Evolution of Digestive Enzymes and RNASE1 Provides Insights into Dietary Switch of Cetaceans

Abstract

Although cetaceans (whales, porpoises, and dolphins) have multi-chambered stomachs, feeding habits of modern cetaceans have dramatically changed from herbivorous to carnivorous. However, the genetic basis underlying this dietary switch remains unexplored. Here, we present the first systematic investigation of 10 digestive enzymes genes (i.e., CYP7A1, CTRC, LIPC, LIPF, PNLIP, PGC, PRSS1, SI, SLC5A1, and TMPRSS15) of representative cetaceans, and the evolutionary trajectory of RNASE1 in cetartiodactylans. Positive selections were detected with proteinases (i.e., CTRC, PRSS1, and TMPRSS15) and lipases (i.e., CYP7A1, LIPF, and PNLIP) suggesting that cetaceans have evolved an enhanced digestion capacity for proteins and lipids, the major nutritional components of their prey (fishes and invertebrates). In addition, it was found that RNASE1 gene duplicated after the cetartiodactylan speciation and two independent gene duplication events took place in Camelidae and Ruminantia. Positive selection was detected with RNASE1 of Camelidae and Bovidae, suggesting enhanced digestive efficiency in the ruminants. Remarkably, even though the ancestors of cetaceans were terrestrial artiodactyls that are herbivorous, modern cetaceans lost the pancreatic RNASE1 copy with digestive function, which is in accordance with the dietary change from herbivorous to carnivorous. In sum, this is the first study that provides new insights into the evolutionary mechanism of dietary switch in cetaceans.

Comparative functional analysis of ribonuclease 1 homologs: molecular insights into evolving vertebrate physiology

“…A similar phenomenon is known to have occurred in leaf-eating monkeys, where a secondary form of RNase 1 evolved to participate in ruminant-like digestion [31]. Analogously, modern whales and dolphins, which share a common ancestor with cattle, seemingly lost their extra copies of RNase 1 concurrent to switching from a herbivorous to a carnivorous diet [32]. Taken together, extant evidence suggests that cow RNase A—the original so-called “pancreatic ribonuclease”—might be a functional outlier among RNase 1 homologs, with the true physiological role of RNase 1 in other vertebrates still to be unveiled.…”

Adaptive evolutionary expansion of the ribonuclease 6 in Rodentia

“…Unlike RNase1, which has been extensively studied with gene duplication events observed in many mammals (Zhang et al 2002;Liu et al 2014;Wang et al 2016;Lang et al 2017), RNase6 has been examined in only a few species (Rosenberg & Dyer 1996;Deming et al 1998;Dyer et al 2004;Goo & Cho 2013). We studied 27 species representing the 3 main lineages of rodents and 10 families to investigate the evolutionary mechanism of RNase6.…”

“…Novel physiological functions may have evolved in group B and group C, which is reflected by selection pressures, key sites, isoelectric points and positive net charge. Positive selection has been used as one of the key evolutionary forces for the functional divergence of the duplicate genes and the association between positive selection and function divergence has been reported in some members of the RNase A superfamily (Zhang et al 2002;Liu et al 2014;Wang et al 2016;Lang et al 2017). One of the classical examples is the eosinophil-derived neurotoxin (EDN) and eosinophil cationic protein (ECP) of humans (Zhang et al 2000).…”

“…Using Mus musculus RNase6 sequences, TBLASTN and BLATN searches were carried out on Rodentia genomes to identify variation in this enzyme family. We used 10 −10 as the E-value cutoff for our searches (Cho et al 2005;Cho & Zhang 2006;Goo & Cho 2013;Wang et al 2016). In total, 27 species representing 10 families of Rodentia were examined in this study.…”

Genes lost during the transition from land to water in cetaceans highlight genomic changes involved in aquatic adaptations

“…Comparative analysis of cetacean genomes has provided important insights into the genomic determinants of cetacean traits and aquatic specializations (8). Several studies revealed patterns of positive selection in genes with roles in the nervous system, osmoregulation, oxygen transport, blood circulation, protein and lipid digestion, or bone microstructure (9)(10)(11)(12)(13)(14)(15)). An adaptive increase in myoglobin surface charge likely permitted a high concentration of this oxygen transport and storage protein in cetacean muscles (16).…”