Luca Pozzi

Primate phylogenetic relationships and divergence dates inferred from complete mitochondrial genomes.

The origins and the divergence times of the most basal lineages within primates have been difficult to resolve mainly due to the incomplete sampling of early fossil taxa. The main source of contention is related to the discordance between molecular and fossil estimates: while there are no crown primate fossils older than 56Ma, most molecule-based estimates extend the origins of crown primates into the Cretaceous. Here we present a comprehensive mitogenomic study of primates. We assembled 87 mammalian mitochondrial genomes, including 62 primate species representing all the families of the order. We newly sequenced eleven mitochondrial genomes, including eight Old World monkeys and three strepsirrhines. Phylogenetic analyses support a strong topology, confirming the monophyly for all the major primate clades. In contrast to previous mitogenomic studies, the positions of tarsiers and colugos relative to strepsirrhines and anthropoids are well resolved. In order to improve our understanding of how fossil calibrations affect age estimates within primates, we explore the effect of seventeen fossil calibrations across primates and other mammalian groups and we select a subset of calibrations to date our mitogenomic tree. The divergence date estimates of the Strepsirrhine/Haplorhine split support an origin of crown primates in the Late Cretaceous, at around 74Ma. This result supports a short-fuse model of primate origins, whereby relatively little time passed between the origin of the order and the diversification of its major clades. It also suggests that the early primate fossil record is likely poorly sampled.

Pleistocene diversification of living squirrel monkeys (Saimiri spp.) inferred from complete mitochondrial genome sequences

In order to enhance our understanding of the evolutionary history of squirrel monkeys (Saimiri spp.), we newly sequenced and analyzed data from seven complete mitochondrial genomes representing six squirrel monkey taxa. While previous studies have lent insights into the taxonomy and phylogeny of the genus, phylogenetic relationships and divergence date estimates among major squirrel monkey clades remain unclear. Using maximum likelihood and Bayesian procedures, we inferred a highly resolved phylogenetic tree with strong support for a sister relationship between Saimiri boliviensis and all other Saimiri, for monophyly of Saimiri oerstedii and Saimiri sciureus sciureus, and for Saimiri sciureus macrodon as the sister lineage to the S. oerstedii/S. s. sciureus clade. We inferred that crown lineages for extant squirrel monkeys diverged around 1.5 million years ago (MYA) in the Pleistocene Epoch, with other major clades diverging between 0.9 and 1.1 MYA. Our results suggest a relatively recent timeline of squirrel monkey evolution and challenge previous conceptions about the diversification of the genus and its expansion into Central America.

Use of different approaches to model presence/absence of Salmo marmoratus in Piedmont (Northwestern Italy)

Abstract In Piedmont (Italy) the environmental changes due to human impact have had profound effects on rivers and their inhabitants. Thus, it is necessary to develop practical tools providing accurate ecological assessments of river and species conditions. We focus our attention on Salmo marmoratus , an endangered salmonid which is characteristic of the Po river system in Italy. In order to contribute to the management of the species, four different approaches were used to assess its presence: discriminant function analysis, logistic regression, decision tree models and artificial neural networks. Either all the 20 environmental variables measured in the field or the 7 coming from feature selection were used to classify sites as positive or negative for S. marmoratus . The performances of the different models were compared. Discriminant function analysis, logistic regression, and decision tree models (unpruned and pruned) had relatively high percentages of correctly classified instances. Although neither tree-pruning technique improved the reliability of the models significantly, they did reduce the tree complexity and hence increased the clarity of the models. The artificial neural network (ANN) approach, especially the model built with the 7 inputs coming from feature selection, showed better performance than all the others. The relative contribution of each independent variable to this model was determined by using the sensitivity analysis technique. Our findings proved that the ANNs were more effective than the other classification techniques. Moreover, ANNs achieved their high potentials when they were applied in models used to make decisions regarding river and conservation management.

A multilocus phylogeny reveals deep lineages within African galagids (Primates: Galagidae)

