Abstract
BackgroundTeleosts display a spectacular diversity of craniofacial adaptations that often mediates ecological specializations. A considerable amount of research has revealed molecular players underlying skeletal craniofacial morphologies, but less is known about soft craniofacial phenotypes. Here we focus on an example of lip hypertrophy in the benthivorous Lake Tangnayika cichlid, Gnathochromis permaxillaris, considered to be a morphological adaptation to extract invertebrates out of the uppermost layer of mud bottom. We investigate the molecular and regulatory basis of lip hypertrophy in G. permaxillaris using a comparative transcriptomic approach.ResultsWe identified a gene regulatory network involved in tissue overgrowth and cellular hypertrophy, potentially associated with the formation of a locally restricted hypertrophic lip in a teleost fish species. Of particular interest were the increased expression level of apoda and fhl2, as well as reduced expression of cyp1a, gimap8, lama5 and rasal3, in the hypertrophic lip region which have been implicated in lip formation in other vertebrates. Among the predicted upstream transcription factors, we found reduced expression of foxp1 in the hypertrophic lip region, which is known to act as repressor of cell growth and proliferation, and its function has been associated with hypertrophy of upper lip in human.ConclusionOur results provide a genetic foundation for future studies of molecular players shaping soft and exaggerated, but locally restricted, craniofacial morphological changes in fish and perhaps across vertebrates. In the future, we advocate integrating gene regulatory networks of various craniofacial phenotypes to understand how they collectively govern trophic and behavioural adaptations.
Highlights
Teleost fishes show striking adaptive diversity in their craniofacial anatomy, which reflects an striking variety of ecological and trophic specializations
The low reads for some of the samples limit the results of our study to differentially expressed (DE) genes that have relatively high expression levels, in other words, it is likely that some of the low expressed genes are not detected among the list of DE genes due to the low coverage of some samples
We investigated the soft-tissue craniofacial trait of the hypertrophic lip in G. permaxillaris, in a comparative transcriptomic framework with G. bellcrossi, which are both from the Limnochromini tribe belonging to the cichlid adaptive radiation of Lake Tanganyika
Summary
Teleost fishes show striking adaptive diversity in their craniofacial anatomy, which reflects an striking variety of ecological and trophic specializations. A novel model system for adaptive radiation, the molecular mechanisms underlying exaggerated soft-tissue morphologies in lip, nose and nuchal hump phenotypes have been addressed only recently [6,7,8,9,10,11]. The exaggerated thickening of the lip might not follow a uniform pattern across the entire upper and lower lip and the extent of lip hypertrophy is significantly reduced in captivity under flake food diet, when the fish are not using this foraging strategy, so that lip hypertrophy seems highly dependent on foraging performance, making it a phenotypically plastic trait [12] Both genetic and phenotypic plasticity take part in the adaptive morphogenesis of this phenotype [6, 15]. We investigate the molecular and regulatory basis of lip hypertrophy in G. permaxillaris using a comparative transcriptomic approach
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