Research Article: Comparative transcriptome analysis reveals potential evolutionary differences in adaptation of temperature and body shape among four Percidae species

Date Published: May 7, 2019

Publisher: Public Library of Science

Author(s): Peng Xie, Shao-Kui Yi, Hong Yao, Wei Chi, Yan Guo, Xu-Fa Ma, Han-Ping Wang, Paolo Ruggeri.


Considering the divergent temperature habitats and morphological traits of four Percidae species: yellow perch (Perca flavescens), Eurasian perch (Perca fluviatilis), pike perch (Sander lucioperca), and ruffe (Gymnocephalus cernua), we stepped into the transcriptome level to discover genes and mechanisms that drive adaptation to different temperature environments and evolution in body shape. Based on 93,566 to 181,246 annotated unigenes of the four species, we identified 1,117 one-to-one orthologous genes and subsequently constructed the phylogenetic trees that are consistent with previous studies. Together with the tree, the ratios of nonsynonymous to synonymous substitutions presented decreased evolutionary rates from the D. rerio branch to the sub-branch clustered by P. flavescens and P. fluviatilis. The specific 93 fast-evolving genes and 57 positively selected genes in P. flavescens, compared with 22 shared fast-evolving genes among P. fluviatilis, G. cernua, and S. lucioperca, showed an intrinsic foundation that ensure its adaptation to the warmer Great Lakes and farther south, especially in functional terms like “Cul4-RING E3 ubiquitin ligase complex.” Meanwhile, the specific 78 fast-evolving genes and 41 positively selected genes in S. lucioperca drew a clear picture of how it evolved to a large and elongated body with camera-type eyes and muscle strength so that it could occupy the highest position in the food web. Overall, our results uncover genetic basis that support evolutionary adaptation of temperature and body shape in four Percid species, and could furthermore assist studies on environmental adaptation in fishes.

Partial Text

While reading the book Adaptation and Natural Selection, the preface sentence “Natural selection is the only acceptable explanation for the genesis and maintenance of adaptation,” will certainly resonate with ecologists [1]. Interestingly, “adaptive evolution” and “evolutionary adaptation” have been documented by researchers’ studies on numerous organisms; either way, natural selection is still the most critical part. Undoubtedly, both adaptation and evolution are inseparable from organisms and the environment. Organisms need to adapt to various environments, and in turn, specific environments drive the evolution of organisms. One of the fundamental concerns in molecular evolution often focuses on the role of adaptation, for instance, the relationship between adaptive evolution and neutral evolution [2]. In the process of evolution, the stresses that a species adapts to an environment often lead to adjustments of key genes, as well as changes in traits [3–6]—this is the power of selection. Thus, one of the central interests is to discover potential genes and mechanisms that are subject to such power. With advances in next-generation sequencing techniques and bioinformatic analyses, the ratio, numbers, and patterns of nonsynonymous and synonymous substitutions in protein-coding genes could be computed and applied to detect selection [7–11]. To be noted, RNA-seq is one of the frequently applied and efficient methods to reveal information like transcriptomes and expression of genes, even without genome annotation [12–14].

Given that yellow perch populations are widely distributed in the North American continent, and isolated by both geographic and genetic distances to some extent [66], we could imply that the southeast populations had already adapted to the warmer regions. The yellow and European perch diverged at 19.8 million years ago during the early Miocene Epoch, while the divergence time among Perca, pike perch, and ruffe should also be tens of million years ago [60]. Thus, environmental stress should have accumulated enough selection during the adaptive evolution among these species. In the respect to evolution, high ratios of dN/dS generally suggest the frequent occurrence of adaptive evolution with a high rate of functional protein divergence arising from direction selection, which also indicates the role and strength of natural selection in phenotypic evolution and divergence among species [67]. With comparisons among genomes, one can study the evolution of genes and other genomic sequences and how molecular evolution relates to adaptation and phenotypic evolution at the organismic level, concerning fast-evolving and positively selected genes that attribute to natural selection on beneficial alleles in driving DNA sequence evolution.

The four Percidae fish involved in this study showed differences in adaptation to temperature environment and body shape, to some extent. Although the findings of this study are not able to confirm any “signature of selection”, there are indications that selective processes in the transcriptome could be enacted to allow these Percidae fish to locally adapt to different ranges of temperature, and explain the evolutionary difference in body shape, to some extent. We identified the fast-evolving and positively selected genes among these four Percidae fish with O. niloticus and D. rerio as references, so as to predict molecular insights into ecological niche partitioning and divergent adaptation involved in the evolutionary race [159, 160]. However, referring to Stepien et al.’s comprehensive study on evolutionary and adaptive issues of perch [66], we realized that our study lacked sufficient geographic populations and phylogenetic species to emphasize more powerful and inherent mechanisms responsible for evolution. Moreover, quantitative trait locus (QTL) were also necessary for expounding the power of natural selection and genetic mutation/drift [161]. Nevertheless, the naturally selected genes and mechanisms presented in this study attract our further interest in studying the influence of temperature on the adaptation and growth of fish.




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