BackgroundBushbabies (Galagidae) are among the most morphologically cryptic of all primates and their diversity and relationships are some of the most longstanding problems in primatology. Our knowledge of galagid evolutionary history has been limited by a lack of appropriate molecular data and a paucity of fossils. Most phylogenetic studies have produced conflicting results for many clades, and even the relationships among genera remain uncertain. To clarify galagid evolutionary history, we assembled the largest molecular dataset for galagos to date by sequencing 27 independent loci. We inferred phylogenetic relationships using concatenated maximum-likelihood and Bayesian analyses, and also coalescent-based species tree methods to account for gene tree heterogeneity due to incomplete lineage sorting.ResultsThe genus Euoticus was identified as sister taxon to the rest of the galagids and the genus Galagoides was not recovered as monophyletic, suggesting that a new generic name for the Zanzibar complex is required. Despite the amount of genetic data collected in this study, the monophyly of the family Lorisidae remained poorly supported, probably due to the short internode between the Lorisidae/Galagidae split and the origin of the African and Asian lorisid clades. One major result was the relatively old origin for the most recent common ancestor of all living galagids soon after the Eocene-Oligocene boundary.ConclusionsUsing a multilocus approach, our results suggest an early origin for the crown Galagidae, soon after the Eocene-Oligocene boundary, making Euoticus one of the oldest lineages within extant Primates. This result also implies that one – or possibly more – stem radiations diverged in the Late Eocene and persisted for several million years alongside members of the crown group.

The use of Artificial Neural Networks to classify primate vocalizations: a pilot study on black lemurs

The identification of the vocal repertoire of a species represents a crucial prerequisite for a correct interpretation of animal behavior. Artificial Neural Networks (ANNs) have been widely used in behavioral sciences, and today are considered a valuable classification tool for reducing the level of subjectivity and allowing replicable results across different studies. However, to date, no studies have applied this tool to nonhuman primate vocalizations. Here, we apply for the first time ANNs, to discriminate the vocal repertoire in a primate species, Eulemur macaco macaco. We designed an automatic procedure to extract both spectral and temporal features from signals, and performed a comparative analysis between a supervised Multilayer Perceptron and two statistical approaches commonly used in primatology (Discriminant Function Analysis and Cluster Analysis), in order to explore pros and cons of these methods in bioacoustic classification. Our results show that ANNs were able to recognize all seven vocal categories previously described (92.5–95.6%) and perform better than either statistical analysis (76.1–88.4%). The results show that ANNs can provide an effective and robust method for automatic classification also in primates, suggesting that neural models can represent a valuable tool to contribute to a better understanding of primate vocal communication. The use of neural networks to identify primate vocalizations and the further development of this approach in studying primate communication are discussed. Am. J. Primatol. 72:337–348, 2010.

Remarkable ancient divergences amongst neglected lorisiform primates.

Lorisiform primates (Primates: Strepsirrhini: Lorisiformes) represent almost 10% of the living primate species and are widely distributed in sub‐Saharan Africa and South/South‐East Asia; however, their taxonomy, evolutionary history, and biogeography are still poorly understood. In this study we report the largest molecular phylogeny in terms of the number of represented taxa. We sequenced the complete mitochondrial cytochrome b gene for 86 lorisiform specimens, including ∼80% of all the species currently recognized. Our results support the monophyly of the Galagidae, but a common ancestry of the Lorisinae and Perodicticinae (family Lorisidae) was not recovered. These three lineages have early origins, with the Galagidae and the Lorisinae diverging in the Oligocene at about 30 Mya and the Perodicticinae emerging in the early Miocene. Our mitochondrial phylogeny agrees with recent studies based on nuclear data, and supports Euoticus as the oldest galagid lineage and the polyphyletic status of Galagoides. Moreover, we have elucidated phylogenetic relationships for several species never included before in a molecular phylogeny. The results obtained in this study suggest that lorisiform diversity remains substantially underestimated and that previously unnoticed cryptic diversity might be present within many lineages, thus urgently requiring a comprehensive taxonomic revision of this primate group. © 2015 The Linnean Society of London

The stem catarrhine Saadanius does not inform the timing of the origin of crown catarrhines

A precise knowledge of the divergence time between Hominoidea (apes and humans) and Cercopithecoidea (Old World monkeys) has been hampered by the paucity of fossils between the early Miocene (23Ma) and the early Oligocene (30Ma). The earliest known Old World monkey is represented by Victoriapithecus macinnesi from Kenya, dated to 19 Ma (Benefit and McCrossin, 2002; Pilbeam and Walker, 1968), while several potential early hominoid fossils are dated to around 20 Ma, including Proconsul at 20e22.5 Ma (Harrison, 2010; Harrison and Andrews, 2009), Morotopithecus at 20 Ma (Gebo et al., 1997), and Ugandapithecus at 19e20 Ma (Senut et al., 2000). Kamoyapithecus, only known from some isolated dentition, dates back to the late Oligocene (23.9e27.8 Ma); however, its phylogenetic position remains controversial and not all authors classify it as a crown catarrhine (Harrison, 2002; Leakey et al., 1995). Based on this evidence in the fossil record, the divergence between hominoids and cercopithecoids is understood to be older than 20 Mya and most molecular estimates of primate divergences have used this as a calibration point (Chatterjee et al., 2009; Fabre et al., 2009; Hodgson et al., 2009; Raaum et al., 2005; Steiper and Young, 2008) In a recent study, Zalmout et al. (2010) describe a new Oligocene primate from Saudi Arabia, which they claim provides new insights into the time of divergence between apes and Old World monkeys. The newly described fossil, named Saadanius hijazensis and dated to w29Ma, is inferred to be a stem catarrhine, closely related to living apes and Old World monkeys (crown Catarrhini). According to the authors, this finding indicates an origin for crown Catarrhini after

