Evolutionary Anthropology 25:253–266 (2016) ARTICLE Digestive Enzymes of Human and Nonhuman Primates MAREIKE CORA JANIAK All living organisms need to consume nutrients to grow, survive, and that were previously difficult or reproduce, making the successful acquisition of food resources a powerful impossible to digest. These changes selective pressure. However, acquiring food is only part of the challenge. can occur quite rapidly12 and thus While all animals spend much of their daily activity budget hunting, search- could be an important adaptive ing for, or otherwise procuring food, a large part of what is involved in response that allows animals to overall nutrition occurs once the meal has been swallowed. Most nutrition- carve out separate dietary niches in al components are too complex for immediate use and must be broken environments where several species down into simpler compounds, which can then be absorbed by the body. are competing for food resources. This process, digestion, is catalyzed by enzymes that are either endoge- Both South America and Madagas- nous or produced by the host’s microbial population.1 Research shows car were populated by a small num- that the nutritional value of food is partially constrained by the digestive ber of primates rafting from the abilities of the microbial community present in the host’s gut and that African mainland.13 Upon arrival, these microbes rapidly adapt to changes in diet and other environmental these primates rapidly diversified 2 pressures. An accumulating body of evidence suggests that endogenously and filled the available dietary produced digestive enzymes also have been, and still are, common targets niches,14 evolving a suite of physio- of natural selection, further cementing their crucial role in an organism’s logical, morphological, and behavior- 3–5 digestive system. al characteristics to process a range of different diets.15–18 Since digestive enzyme adaptations are not just In this paper, I focus on the enzymes in it, has evolved in important for the ability to tolerate endogenous digestive enzymes that response to a multitude of pressures. new food resources, but also to max- are known to be important to pri- Recently, many research efforts have imize the energy obtained from mates. Primates exhibit a particular- focused on the gut microbiome, pro- them, changes in digestive enzymes ly diverse array of dietary ecologies. viding new insights into the interplay were likely part of this adaptive From exclusively insectivorous spe- between diet and gut adaptation for suite. Especially in human evolution, cies to grass-eating monkeys, the pri- a variety of animals, including maximizing the energy extracted mate digestive system, including the human and nonhuman primates.6–11 from foods may have been a crucial These are exciting new findings, but factor in fueling the growth of our to achieve a full picture of an ani- large brains.19 In nonhuman pri- mal’s digestive adaptations, the gut mates, many species depend on rela- Mareike Janiak is a doctoral candidate in microbiome and endogenously pro- tively low-quality foods, such as the Department of Anthropology at Rutgers University. She is interested in the diets and duced digestive enzymes should be leaves, which can only be digested dietary adaptations of primates. Her doc- viewed as complementary parts of efficiently with specific gut adapta- toral dissertation research seeks to identify the system. While the genes coding whether the digestive enzymes of New tions, such as foregut fermentation World monkeys exhibit adaptations for for digestive enzymes do not change and/or special digestive enzymes. insectivorous diets. as quickly as those of the micro- Recent work on primate nutrition- Email: [email protected] biome, the variety of endogenous al ecology has highlighted the many digestive enzymes within primates challenges primates face to meet not nevertheless constitutes a major just overall energy requirements, but Key words: dietary adaptations; amylase; lactase; adaptive strategy and warrants spe- also to balance micronutrients and chitinase; pepsin cial attention in this paper. protein intake,20–23 all while dealing Changes in the expression of diges- with fiber, tannins, and toxins con- 24,25 VC 2016 Wiley Periodicals, Inc. tive enzymes are important dietary tained in foods. The ability to DOI: 10.1002/evan.21498 adaptations that may allow an Published online in Wiley Online Library meet nutritional goals depends in (wileyonlinelibrary.com). organism to exploit food sources part on foraging decisions and the 254 Janiak ARTICLE TABLE 1. Endogenously Produced Digestive Enzymes of Primates Enzyme Gene symbol Substrate Alpha-Amylase AMY1 Starch Maltase MGAM Disaccharide maltose (product of starch