Abstract
BackgroundVariation in locomotor capacity among animals often reflects adaptations to different environments. Despite evidence that physical performance is heritable, the molecular basis of locomotor performance and performance trade-offs remains poorly understood. In this study we identify the genes, signaling pathways, and regulatory processes possibly responsible for the trade-off between burst performance and endurance observed in Xenopus allofraseri, using a transcriptomic approach.ResultsWe obtained a total of about 121 million paired-end reads from Illumina RNA sequencing and analyzed 218,541 transcripts obtained from a de novo assembly. We identified 109 transcripts with a significant differential expression between endurant and burst performant individuals (FDR ≤ 0.05 and logFC ≥2), and blast searches resulted in 103 protein-coding genes. We found major differences between endurant and burst-performant individuals in the expression of genes involved in the polymerization and ATPase activity of actin filaments, cellular trafficking, proteoglycans and extracellular proteins secreted, lipid metabolism, mitochondrial activity and regulators of signaling cascades. Remarkably, we revealed transcript isoforms of key genes with functions in metabolism, apoptosis, nuclear export and as a transcriptional corepressor, expressed in either burst-performant or endurant individuals. Lastly, we find two up-regulated transcripts in burst-performant individuals that correspond to the expression of myosin-binding protein C fast-type (mybpc2). This suggests the presence of mybpc2 homoeologs and may have been favored by selection to permit fast and powerful locomotion.ConclusionThese results suggest that the differential expression of genes belonging to the pathways of calcium signaling, endoplasmic reticulum stress responses and striated muscle contraction, in addition to the use of alternative splicing and effectors of cellular activity underlie locomotor performance trade-offs. Ultimately, our transcriptomic analysis offers new perspectives for future analyses of the role of single nucleotide variants, homoeology and alternative splicing in the evolution of locomotor performance trade-offs.
Highlights
Variation in locomotor capacity among animals often reflects adaptations to different environments
Kinectin 1, a receptor for kinesin that accumulates in integrin-based adhesion complexes, is up-regulated in endurant individuals, whereas mef2a, a DNA-binding transcription factor of we found a differential expression of several protein-coding genes related to cellular trafficking and the Golgi apparatus
Whereas one major factor contributing to the differences in contractile properties between fiber types is the presence of different myosin heavy chain (MHC) isoforms [78, 79], we found the third most up-regulated transcripts in burst-performant individuals (LOC108701289) to be an ortholog of Xenopus tropicalis speg gene, which encodes a protein with similarity to members of the myosin light chain kinase family
Summary
Variation in locomotor capacity among animals often reflects adaptations to different environments. Despite evidence that physical performance is heritable, the molecular basis of locomotor performance and performance trade-offs remains poorly understood. In this study we identify the genes, signaling pathways, and regulatory processes possibly responsible for the trade-off between burst performance and endurance observed in Xenopus allofraseri, using a transcriptomic approach. The evolution of locomotor performance can be constrained if performance traits are involved in traded-offs, as often observed between burst performance and endurance capacity in vertebrates [4,5,6,7,8,9]. The physiological basis of this performance trade-off has been documented, how it is governed at the gene expression level remains poorly understood. Uncovering the molecular basis and biological pathways underlying performance trade-offs is essential for understanding the adaptive evolution of these traits
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