The Evolution Of Cetacean Fat Metabolism - Related Genes And Their Relationship With Aquatic Adaptation

Cetaceans (whales, dolphins and porpoises) are a group of secondarily adapted marine mammals with important and special significance during evolution. Approximately 56-53 million years ago, cetacean ancestors transformed from a fully terrestrial quadruped to an obligate aquatic habitat, and subsequently diverse extant cetaceans radiated around the world with a series of remarkable morphological change and fast adapatation. During this evolutionary transition, life medium has changed from air to water, and it has been known that water conducts heat away from a body 25 times faster than air at the same temperature. Therefore, energy reserves and the maintenance of body temperature were the most critical challenges that these species encountered. Strikingly, the thickness of blubber in whales is greater than that of other artiodactyls species. The blubber of cetaceans is dynamic and multifunctional, acting as a metabolic energy storage site, contributing to positive buoyancy, providing thermal insulation, supporting locomotion and increasing efficiency by streamlining the body surface. More importantly, blubber can also provide energy and fresh water through fat metabolism. Obviously, cetaceans have evolved the perfect physiological mechanism to maintenant the thickened blubber and fat metabolism. However, the genetic basis underlying this adaption in cetacean remains poorly explored. Here, the candidate genes related to fat digestion, blubber thickening and lipids metabolism were investigated and compared to orthologous sequences from terrestrial mammals using multiple approaches. The goal of the present study was to test whether evolutionary changes in these genes were associated with their transition from land to water, and to determine the molecular mechanism underlying the cetacean blubber thickening during this adaptive process.In the second chapter of dissertation, four lipases genes (PNLIP, LIPC, LIPF and CYP7A1) were investigated in representatives of major cetacean lineages and compared with orthologous sequences from the terrestrial relatives, with an aim to uncover the process and pattern of evolution during the transition from land to water. Strong signals of positive selection were detected in genes involved in lipase (i.e. CYP7A1, LIPF and PNLIP), suggesting that cetaceans have evolved enhanced ability of digesting lipids in response to their new feeding habit of preying mainly on animal food. In addition, three parallel/convergent nonsynonymous amino acid substitutions were identified in two positively selected lipases (CYP7A1 and PNLIP) along the cetacean and carnivore lineages, which suggested both lineages have evolved similar mechanism in the enhanced digestion of lipids, at least to some degree, in response to the pressure from similar carnivorous diet.In the third chapter of dissertation,88 candidate genes associated with triacylglycerol metabolism were firstly investigated in representative cetaceans and other mammals to test whether the thickened blubber matched adaptive evolution of triacylglycerol metabolism-related genes. Positive selection was detected in 41 of the 88 candidate genes, and functional characterization of these genes indicated that these are involved mainly in triacylglycerol synthesis and lipolysis processes. In addition, some essential regulatory genes underwent significant positive selection in cetacean-specific lineages, whereas no selection signal was detected in the counterpart terrestrial mammals. The extensive occurrence of positive selection in triacylglycerol metabolism-related genes is suggestive of their essential role in secondary adaptation to an aquatic life, and further implying that ’obesity’ might be an indicator of good health for cetaceans.In the fourth chapter of dissertation,327 genes of the whole KEGG lipid metabolism pathway were analysed to completely determine the role of the evolution of cetacean lipid metabolism genes in their adaptation to new ecological niches. Evolutionary analyses demonstrated that cetacean 149 genes were detected under positive selection and scattered in 15 point pathways of lipid metabolism, and positively selected genes were detected in the entire cetacean phylogeny, which indicates the ongoing adaptive evolution of cetacean lipid metabolism genes. Considering the function of the various point pathways, the present study suggested that cetaceans have possessed an effective ability to enhance their TAG synthesis, fatty acid degradation, biosynthesis of unsaturated fatty acids, and so on, since their origin and subsequent diversification in waters throughout the world.