Function and evolution of specialized endogenous lipids in toothed whales

Abstract

The Odontocetes (toothed whales) possess two types of specialized fat and, therefore, represent an interesting group when considering the evolution and function of adipose tissue. All whales have a layer of superficial blubber, which insulates and streamlines, provides buoyancy and acts as an energy reserve. Some toothed whales deposit large amounts of wax esters, rather than triacylglycerols, in blubber, which is unusual. Waxes have very different physical and physiological properties, which may impact blubber function. The cranial acoustic fat depots serve to focus sound during echolocation and hearing. The acoustic fats have unique morphologies; however, they are even more specialized biochemically because they are composed of a mix of endogenous waxes and triacylglycerols with unusual branched elements (derived from amino acids) that are not present in other mammals. Both waxes and branched elements alter how sound travels through a fat body; they are arranged in a 3D topographical pattern to focus sound. Furthermore, the specific branched-chain acid/alcohol synthesis mechanisms and products vary phylogenetically (e.g. dolphins synthesize lipids from leucine whereas beaked whales use valine). I propose that these specialized lipids evolved first in the head: wax synthesis first emerged to serve an acoustic function in toothed whales, with branched-chain synthesis adding additional acoustic focusing power, and some species secondarily retained wax synthesis pathways for blubber. Further research is necessary to elucidate specific molecular mechanisms controlling the synthesis and deposition of wax esters and branched-chain fatty acids, as well as their spatial deposition within tissues and within adipocytes.

Lipids of lung and lung fat emboli of the toothed whales (Odontoceti)

“…Considering all that was mentioned previously, fatty acids present in the lungs seem to be phylogenetically conserved across toothed whale species, with only small differences in the presence (i-C12:0) and proportion of specific fatty acids (C16:0 and C18:1ω9). This fact differs from other toothed whale tissues, like acoustic fats, where a robust phylogenetic diversity in the fatty acids present has been described 4 .…”

“…In ziphiids, i-C12:0 constitutes a major fatty acid in melon and mandibular fat tissues 3,4,7,13 , and it was also present, although in much lower quantities, in their lung tissue. In those species in which i-C12:0 was not detected in acoustic tissues, such as P. macrocephalus and delphinid species 4 , i-C12:0 was present in negligible quantities (close to 0) or not present at all in the lung.…”

“…Since wax esters consist of a fatty alcohol esterified to a fatty acid, the presence of fatty alcohols indicates that component was sourced exclusively from a wax ester. Wax esters are the major components in both acoustic fats and the blubber of species from the family Ziphiidae 3,4 , and nitrogen has proven to be highly soluble in them 33,34 . Thus, the presence and identification of fatty alcohols exclusively in the lungs positive to fat embolism would provide invaluable knowledge to the etiopathogenesis of fat embolism in these animals.…”

Fatty Acid Composition in Blubber, Liver, and Muscle of Marine Mammals in the Southern Baltic Sea

“…The pattern of stratification in the marine mammals is prevalent, with increasing proportions of monounsaturated fatty acids (MUFAs) to the outer layer and increasing proportions of saturated and polyunsaturated fatty acids (SFAs, PUFAs) to the inner layer [26,27]. This variation in the fatty acid composition between the inner and outer blubber layer seems to be an indicator of different metabolic pathways, as recently shown in grey seals [28]. Due to the difficult sampling, much less is known about the lipid composition in the liver and skeletal muscles of whales and seals.…”

“…Due to the difficult sampling, much less is known about the lipid composition in the liver and skeletal muscles of whales and seals. Koopman described that most marine species synthesize and deposit large quantities of wax esters as storage lipids in muscle, liver, and adipose tissues [28].…”