Development and annotation of shotgun sequence libraries from New World monkeys.

The draft genome sequences of several primates are available, providing insights into evolutionary and anthropological research. However, genomic resources from New World monkeys are conspicuously lacking. To date, the genomes of only two platyrrhine species, the common marmoset and the Bolivian squirrel monkey, have been fully sequenced. This is especially limiting for comparative genomics research, considering that New World monkeys are the most speciose primate group, and platyrrhine genetic diversity is comparable to that of the catarrhines (i.e. apes and Old World monkeys). Here, we present the generation and annotation of numerous sequence reads from the genomes of Spider monkey (Ateles belzebuth), Owl monkey (Aotus lemurinus) and Uakari (Cacajao calvus), representing the three platyrrhine families, Atelidae, Cebidae and Pitheciidae, respectively. These sequencing reads were developed from gDNA shotgun libraries containing over 3000 individual sequences with an average length of 726 bps. Of these sequences, 1220 contain <20% repeats, and thus are potentially highly useful phylogenetic markers for other platyrrhine species. Among them, a large number of sequencing reads were found to match unique regions within the human (2462 sequences) and the marmoset (2829 sequences) genomes. In particular, the majority of these sequencing reads are from putatively neutrally evolving intergenic regions. Thus, they are likely to be highly informative for inferring neutral evolutionary patterns and genomic evolution for other New World monkeys.

Genomic data reject the hypothesis of a prosimian primate clade.

The phylogenetic position of tarsiers within the primates has been a controversial subject for over a century. Despite numerous morphological and molecular studies, there has been weak support for grouping tarsiers with either strepsirrhine primates in a prosimian clade or with anthropoids in a haplorrhine clade. Here, we take advantage of the recently released whole genome assembly of the Philippine tarsier, Tarsius syrichta, in order to infer the phylogenetic relationship of Tarsius within the order Primates. We also present estimates of divergence times within the primates. Using a 1.26 million base pair multiple sequence alignment derived from 1078 orthologous genes, we provide overwhelming statistical support for the presence of a haplorrhine clade. We also present divergence date estimates using local relaxed molecular clock methods. The estimated time of the most recent common ancestor of extant Primates ranged from 64.9 Ma to 72.6 Ma, and haplorrhines were estimated to have a most recent common ancestor between 58.9 Ma and 68.6 Ma. Examination of rates of nucleotide substitution in the three major extant primate clades show that anthropoids have a slower substitution rate than either strepsirrhines or tarsiers. Our results provide the framework on which primate morphological, reproductive, and genomic features can be reconstructed in the broader context of mammalian phylogeny.

Ancient origin of placental expression in the growth hormone genes of anthropoid primates.

In anthropoid primates, growth hormone (GH) genes have undergone at least 2 independent locus expansions, one in platyrrhines (New World monkeys) and another in catarrhines (Old World monkeys and apes). In catarrhines, the GH cluster has a pituitary-expressed gene called GH1; the remaining GH genes include placental GHs and placental lactogens. Here, we provide cDNA sequence evidence that the platyrrhine GH cluster also includes at least 3 placenta expressed genes and phylogenetic evidence that placenta expressed anthropoid GH genes have undergone strong adaptive evolution, whereas pituitary-expressed GH genes have faced strict functional constraint. Our phylogenetic evidence also points to lineage-specific gene gain and loss in early placental mammalian evolution, with at least three copies of the GH gene present at the time of the last common ancestor (LCA) of primates, rodents, and laurasiatherians. Anthropoid primates and laurasiatherians share gene descendants of one of these three copies, whereas rodents and strepsirrhine primates each maintain a separate copy. Eight of the amino-acid replacements that occurred on the lineage leading to the LCA of extant anthropoids have been implicated in GH signaling at the maternal-fetal interface. Thus, placental expression of GH may have preceded the separate series of GH gene duplications that occurred in catarrhines and platyrrhines (i.e., the roles played by placenta-expressed GHs in human pregnancy may have a longer evolutionary history than previously appreciated).

A fully resolved genus level phylogeny of neotropical primates (Platyrrhini).

There are more than 125 species of extant New World monkeys (Primates: Platyrrhini) found in approximately 15 genera. The phylogenetic relationships of these neotropical primates have been extensively studied from a molecular perspective. While these studies have been successful at inferring many of the relationships within the platyrrhines, key questions remain. The current study provides a framework for using non-genic, non-coding markers in comparative primate phylogenomic studies in species whose genomes are not yet scheduled for complete sequencing. A random genomic shotgun library was generated from the nocturnal Owl monkey Aotus lemurinus. Eleven unlinked, non-coding, non-genic, non-repetitive, nuclear DNA markers derived from this library were sequenced in at least one representative species of every platyrrhine genus. The combined sequence from these markers yielded a 7.7 kb multiple sequence alignment of 22 taxa. We analyzed these markers independently and combined with a 10 kb dataset consisting of "traditional," previously published markers located within or directly adjacent to genes. Parsimony, maximum likelihood, and Bayesian analysis converged on a single topology for the platyrrhine generic relationships. Notably, we confidently inferred that Pitheciidae is the sister taxon to the other two platyrrhine families (Cebidae, Atelidae). This relationship is supported by high values of branch support as well as topology tests. Additionally, Aotus formed a sister taxon to a clade comprising Cebus and Saimiri. With a fully resolved platyrrhine phylogeny in place it is now possible to design and test hypotheses regarding the evolution and diversification of platyrrhine phenotypes and life histories.