mouthbrooding
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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.
- Klíčová slova
- brood parasitism, cichlid fish, embryo predation, mouthbrooding, siblicide, sibling competition,
- Publikační typ
- časopisecké články MeSH
Early offspring separation from mothers causes social deprivation. Mouthbrooding, when eggs and fry are incubated in the buccal cavity of the parent, is one of the reproductive strategies in fish. The mother is the incubating parent in African lake cichlids from the genus Tropheus. Many of these are produced in captivity and some producers use artificial incubators in which eggs are incubated separately from the mother. We hypothesized that this practice may dramatically modify the reproduction rate of fish individuals produced by the method of artificial incubation. The long-term experiment focused on Tropheus sp. "Caramba" had been carried out for 10 years when maternally incubated and separated individuals were compared. We found a negative effect of artificial egg and offspring incubation out of the mother's buccal cavity. The deprived females laid the same number of eggs as maternally incubated females, but most eggs were lost during the incubation. Moreover, the reproduction frequency was significantly lower in deprived females in comparison with those maternally incubated. This study should be perceived as preliminary. For this reason and with respect to welfare principles, we strongly recommend similarly designed experiments focused on other potentially sensitive fish mouthbrooders. Once the syndrome would be confirmed, we recommend avoiding artificial incubation of mouthbrooding fish in general.
- MeSH
- cichlidy * MeSH
- míra přežití MeSH
- rozmnožování MeSH
- sociální deprivace MeSH
- ústa MeSH
- zvířata MeSH
- Check Tag
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
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.
- Klíčová slova
- brood parasitism, fish, host specialisation, host-parasite relationship, interspecific interactions, social evolution,
- MeSH
- cichlidy * genetika MeSH
- fylogeneze MeSH
- hnízdění MeSH
- interakce hostitele a parazita genetika MeSH
- paraziti * MeSH
- sumci * genetika MeSH
- voda MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- voda MeSH
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.
- MeSH
- biologická evoluce * MeSH
- cichlidy fyziologie MeSH
- druhová specificita MeSH
- rozmnožování MeSH
- sumci fyziologie MeSH
- symbióza * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
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.
- MeSH
- cichlidy * MeSH
- fyziologická adaptace MeSH
- ptáci MeSH
- sumci * MeSH
- symbióza MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
The goals of this paper were to investigate phylogenetic and evolutionary patterns of cichlid fish from West Africa and their Cichlidogyrus and Scutogyrus monogenean parasites, to uncover the presence of host-parasite cospeciation and to assess the level of morphological adaptation in parasites. This required the following steps, each one representing specific objectives of this paper: (1) to build phylogenetic trees for Cichlidogyrus and Scutogyrus species based on ribosomal DNA sequences, (2) to investigate phylogenetic relationships within West African cichlid fish based on the analysis of mitochondrial cytochrome b DNA sequences, (3) to investigate host-parasite cophylogenetic history to gain clues on parasite speciation process, and (4) to investigate the link between the morphology of the attachment apparatus and parasite phylogeny. Phylogenetic analyses supported the monophyletic origin of the Cichlidogyrus/Scutogyrus group, and suggested that Cichlidogyrus is polyphyletic and that Scutogyrus is monophyletic. The phylogeny of Cichlidae supported the separation of mouthbrooders and substrate-brooders and is consistent with the hypothesis that the mouthbrooding behavior of Oreochromis and Sarotherodon evolved from substrate-brooding behavior. The mapping of morphological characters of the haptor onto the parasite phylogenetic tree suggests that the attachment organ has evolved from a very simple form to a more complex one. The cophylogenetic analyses indicated a significant fit between trees using distance-based tests, but no significant cospeciation signal using tree-based tests, suggesting the presence of parasite duplications and host switches on related host species. This shed some light on the diversification process of Cichlidogyrus species parasitizing West African cichlids.
- MeSH
- biologická evoluce * MeSH
- cichlidy parazitologie MeSH
- fylogeneze MeSH
- interakce hostitele a parazita * MeSH
- ploštěnci klasifikace genetika MeSH
- ribozomální DNA MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- ribozomální DNA MeSH
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'.
- Klíčová slova
- brood parasite, cichlidae, coevolutionary arms race, host–parasite evolution,
- MeSH
- cichlidy parazitologie MeSH
- hnízdění MeSH
- interakce hostitele a parazita * MeSH
- sumci růst a vývoj fyziologie MeSH
- zvířata MeSH
- Check Tag
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Obligate brood parasites delegate the workload of costly parental care to their hosts. Theory predicts that release from demanding parental care increases the importance of other factors to shape mating patterns. However, behavioural observations and parentage estimates are notoriously difficult to obtain in species with covert reproductive strategies, such as brood parasites, and evidence for their mating strategies are scarce. Molecular genetic methods provide a powerful tool to identify concealed mating patterns. Here, we reconstruct the parentage of cuckoo catfish (Synodontis multipunctatus) clutches collected in the wild using a combination of newly developed microsatellite markers, mitochondrial markers, and maximum likelihood estimates of pairwise relatedness. Cuckoo catfish parasitise mouthbrooding cichlids in Lake Tanganyika, but a natural spawning of the brood parasite has never been observed. We examined 429 females of confirmed host cichlid species (parasitism prevalence 6%; 24 parasitised clutches with 1-14 embryos) and found that 46% of clutches with three or more offspring (i.e., 6 out of 13) were parented by more than two catfish individuals. We demonstrated variable mating patterns including polyandrous and polygynous mating, and host sharing by separate, genetically monogamous, catfish pairs. This indicates that cuckoo catfish parasitism involves groups of catfish with reduced capability to monopolise mating opportunities. In general, our results demonstrate how reproductive strategy and mating patterns in a species with concealed breeding behaviour can be investigated and provide valuable insights into the mating system of a brood parasitic species other than hitherto studied avian brood parasites.
- Klíčová slova
- Synodontis multipunctatus, African cichlids, Lake Tanganyika, parentage analysis, reproductive parasitism, reproductive success,
- MeSH
- cichlidy parazitologie MeSH
- hnízdění MeSH
- jezera MeSH
- mikrosatelitní repetice MeSH
- mitochondriální DNA genetika MeSH
- pravděpodobnostní funkce MeSH
- rozmnožování genetika MeSH
- sexuální chování zvířat * MeSH
- sumci * genetika fyziologie parazitologie MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- mitochondriální DNA MeSH