Tracing evolutionary decoupling of oral and pharyngeal jaws in cichlid fishes.
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ABSTRACT:
SUBMITTER: Ronco F
PROVIDER: S-EPMC8645199 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Evolutionary constraints may significantly bias phenotypic change, while "breaking" from such constraints can lead to expanded ecological opportunity. Ray-finned fishes have broken functional constraints by developing two jaws (oral-pharyngeal), decoupling prey capture (oral jaw) from processing (pharyngeal jaw). It is hypothesized that the oral and pharyngeal jaws represent independent evolutionary modules and this facilitated diversification in feeding architectures. Here we test this hypothesis in African cichlids. Contrary to our expectation, we find integration between jaws at multiple evolutionary levels. Next, we document integration at the genetic level, and identify a candidate gene, smad7, within a pleiotropic locus for oral and pharyngeal jaw shape that exhibits correlated expression between the two tissues. Collectively, our data show that African cichlid evolutionary success has occurred within the context of a coupled jaw system, an attribute that may be driving adaptive evolution in this iconic group by facilitating rapid shifts between foraging habitats, providing an advantage in a stochastic environment such as the East African Rift-Valley.
| S-EPMC8445992 | biostudies-literature
Project description:East African cichlid fishes represent one of the most striking examples of rapid and convergent evolutionary radiation among vertebrates. Models of ecological speciation would suggest that functional divergence in feeding morphology has contributed to the origin and maintenance of cichlid species diversity. However, definitive evidence for the action of natural selection has been missing. Here we use quantitative genetics to identify regions of the cichlid genome responsible for functionally important shape differences in the oral jaw apparatus. The consistent direction of effects for individual quantitative trait loci suggest that cichlid jaws and teeth evolved in response to strong, divergent selection. Moreover, several chromosomal regions contain a disproportionate number of quantitative trait loci, indicating a prominent role for pleiotropy or genetic linkage in the divergence of this character complex. Of particular interest are genomic intervals with concerted effects on both the length and height of the lower jaw. Coordinated changes in this area of the oral jaw apparatus are predicted to have direct consequences for the speed and strength of jaw movement. Taken together, our results imply that the rapid and replicative nature of cichlid trophic evolution is the result of directional selection on chromosomal packages that encode functionally linked aspects of the craniofacial skeleton.
| S-EPMC154331 | biostudies-literature
Project description:BackgroundMajor modifications to the pharyngeal jaw apparatus are widely regarded as a recurring evolutionary key innovation that has enabled adaptive radiation in many species-rich clades of percomorph fishes. However one of the central predictions of this hypothesis, that the acquisition of a modified pharyngeal jaw apparatus will be positively correlated with explosive lineage diversification, has never been tested. We applied comparative methods to a new time-calibrated phylogeny of labrid fishes to test whether diversification rates shifted at two scales where major pharyngeal jaw innovations have evolved: across all of Labridae and within the subclade of parrotfishes.ResultsDiversification patterns within early labrids did not reflect rapid initial radiation. Much of modern labrid diversity stems from two recent rapid diversification events; one within julidine fishes and the other with the origin of the most species-rich clade of reef-associated parrotfishes. A secondary pharyngeal jaw innovation was correlated with rapid diversification within the parrotfishes. However diversification rate shifts within parrotfishes are more strongly correlated with the evolution of extreme dichromatism than with pharyngeal jaw modifications.ConclusionThe temporal lag between pharyngeal jaw modifications and changes in diversification rates casts doubt on the key innovation hypothesis as a simple explanation for much of the richness seen in labrids and scarines. Although the possession of a secondarily modified PJA was correlated with increased diversification rates, this pattern is better explained by the evolution of extreme dichromatism (and other social and behavioral characters relating to sexual selection) within Scarus and Chlorurus. The PJA-innovation hypothesis also fails to explain the most dominant aspect of labrid lineage diversification, the radiation of the julidines. We suggest that pharyngeal jaws might have played a more important role in enabling morphological evolution of the feeding apparatus in labrids and scarines rather than in accelerating lineage diversification.
