Primate Research Supplement

Gibbons, lesser apes, are characterized by their evolutionary plasticity of the chromosomal organization (karyotype). It is not well understood if and how this instability affects evolution of multigene families such as bitter taste receptor genes (TAS2Rs). TAS2Rs are spread into multiple chromosomes and are clustered in these chromosomes. The aim of this study is to elucidate the composition of TAS2R gene family across different gibbon species and compare them with other hominoid species to shed light on the influence of chromosomal instability to the gene composition. We examined fourteen individuals from nine gibbon species representing all four genera: Hylobates, Hoolock, Nomascus and Symphalangus. High-throughput targeted capture technology was employed to selectively enrich TAS2Rs, followed by short-read high-depth massive parallel sequencing. We showed that gibbons have 19 to 21 intact TAS2Rs, considerably fewer than 32 intact TAS2Rs estimated to have existed in the common ancestor of hominoids. Expectedly from the chromosomal instability, a gene cluster spanning approximately 125 kb-170kb including five TAS2Rs found in other hominoid species was lost in all gibbon species. This suggests that the region was lost at the common ancestor of all gibbon genera. Gibbons’ unique ecological niche as a swift brachiator may provide gibbons with an ecological superiority even with the reduction of large number of TAS2Rs which are usually required to select non-toxic foods in competition with other animals.

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Hair color variation in primates, including humans, has evolved through complex genetic mechanisms influenced by thermoregulation, immune function, and social communication. Melanism, characterized by increased dark pigmentation, has independently arisen multiple times across primate lineages. However, the genetic underpinnings of melanism remain incompletely understood. In this study, we investigated the molecular basis of melanism by analyzing hair root transcriptomes from Macaca nigra, which exhibits uniform dark pigmentation, and Macaca ochreata, which displays a dark-light hair pattern. Principal Component Analysis of RNA-seq sequence revealed a strong correlation between PC1 and hair lightness (L), suggesting that genes contributing to PC1 were associated with darker pigmentation. Differential gene expression analysis identified key regulators of melanin synthesis and intracellular transport, including TYRP1, RAB27B, and DYNLT3. DYNLT3, a dynein-associated motor protein facilitating melanosome maturation and transfer to keratinocytes, was significantly upregulated in dark hairs of M. nigra. Additionally, RAB27B, a GTPase involved in endosomal trafficking, exhibited high expression, suggesting a potential role in intracellular vesicle transport contributing to pigmentation regulation in primates.These findings highlight the critical role of intracellular transport in primate melanism and provide a transcriptomic framework for understanding the genetic basis of pigmentation.

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Recent research has revealed considerable evolutionary diversity in umami-taste (amino acids and nucleotides) and sweet-taste receptor TAS1R genes across vertebrate species. To contribute to a growing understand of how diet shapes taste evolution, we studied TAS1R genes in non-anthropoid primates with highly diverse diets, including members of the Strepsirrhini, comprised of Lorisiformes (lorises) and Lemuriformes (lemurs and aye-aye), as well as members of the Tarsiiformes (tarsiers). We employed a targeted capture (TC) approach specifically probing all the three mammalian TAS1R genes, i.e., TAS1R1 (for sensing umami), TAS1R2 (sweet) and TAS1R3 (required for forming a heterodimer), followed by short-read massive-parallel sequencing for three lorisiform, four lemuriform, and one tarsiiform species. Analyzing together with publicly available whole-genome assemblies (WGAs) of non-anthropoids, we found that TAS1R1 and TAS1R2 of some lorisiform species were disrupted. The relative evolutionary rates in introns and synonymous sites of all the three TAS1R genes, as well as non-genic genome regions, of lorisiforms were higher than those of lemuriforms, a finding consistent with the higher genome-wide mutation rate of the lorisiforms. We found the same pattern in the amino acid sequences and nonsynonymous sites of the sweet receptor TAS1R2 in lorisiforms. Evolutionary rates of amino acid sequences and nonsynonymous sites in TAS1R1 and TAS1R3 of lorisiforms were as slow as those of lemuriforms. This suggests that functional constraint on sweet sensing has been relaxed in lorisiform primates since their common ancestor. These results shed a new light on understanding evolutionary diversification of umami and sweet sensing in a diverse group of mammals.

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Sensing taste helps animals make decisions about ingesting beneficial foods. The umami and sweet tastes are sensed by TAS1R1-TAS1R3 and TAS1R2- TAS1R3 heterodimers, respectively. Recent researches have revealed evolutionary diversity of genes encoding these receptors, TAS1R1, TAS1R2 and TAS1R3. However, much information has largely relied on whole-genome assembly data which are often incomplete. Platyrrhine primates are suitable for understanding the evolutionary diversity of umami-sweet taste receptor gene family because of their remarkable diversity in diets as well as in color vision which has often been discussed in relation to ecological diversification. In this study, we applied targeted capture followed by short-read high-depth massive parallel sequencing for the three genes from 18 species of platyrrhines from all three platyrrhine Families. While the three genes were overall conservative, we noted that TAS1R1 was disrupted in three genera of Subfamily Callitrichinae, tamarins (Saguinus), Saddle-back tamarins (Leontocebus) and lion tamarins (Leontopithecus), implying three independent disruption events in the three genera or at least two independent disruptions in Leontopithecus and the common ancestor of Saguinus and Leontocebus. This implies less importance of sensing umami in these genera. Their variation pattern of color vision and dietary dependence on tree-sap are also observed in other callitrichine species of which TAS1R1 was intact. Thus, it is currently not certain why TAS1R1 was disrupted in the three tamarin genera. Further studies on other taste and chemical sensor genes should complement this study and facilitate our understanding on the sensory diversity of platyrrhines and primates in general.

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