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theses

Primates have a particularly diverse array of dietary ecologies, from exclusively insectivorous species to grass-eating monkeys, the primate digestive system has evolved in response to a multitude of pressures. Endogenous digestive enzymes are an important part of the dietary adaptations found in primates, but comparatively little research has sought to understand how primate digestive enzymes have adapted to the variety of challenges posed by primate foods. This dissertation examines the genes coding for the digestive enzymes lysozyme C (LYZ), pancreatic ribonuclease (RNASE1), and acidic mammalian chitinase (CHIA) in a comparative non-human primate sample (n = 7, n = 25, n = 35, respectively). Specifically, I investigate evidence for inter-specific variation and adaptive evolution in these digestive enzyme genes related to folivorous and insectivorous diets. Datasets were assembled through gene sequencing and genome mining, and evaluated with phylogenetic analyses, including PAML and RELAX. My results show evidence for diet-related changes in pancreatic ribonuclease and acidic mammalian chitinase genes in primates. In the folivorous New World monkey Alouatta palliata, the RNASE1 gene was duplicated twice and the daughter genes exhibit changes that are indicative of a reduced efficiency against double-stranded RNA, suggesting a novel, and possibly digestive function. This had previously only been shown in colobine primates, but these findings suggest that in both foregut and caeco-colic fermenting primates pancreatic ribonuclease has convergently evolved a new role for digesting the products of microbial fermentation. For acidic mammalian chitinase, results are consistent with the hypothesis that the enzyme is used for the digestion of insect exoskeletons. Early primates likely had three CHIA genes, in congruence with the theory that insects were an important component of the ancestral primate diet. Most extant primate species retain only one functional CHIA paralog. Exceptions include two colobine species (non-insectivorous), in which all CHIA genes have premature stop codons, and several New World monkey species that retain two functional genes. The more insectivorous species in the sample also have the largest number of functional CHIA genes, retaining three functional CHIA paralogs. Tarsius syrichta, the most insectivorous primate, has a total of five CHIA genes, two of which may be duplications specific to the tarsier lineage. Selection analyses indicate that CHIA genes are under more intense selection in species with higher insect consumption, as well as in smaller-bodied species (<500 g), providing molecular support for Kay’s Threshold, a well-established component of primatological theory. CHIA genes are not subject to copy number variation in primates. Overall, these results provide evidence that pancreatic ribonuclease and acidic mammalian chitinase are important digestive enzyme adaptations for folivorous howler monkeys and insectivorous primates, respectively. These proteins may provide crucial adaptive benefits by improving the digestion of foliage and insects, and thus increasing energy and amino acid returns to the animal.

ETD_8543

Ph.D.

Includes bibliographical references

by Mareike Cora Janiak

doi:10.7282/T3M33070

ETD doctoral

The author owns the copyright to this work.