| S-EPMC2779191 | biostudies-literature
Project description:BackgroundPost-transcriptional regulation is crucial for the control of eukaryotic gene expression and might contribute to adaptive divergence. The three prime untranslated regions (3' UTRs), that are located downstream of protein-coding sequences, play important roles in post-transcriptional regulation. These regions contain functional elements that influence the fate of mRNAs and could be exceptionally important in groups such as rapidly evolving cichlid fishes.ResultsTo examine cichlid 3' UTR evolution, we 1) identified gene features in nine teleost genomes and 2) performed comparative analyses to assess evolutionary variation in length, functional motifs, and evolutionary rates of 3' UTRs. In all nine teleost genomes, we found a smaller proportion of repetitive elements in 3' UTRs than in the whole genome. We found that the 3' UTRs in cichlids tend to be longer than those in non-cichlids, and this was associated, on average, with one more miRNA target per gene in cichlids. Moreover, we provided evidence that 3' UTRs on average have evolved faster in cichlids than in non-cichlids. Finally, analyses of gene function suggested that both the top 5% longest and 5% most rapidly evolving 3' UTRs in cichlids tended to be involved in ribosome-associated pathways and translation.ConclusionsOur results reveal novel patterns of evolution in the 3' UTRs of teleosts in general and cichlids in particular. The data suggest that 3' UTRs might serve as important meta-regulators, regulators of other mechanisms governing post-transcriptional regulation, especially in groups like cichlids that have undergone extremely fast rates of phenotypic diversification and speciation.
| S-EPMC5987618 | biostudies-literature
Project description:BackgroundFishes in the families Cichlidae and Labridae provide good probable examples of vertebrate adaptive radiations. Their spectacular trophic radiations have been widely assumed to be due to structural key innovation in pharyngeal jaw apparatus (PJA), but this idea has never been tested based on a reliable phylogeny. For the first step of evaluating the hypothesis, we investigated the phylogenetic positions of the components of the suborder Labroidei (including Pomacentridae and Embiotocidae in addition to Cichlidae and Labridae) within the Percomorpha, the most diversified (> 15,000 spp) crown clade of teleosts. We examined those based on 78 whole mitochondrial genome sequences (including 12 newly determined sequences) through partitioned Bayesian analyses with concatenated sequences (13,933 bp).ResultsThe resultant phylogenies indicated that the Labridae and the remaining three labroid families have diverged basally within the Percomorpha, and monophyly of the suborder was confidently rejected by statistical tests using Bayes factors.ConclusionThe resultant phylogenies indicated that the specified PJA evolved independently at least twice, once in Labridae and once in the common ancestor of the remaining three labroid families (including the Cichlidae). Because the independent evolution of pharyngeal jaws appears to have been followed by trophic radiations, we consider that our result supports, from the aspect of historical repeatability, the idea that the evolution of the specialized PJA provided these lineages with the morphological potential for their spectacular trophic radiations. The present result will provide a new framework for the study of functional morphology and genetic basis of their PJA.
| S-EPMC1797158 | biostudies-literature
Project description:Cichlid fishes are exceptionally species-rich, speciated at explosive rates and, hence, are a model system in speciation research. Yet, their reproductive isolating barriers have, so far, not been comprehensively studied. Here, we review current knowledge on pre- and postzygotic mechanisms in cichlids. While premating isolation is the norm in cichlids, its strength varies across lineages and with the geographical setting. Moreover, manipulations of ambient conditions tended to reduce assortative mating among closely related species, suggesting that premating isolation in cichlids is often fragile and context dependent. The observed lack of complete reproductive isolation is supported by past and present hybridization events that have contributed to diversity by creating novel allelic combinations. On the other hand, our meta-analysis highlights that intrinsic postzygotic isolation might accumulate faster than assumed. Mild forms of genetic incompatibilities, such as sex ratio distortion, can already be observed among closely related species. Therefore, cessation of gene flow by strong reproductive isolation in cichlids requires a combination of premating prezygotic isolation supplemented with intrinsic and extrinsic postzygotic barriers. Further, we suggest crucial next steps to improve our knowledge about reproductive barriers in cichlids to understand the evolutionary dynamics of pre- and postzygotic isolation mechanisms during adaptive radiations. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.
| S-EPMC7423275 | biostudies-literature
Project description:Color patterns in African cichlid fishes vary spectacularly. Although phylogenetic analysis showed already 30 years ago that many color patterns evolved repeatedly in these adaptive radiations, only recently have we begun to understand the genomic basis of color variation. Horizontal stripe patterns evolved and were lost several times independently across the adaptive radiations of Lake Victoria, Malawi, and Tanganyika and regulatory evolution of agouti-related peptide 2 (agrp2/asip2b) has been linked to this phenotypically labile trait. Here, we asked whether the agrp2 locus exhibits particular characteristics that facilitate divergence in color patterns. Based on comparative genomic analyses, we discovered several recent duplications, insertions, and deletions. Interestingly, one of these events resulted in a tandem duplication of the last exon of agrp2. The duplication likely precedes the East African radiations that started 8-12 Ma, is not fixed within any of the radiations, and is found to vary even within some species. Moreover, we also observed variation in copy number (two to five copies) and secondary loss of the duplication, illustrating a surprising dynamic at this locus that possibly promoted functional divergence of agrp2. Our work suggests that such instances of exon duplications are a neglected mechanism potentially involved in the repeated evolution and diversification that deserves more attention.
