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Phylogeography and Ecological Niche Shape the Cichlid Fish Gut Microbiota in Central American and African Lakes.

ABSTRACT: Cichlid fishes, with their repeated colonization of lakes and subsequent radiations at different scales of phylogenetic and ecological diversification, offer an excellent model system to understand the factors shaping the host-gut microbiota association in nature. Here, we characterized the gut microbiota of the Amphilophus species complex from Central America (known as the Midas cichlid complex), encompassing 158 wild specimens (13 species) collected from seven Nicaraguan lakes, and combined these data with previously published data from two African lakes (spanning 29 species). Our aim was to comprehensively explore trends in microbiota variation and persistence along the large spatial and temporal scales of cichlid diversification (from the oldest radiation in L. Tanganyika, 9-12 My old, to young ones in Nicaraguan crater lakes, <0.5 My old), in allopatry and sympatry (within and across lakes), and across the range of dietary niches (from highly specialized to generalist feeders). Despite their extraordinary diversity, cichlids shared a remarkably conserved microbial taxonomic profile, which argues for a primary role of the host genetics in the assembly and maintenance of these microbial communities. Within this partly constrained microbiota profile, geographic isolation (continent and lake) represented the first level of discrimination. For the Midas cichlid, a partial congruency was found between host microbiota and genetic distances, suggesting that microbial communities have partly diversified along their cichlid phylogeographic history of crater lake colonization. In sympatry (within lakes), the young and poorly ecologically diversified cichlid assemblages of Central American lakes display largely unresolved gut microbiotas (in terms of both alpha and beta diversities), whereas the phylogenetically and ecologically diverse species found in African lakes showed greater microbial interspecific diversity. This pattern largely points to the level of habitat segregation, trophic niche overlap, and reproductive barriers as major modulators of the gut microbiota connectivity among sympatric species.

SUBMITTER: Baldo L

PROVIDER: S-EPMC6803461 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Phylogeography and Ecological Niche Shape the Cichlid Fish Gut Microbiota in Central American and African Lakes.

Baldo Laura L Riera Joan Lluís JL Salzburger Walter W Barluenga Marta M

Frontiers in microbiology 20191015

Cichlid fishes, with their repeated colonization of lakes and subsequent radiations at different scales of phylogenetic and ecological diversification, offer an excellent model system to understand the factors shaping the host-gut microbiota association in nature. Here, we characterized the gut microbiota of the <i>Amphilophus</i> species complex from Central America (known as the Midas cichlid complex), encompassing 158 wild specimens (13 species) collected from seven Nicaraguan lakes, and comb ...[more]

PMID: 31681230

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Project description:BackgroundCichlids are a prime model system in evolutionary research and several of the most prominent examples of adaptive radiations are found in the East African Lakes Tanganyika, Malawi and Victoria, all part of the East African cichlid radiation (EAR). In the past, great effort has been invested in reconstructing the evolutionary and biogeographic history of cichlids (Teleostei: Cichlidae). In this study, we present new divergence age estimates for the major cichlid lineages with the main focus on the EAR based on a dataset encompassing representative taxa of almost all recognized cichlid tribes and ten mitochondrial protein genes. We have thoroughly re-evaluated both fossil and geological calibration points, and we included the recently described fossil †Tugenchromis pickfordi in the cichlid divergence age estimates.ResultsOur results estimate the origin of the EAR to Late Eocene/Early Oligocene (28.71 Ma; 95% HPD: 24.43-33.15 Ma). More importantly divergence ages of the most recent common ancestor (MRCA) of several Tanganyika cichlid tribes were estimated to be substantially older than the oldest estimated maximum age of the Lake Tanganyika: Trematocarini (16.13 Ma, 95% HPD: 11.89-20.46 Ma), Bathybatini (20.62 Ma, 95% HPD: 16.88-25.34 Ma), Lamprologini (15.27 Ma; 95% HPD: 12.23-18.49 Ma). The divergence age of the crown haplochromine H-lineage is estimated to 22.8 Ma (95% HPD: 14.40-26.32 Ma) and of the Lake Malawi radiation to 4.07 Ma (95% HDP: 2.93-5.26 Ma). In addition, we recovered a novel lineage within the Lamprologini tribe encompassing only Lamprologus of the lower and central Congo drainage with its divergence estimated to the Late Miocene or early Pliocene. Furthermore we recovered two novel mitochondrial haplotype lineages within the Haplochromini tribe: 'Orthochromis' indermauri and 'Haplochormis' vanheusdeni.ConclusionsDivergence time estimates of the MRCA of several Tanganyika cichlid tribes predate the age of the extant Lake Tanganyika basin, and hence are in line with the recently formulated "Melting-Pot Tanganyika" hypothesis. The radiation of the 'Lower Congo Lamprologus clade' might be linked with the Pliocene origin of the modern lower Congo rapids as has been shown for other Lower Congo cichlid assemblages. Finally, the age of origin of the Lake Malawi cichlid flock agrees well with the oldest age estimate for lacustrine conditions in Lake Malawi.