A New Method for Genome-wide Marker Development and Genotyping Holds Great Promise for Molecular Primatology

Over the last two decades primatologists have benefited from the use of numerous molecular markers to study various aspects of primate behavior and evolutionary history. However, most of the studies to date have been based on a single locus, usually mitochondrial DNA, or a few nuclear markers, e.g., microsatellites. Unfortunately, the use of such markers not only is unable to address successfully important questions in primate population genetics and phylogenetics (mainly because of the discordance between gene tree and species tree), but also their development is often a time-consuming and expensive task. The advent of next-generation sequencing allows researchers to generate large amounts of genomic data for nonmodel organisms. However, whole genome sequencing is still cost prohibitive for most primate species. We here introduce a second-generation sequencing technique for genotyping thousands of genome-wide markers for nonmodel organisms. Restriction site–associated DNA sequencing (RAD-seq) reduces the complexity of the genome and allows inexpensive and fast discovery of thousands of markers in many individuals. Here, we describe the principles of this technique and we demonstrate its application in five primates, Microcebus sp., Cebus sp., Theropithecus gelada, Pan troglodytes, and Homo sapiens, representing some of the major lineages within the order. Despite technical and bioinformatic challenges, RAD-seq is a promising method for multilocus phylogenetic and population genetic studies in primates, particularly in young clades in which a high number of orthologous regions are likely to be found across populations or species.

Distribution of mitochondrial clades and morphotypes of baboons Papio spp. (Primates: Cercopithecidae) in eastern Africa

ABSTRACT Recent genetic studies, using maternally inherited mitochondrial DNA, indicate a complex evolutionary history for baboons Papio spp. in general, and for eastern African baboons in particular. To further address this topic and to improve our understanding of phylogeographic patterns of baboons in eastern Africa, mitochondrial cytochrome b sequence data were analysed from 148 baboon samples from 103 locations in eastern Africa. The resultant phylogenetic reconstructions suggest an initial split of baboons into four main clades: southern chacma baboons, baboons from Mahale Mountains in Tanzania, main southern, and main northern. We confirm that the boundary between southern and northern clades lies along the Ugalla-Malagarasi River and Ruaha-Rufiji River of central Tanzania. We detected new mitochondrial haplogroups, most notably the Mahale Mountains clade, and refined haplogroup distributions. The evolutionary divergence of baboons in eastern Africa was most likely triggered and maintained by numerous episodes of population division and reconnection, probably related mainly to climate change. To better understand these processes, nuclear DNA information is required, especially to assess gene flow among populations.

Genetic population structure and relatedness in the narrow-striped mongoose (Mungotictis decemlineata), a social Malagasy carnivore with sexual segregation.

Abstract Information on the genetic structure of animal populations can allow inferences about mechanisms shaping their social organization, dispersal, and mating system. The mongooses (Herpestidae) include some of the best‐studied mammalian systems in this respect, but much less is known about their closest relatives, the Malagasy carnivores (Eupleridae), even though some of them exhibit unusual association patterns. We investigated the genetic structure of the Malagasy narrow‐striped mongoose (Mungotictis decemlineata), a small forest‐dwelling gregarious carnivore exhibiting sexual segregation. Based on mtDNA and microsatellite analyses, we determined population‐wide haplotype structure and sex‐specific and within‐group relatedness. Furthermore, we analyzed parentage and sibship relationships and the level of reproductive skew. We found a matrilinear population structure, with several neighboring female units sharing identical haplotypes. Within‐group female relatedness was significantly higher than expected by chance in the majority of units. Haplotype diversity of males was significantly higher than in females, indicating male‐biased dispersal. Relatedness within the majority of male associations did not differ from random, not proving any kin‐directed benefits of male sociality in this case. We found indications for a mildly promiscuous mating system without monopolization of females by males, and low levels of reproductive skew in both sexes based on parentages of emergent young. Low relatedness within breeding pairs confirmed immigration by males and suggested similarities with patterns in social mongooses, providing a starting point for further investigations of mate choice and female control of reproduction and the connected behavioral mechanisms. Our study contributes to the understanding of the determinants of male sociality in carnivores as well as the mechanisms of female competition in species with small social units.