| S-EPMC6916709 | biostudies-literature
Project description:A comparative cytogenetic analysis was carried out in five species of a monophyletic clade of neotropical Cichlasomatine cichlids, namely Cleithracara maronii Steindachner, 1881, Ivanacara adoketa (Kullander & Prada-Pedreros, 1993), Nannacara anomala Regan, 1905, N. aureocephalus Allgayer, 1983 and N. taenia Regan, 1912. Karyotypes and other chromosomal characteristics were revealed by CDD banding and mapped onto the phylogenetic hypothesis based on molecular analyses of four genes, namely cyt b, 16S rRNA, S7 and RAG1. The diploid numbers of chromosomes ranged from 44 to 50, karyotypes were composed predominantly of monoarmed chromosomes and one to three pairs of CMA3 signal were observed. The results showed evolutionary reduction in this monophyletic clade and the cytogenetic mechanisms (fissions/fusions) were hypothesized and discussed.
| S-EPMC4205487 | biostudies-literature
Project description:Theory proposes that genomic admixture between formerly reproductively isolated populations can generate phenotypic novelty for selection to act upon. Secondary contact may therefore be a significant promoter of phenotypic novelty that allows species to overcome environmental challenges and adapt to novel environments, including during adaptive radiation. To date, this has largely been considered from the perspective of interspecific hybridization at contact zones. However, it is also possible that this process occurs more commonly between natural populations of a single species, and thus its importance in adaptive evolution may have been underestimated. In this study, we tested the consequences of genomic introgression during apparent secondary contact between phenotypically similar lineages of the riverine cichlid fish Astatotilapia calliptera. We provide population genetic evidence of a secondary contact zone in the wild, and then demonstrate using mate-choice experiments that both lineages can reproduce together successfully in laboratory conditions. Finally, we show that genomically admixed individuals display extreme phenotypes not observed in the parental lineages. Collectively, the evidence shows that secondary contact can drive the evolution of phenotypic novelty, suggesting that pulses of secondary contact may repeatedly seed genetic novelty, which when coupled with ecological opportunity could promote rapid adaptive evolution in natural circumstances.
| S-EPMC4262179 | biostudies-literature
Project description:BackgroundColor vision plays a critical role in visual behavior. An animal's capacity for color vision rests on the presence of differentially sensitive cone photoreceptors. Spectral sensitivity is a measure of the visual responsiveness of these cones at different light wavelengths. Four classes of cone pigments have been identified in vertebrates, but in teleost fishes, opsin genes have undergone gene duplication events and thus can produce a larger number of spectrally distinct cone pigments. In this study, we examine the question of large-scale variation in color vision with respect to individual, sex and species that may result from differential expression of cone pigments. Cichlid fishes are an excellent model system for examining variation in spectral sensitivity because they have seven distinct cone opsin genes that are differentially expressed.ResultsTo examine the variation in the number of cones that participate in cichlid spectral sensitivity, we used whole organism electrophysiology, opsin gene expression and empirical modeling. Examination of over 100 spectral sensitivity curves from 34 individuals of three species revealed that (1) spectral sensitivity of individual cichlids was based on different subsets of four or five cone pigments, (2) spectral sensitivity was shaped by multiple cone interactions and (3) spectral sensitivity differed between species and correlated with foraging mode and the spectral reflectance of conspecifics. Our data also suggest that there may be significant differences in opsin gene expression between the sexes.ConclusionsOur study describes complex opponent and nonopponent cone interactions that represent the requisite neural processing for color vision. We present the first comprehensive evidence for pentachromatic color vision in vertebrates, which offers the potential for extraordinary spectral discrimination capabilities. We show that opsin gene expression in cichlids, and possibly also spectral sensitivity, may be sex-dependent. We argue that females and males sample their visual environment differently, providing a neural basis for sexually dimorphic visual behaviour. The diversification of spectral sensitivity likely contributes to sensory adaptations that enhance the contrast of transparent prey and the detection of optical signals from conspecifics, suggesting a role for both natural and sexual selection in tuning color vision.
| S-EPMC2988715 | biostudies-literature