digestion by a-amylase) Chitinase CHIA Chitin (present in cell walls of fungi and exoskeletons) Pepsin A PGA Protein Chymosin CYM Protein Ribonuclease RNASE1 In ruminants and colobines: foregut bacteria Lysozyme LYZ, LZM In ruminants and colobines: foregut bacteria Trypsin PRSS1 Protein Gastricsin PGC Protein Lipases PNLIP, CEL Lipids Lactase LCT Lactose (main carbohydrate in milk) Trehalase TREH Trehalose (disaccharide found in insects, fungi, and plants) Sucrase SI Sucrose, maltose nutritional composition of food disaccharide maltose, which can shows that the ability to express a- items.25–27 However, it is also con- then be hydrolyzed into glucose and amylase in saliva evolved after sever- strained by the gut’s capability to absorbed into the bloodstream.32 All al duplications of the pancreatic extract these nutrients, which is vertebrates express this digestive amylase gene AMY2 within the pri- where digestive enzymes and varia- enzyme in their pancreas, but only mate lineage.34 Two insertions occur tion in them undoubtedly play a key some mammals have evolved to addi- in the promoter region of AMY1, role.1,3,4,28 tionally express a-amylase in their resulting in the expression of a- The enzymes discussed here mouths, where it is secreted by amylase in saliva. Comparing the include amylase, lactase, pepsin A, parotid and/or submaxillary glands.33 gene structures between different chymosin, chitinase, ribonuclease, Species that express a-amylase in primates shows that the first inser- and lysozyme. While this is not an their saliva include some primates, tion, a g-actin pseudogene, arose exhaustive list of the enzymes at rodents, lagomorphs, and bats.34 after the divergence of the New work in primate digestive tracts, they Strikingly, the secretion of a-amylase World monkey lineage.34 The second are the more important ones because by the salivary glands has evolved insertion, an endogenous retrovirus, they usually represent the first step independently several times, sugges- occurred after the split from the Old in the digestion of their respective ting that this phenotype provides a World monkeys and is found only in 1 substrates, and research in primates selective advantage for certain spe- hominoids (Fig. 1).34 Studies with has largely been limited to them. cies.32 Furthermore, there is consid- transgenic mice indicate the retrovi- Table 1 details both the enzymes dis- erable variation, both between and ral insertion is required to change cussed here and ones that have not within species in which salivary amy- the expression site of amylase from been studied in depth in primates. I lase has evolved, in the amount of the pancreas to the parotid gland.36 describe the specific role of each enzyme that is expressed.3,31,35 Evi- This is consistent with the lack of digestive enzyme, summarize what is dence that this may also be the case salivary amylase activity in New known about its inter- and intra- for pancreatic amylase comes from a World monkeys. Old World monkeys, species variability, and discuss the study comparing copy number varia- however, express salivary amylase adaptive implications of such varia- tion of pancreatic amylase genes in despite lacking the retroviral inser- tion. I include information on diges- wolves and domestic dogs.4 tion. More work is needed to tease tive enzymes in nonprimate Within primates, only Old World apart whether the insertion of the g- mammals to build a comparative monkeys, apes, and humans express actin pseudogene plays a role in sali- evolutionary framework. a-amylase in their saliva; New World vary amylase expression or if anoth- monkeys do not (Fig. 1).3,34 No er mechanism is responsible for this AMYLASE investigation of salivary amylase phenotype in Old World monkeys. Starches are a staple in the diets activity in strepsirrhines has been The latter would suggest an addition- of many contemporary human popu- published, suggesting a potential al independent evolution event with- lations.29 They are also present in avenue for future research. However, in the primate order.34 the diets of some nonhuman pri- given current understanding of the Rodents also express salivary amy- mates and other mammals in the evolutionary pattern of this trait in lase, but must have evolved the abili- form of underground storage organs, primates, it is unlikely that strepsir- ty independently from primates.36 unripe fruits, and seeds.30,31 Alpha- rhines express a-amylase in their However, similarities between pan- amylase is the enzyme that catalyzes saliva. creatic and salivary amylase genes in the breakdown of starch into sugar A comparison of the amylase gene mice indicate that the latter resulted by cleaving the glycosidic bonds of structures in New World and Old from duplication