The transcriptional state and chromatin landscape of cichlid jaw shape variation across species and environments

Abstract

Adaptive phenotypes are shaped by a combination of genetic and environmental forces, and while the literature is rich with studies focusing on either genetics or environment contributions, those that consider both are rare. Here we utilize the cichlid oral jaw apparatus to fill this knowledge-gap. First, we employed RNA-seq in bony and ligamentous tissues important for jaw opening to identify differentially expressed genes between species and across foraging environments. Our foraging treatments were designed to force animals to employ either suction or biting/scraping, which broadly mimic pelagic or benthic modes of feeding. We found a large number of differentially expressed genes between species, and while we identified relatively few differences between environments, species differences were far more pronounced when reared in the pelagic versus benthic environment. Further, these data carried the signature of genetic assimilation, and implicated cell cycle regulation in shaping the jaw across species and environments. Next, we repeated the foraging experiment and performed ATAC-seq procedures on nuclei harvested from the same tissues. Cross-referencing results from both analyses revealed subsets of genes that were both differentially expressed and differentially accessible in either the pelagic (n=15) or the benthic environment (n=11), as well as loci where differences were robust to foraging environment (n=13). All in all, these data provide novel insights into the epigenetic, genetic, and cellular bases of species- and environment-specific bone shapes, as well as the evolution of phenotypic plasticity in this iconic model system.

Foraging-induced craniofacial plasticity is associated with an early, robust and dynamic transcriptional response

“…Pelagic foraging also drove differences in slopes between MG and the other two species, whereas slopes were statistically indistinguishable between species when reared under benthic foraging conditions (table 2). This finding is also consistent with previous work [23] showing that the pelagic environment drives species differences at the transcript level. In TO , slopes were nearly identical between treatments for both the CL and OL (figure 3 b ), indicating similar growth rates; however, we note that benthic foragers exhibited generally longer OLs, relative to head length, which suggests a degree of plasticity in this element.…”

“…Conversely, LF exhibited comparatively lower gene expression levels across all markers and timepoints. Trends in gene expression were not only observed among the environmentally sensitive genes selected from our genome-wide dataset [23], but across nearly all bone markers, suggesting that the pattern was not an artefact of choosing a biased set of genes, but rather an intrinsic feature of the larger bone regulatory network.…”

“…We queried a panel of 11 genes including six environmentally sensitive loci from a genome-wide study (i.e. actr6 , asb5 , capn1l , cdc20 , gnmt , kiaa0586 [23]), and five additional genes based on known roles in bone development, mechanical stimulation and remodelling ( sp7 , opg , rankl , ptch1 , notch1a ). See primer sequences in electronic supplementary material, table S2.…”

“…Recently, we took a multiomics approach to identify environmentally sensitive genes that underlie species- and environment-specific differences in jaw shapes in cichlid fishes. Focusing on functionally relevant elements of the feeding apparatus (figure 1 a ), we used overlapping RNA-seq and ATAC-seq datasets to assess differences in transcription levels and chromatin accessibility at single time-points following the onset of foraging challenges [23]. Here, we seek to characterize the expression dynamics of a subset of genes identified from that study over time, and compare them to anatomical shifts over the same time interval.…”

“…Tropheops species are benthic foragers that mainly specialize on attached algae; however, many species within this complex consume a range of food items, including plankton and detritus. Plasticity of the feeding apparatus has previously been described for Maylandia and Tropheops species at the anatomical and transcript levels [14,21,23]. By contrast, Labeotropheus species are extreme benthic specialists, well adapted to consume tough, filamentous, attached algae and characterized by reduced levels of craniofacial plasticity [14,21].…”