The Role of Alternative Splicing and Differential Gene Expression in Cichlid Adaptive Radiation

Abstract

Species diverge eco-morphologically through the continuous action of natural selection on functionally important structures, producing alternative adaptive morphologies. In cichlid fishes, the oral and pharyngeal jaws are such key structures. Adaptive variation in jaw morphology contributes to trophic specialization, which is hypothesized to fuel their rapid speciation in the East African Great Lakes. Much is known about the genes involved in cichlid jaw and craniofacial development. However, it is still unclear what salient sources of variation gave rise to trophic-niche specialization, facilitating adaptive radiation. Here, we explore two sources of transcriptional variation that may underlie species-specific disparities in jaw morphology. Using whole transcriptome RNA-sequencing, we analyze differences in gene expression and alternative splicing, at the end of postlarval development, in fully functional jaws of six species of cichlids from the Lake Tanganyika tribe Tropheini. Our data reveal a surprisingly high degree of alternative splicing events compared with gene expression differences among species and trophic types. This suggests that differential trophic adaptation of the jaw apparatus may have been shaped by transcriptional rewiring of splicing as well as gene expression variation during the rapid radiation of the Tropheini. Specifically, genes undergoing splicing across most species were found to be enriched for pharyngeal jaw gene ontology terms. Overall, jaw transcriptional patterns at postlarval developmental stage were highly dynamic and species-specific. In conclusion, this work indicates that shifts in alternative splicing could have played a more important role in cichlid adaptive radiation, and possibly adaptive radiation in general, than currently recognized.

Rapid establishment of a flowering cline in Medicago polymorpha after invasion of North America

“…Using genetic markers to determine the geographical origins of an invasive plant species, we can determine whether a phenotypic cline present in the invaded range has been transported intact from numerous points of origin across a cline that already exists in the native range, or whether a cline has evolved from founders from a single region of origin. There are several mechanisms by which introduced species can adapt to environmental variation across a novel geographical range, such as genetic interactions during admixture, the presence of large effect alleles in founding populations, epigenetic processes and transcriptional variation such as alternative splicing (reviewed in Ellstrand & Schierenbeck, 2000;Dlugosch, Anderson, Braasch, Cang, & Gillette, 2015;Estoup et al, 2016;Patalano et al, 2015;Singh, Börger, More, & Sturmbauer, 2017;Price et al, 2018). Polymorphisms in loci that have regulatory roles would be able to alter a wide range of physiological processes, including those that could underlie clinal variation (Mitchell-Olds & Schmitt, 2006).…”

Enhanced plasticity of programmed DNA elimination boosts adaptive potential in suboptimal environments

“…Finally, we explored the possible impact of IES retention on cellular functions and found that IES-containing genes are significantly more likely to be involved in processes such as signal transduction, cellular protein modification, and transport of ions across membranes (Table 1) . These results open the possibility that, much like the eukaryotic cellular process of alternative RNA splicing (Lewis et al 2003; Wong et al 2013; Braunschweig et al 2014; Marquez et al 2015; Singh et al 2017; Smith et al 2018a) , regulated IES retention in Paramecium might fine tune gene expression and/or generate alternative DNA splicing isoforms which may ultimately facilitate adaptation to environmental changes.…”

Developmental processes regulate craniofacial variation in disease and evolution

“…Splicing patterns have rapidly diverged in vertebrate evolution, and likely had a more important role in species‐specific phenotypes than do alterations to overall gene expression levels (Barbosa‐Morais et al, ). In a comparison of the jaws of six different species of cichlids, differences in splicing were found to be much higher than overall gene expression differences, suggesting that alterations to splicing may facilitate rapid divergence (Singh, Borger, More, & Sturmbauer, ). Increased alternative splicing has contributed to extensive proteomic diversity in mammals, and especially primates, relative to other clades (Barbosa‐Morais et al, ; Gueroussov et al, ).…”