Project description:The African cichlid fish radiations are the most diverse extant animal radiations and provide a unique system to test predictions of speciation and adaptive radiation theory. The past few years have seen major advances in the phylogenetics, evolutionary biogeography and ecology of cichlid fish. Most of this work has concentrated on the most diverse radiations. Unfortunately, a large number of small radiations and 'non-radiations' have been overlooked, potentially limiting the contribution of the cichlid system to our understanding of speciation and adaptive radiation. I have reviewed the literature to identify 33 intralacustrine radiations and 76 failed radiations. For as many as possible I collected information on lake size, age and phylogenetic relationships. I use these data to address two questions: (i) whether the rate of speciation and the resulting species richness are related to temporal and spatial variation in ecological opportunity and (ii) whether the likelihood of undergoing adaptive radiation is similar for different African cichlid lineages. The former is a key prediction of the ecological theory of adaptive radiation that has been presumed true but remains untested for cichlid radiations. The second is based on the hypothesis that the propensity of cichlids to radiate is due to a key evolutionary innovation shared by all African cichlids. The evidence suggests that speciation rate declines through time as niches get filled up during adaptive radiation: young radiations and early stages of old radiations are characterized by high rates of speciation, whereas at least 0.5 Myr into a radiation speciation becomes a lot less frequent. The number of species in cichlid radiations increases with lake size, supporting the prediction that species diversity increases with habitat heterogeneity, but also with opportunity for isolation by distance. Finally, the data suggest that the propensity to radiate within lakes is a derived property that evolved during the evolutionary history of some African cichlids, and the appearance of which does not coincide with the appearance of proposed key innovations in morphology and life history.

Project description:BackgroundThe patterns and processes linked to the host specificity of parasites represent one of the central themes in the study of host-parasite interactions. We investigated the evolution and determinants of host specificity in gill monogeneans of Cichlidogyrus and Scutogyrus species parasitizing African freshwater fish of Cichlidae.MethodsWe analyzed (1) the link between host specificity and parasite phylogeny, (2) potential morphometric correlates of host specificity (i.e. parasite body size and the morphometrics of the attachment apparatus), and (3) potential determinants of host specificity following the hypothesis of ecological specialization and the hypothesis of specialization on predictable resources (i.e. host body size and longevity were considered as measures of host predictability), and (4) the role of brooding behavior of cichlids in Cichlidogyrus and Scutogyrus diversification.ResultsNo significant relationships were found between host specificity and phylogeny of Cichlidogyrus and Scutogyrus species. The mapping of host specificity onto the parasite phylogenetic tree revealed that an intermediate specialist parasitizing congeneric cichlid hosts represents the ancestral state for the Cichlidogyrus/Scutogyrus group. Only a weak relationship was found between the morphometry of the parasites' attachment apparatus and host specificity. Our study did not support the specialization on predictable resources or ecological specialization hypotheses. Nevertheless, host specificity was significantly related to fish phylogeny and form of parental care.ConclusionsOur results confirm that host specificity is not a derived condition for Cichlidogyrus/Scutogyrus parasites and may reflect other than historical constraints. Attachment apparatus morphometry reflects only partially (if at all) parasite adaptation to the host species, probably because of the morphological similarity of rapidly evolved cichlids (analyzed in our study). However, we showed that parental care behavior of cichlids may play an important role linked to host specificity of Cichlidogyrus/Scutogyrus parasites.

Dataset Information

Phylogeography and Ecological Niche Shape the Cichlid Fish Gut Microbiota in Central American and African Lakes.

Publications

Phylogeography and Ecological Niche Shape the Cichlid Fish Gut Microbiota in Central American and African Lakes.

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