique postural control of S. nigriventris. Light microscopic observation clarified the following aspects: (1) The utricle of S. nigriventris was located at the anterior region of the otocyst and under the semicircular canals, and the saccule and the lagena were located at the posteroventral region of the otocyst like those of S. multipunctatus and the other two fishes. (2) The hair cells of the utricle were arranged on the horizontal plane of the fishes with a variation in cell size at the ventral and ventrolateral sites in S. nigriventris, S. multipunctatus and the other two fishes. (3) The hair cells of the saccule and lagena of S. nigriventris, S. multipunctatus and C. auratus presented perpendicular to the horizontal plane of the fish. (4) Region‐specific differences in the size and shape of the hair cells of S. nigriventris were observed along the three‐dimensional axes of the otolith organs like those of S. multipunctatus and the other two fishes. It is unlikely that the unique postural control of upside‐down catfish is related to the localization of the utricle, the saccule and the lagena and the distribution of the different types of hair cell of the otolith organs. Furthermore, the distribution of the hair cells suggests that the otolith organs in S. nigriventris can detect three‐dimensional postural changes like the organs of other fishes showing generally observed upside‐up swimming posture.

Localization of the neuronal form of nitric oxide synthase (bNOS) in the diencephalon and pituitary gland of the catfish, Synodontis multipunctatus: an immunocytochemical study

The distribution of the neuronal form of nitric oxide synthase (bNOS) was investigated in the brain and pituitary gland of the catfish, Synodontis multipunctatus. Immunoreactive neurons were found mainly in the nucleus praeopticus periventricularis, the parvocellular and supraoptic subdivisions of the nucleus praeopticus, the nucleus recessus lateralis and the nucleus recessus posterioris. In addition, some scattered bNOS labeled somata were noted in the dorsal hypothalamic area. A few positive cells in the adenohypophysis and some reactive fibers in the pituitary stalk were also seen. Our results are compatible with the notion that the cells expressing bNOS in the diencephalon and hypophysis are involved in the control of hormone regulation. Moreover, the presence of bNOS positive cells in the rostral pars distalis of the pituitary gland supports a role of nitric oxide in osmoregulation.