No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
Molecular phylogeny and systematics of bald uakaris, genus Cacajao Lesson, 1840 (Primates: Pitheciidae), with the description of a new species
Abstract
Bald uakaris, genus Cacajao, are Amazonian primates currently classified as one species and four subspecies based on the patterns of pelage coloration. In this study, we test if their current taxonomy is represented by the phylogenetic relationship of the main lineages retrieved from molecular data. We included, for the first time, all bald uakari taxa in a mitochondrial (cytochrome b) and genome-wide (ddRAD) phylogenetic analyses. We also examined the pattern of pelage colouration in specimens from zoological collections. Having determined the number of lineages using Maximum Likelihood and the species tree using coalescent analyses, we test their divergence time using a Bayesian approach. While the cytochrome b analysis only recovered two clades, the ddRAD analysis supported the reciprocal monophyly of five lineages of bald uakaris, with all clades including only individuals with distinct and exclusive diagnostic phenotypic characters. We found that species diversification in Cacajao occurred during the last 300 Kya and may have been influenced by the formation of rivers and flooded forests in western Amazonia. We propose that the four bald uakari subspecies currently recognised can be upgraded to species level and we describe the white uakaris from the basin of the Rio Tarauacá as a new species.
... e-mail: nuria.hermosilla@upf.edu distribution 21,24 ), and genomic traits 21,22 . The bald uakaris comprise five species (C. ...
... The bald uakaris comprise five species (C. calvus, C. amuna, C. novaesi, C. rubicundus, C. ucayalii) 24 and black uakaris, three (C. ayresi, C. hosomi, C. melanocephalus) 25 . ...
... They are mostly found in the forests of Solimões-Japurá and Negro-Branco river systems, and inhabit extensive areas of terra firme forest during some months, including high altitude areas 20 . On the other hand, bald uakaris are mainly flooded-forest specialists found around white water rivers (várzea) and present a red bald face with pelage that ranges from very light-greyish white (white bald uakaris) to red-chestnut (red bald uakaris) 23,24 . The populations of the five species of bald uakaris are found in the Ucayali, Solimões, and Juruá river systems, nearly overlapping but in general south of the black uakaris' distribution range 26 (Fig. 1A). ...
Despite showing the greatest primate diversity on the planet, genomic studies on Amazonian primates show very little representation in the literature. With 48 geolocalized high coverage whole genomes from wild uakari monkeys, we present the first population-level study on platyrrhines using whole genome data. In a very restricted range of the Amazon rainforest, eight uakari species (Cacajao genus) have been described and categorized into the bald and black uakari groups, based on phenotypic and ecological differences. Despite a slight habitat overlap, we show that posterior to their split 0.92 Mya, bald and black uakaris have remained independent, without gene flow. Nowadays, these two groups present distinct genetic diversity and group-specific variation linked to pathogens. We propose differing hydrology patterns and effectiveness of geographic barriers have modulated the intra-group connectivity and structure of bald and black uakari populations. With this work we have explored the effects of the Amazon rainforest’s dynamism on wild primates’ genetics and increased the representation of platyrrhine genomes, thus opening the door to future research on the complexity and diversity of primate genomics.
... The accessibility of cytochrome b sequences of different taxa makes it especially useful in phylogeographic studies, particularly in primates that occur in remote areas and, therefore, are relatively more difficult to get samples. In Cacajao, the sequences available in the GenBank, for example, are from individuals from Peruvian and Brazilian Amazonia, including sequences retrieved from Museum specimens stored in zoological collections in Brazil, the US and Europe Figueiredo-Ready et al., 2013;Silva et al., 2022). Here, we used 77 cytochrome b sequences available in GenBank (Table S1) to perform a time-scaled phylogenetic inference and a continuous phylogeographic analysis using the software package BEAST 1.10.4 ...
... However, when introgression occurs between P3 and either P1 or P2, the frequency of ABBA or BABA patterns will be different, leading to a D significantly different from zero (Malinsky et al., 2021). We used the ddRADseq tree topology presented in Silva et al. (2022) as input for the Dtrios package, defining Chiropotes as the outgroup; and used the Fbranch package to summarise and visualise the results from the ABBA-BABA tests. ...
... retractions of the flooded forests, competition and habitat requirements) were essential to maintain the separation of the recently diverged lineages and influenced their geographic distribution. The tree graph is based on the ddRAD time tree reconstructed by Silva et al. (2022). ...
Aim
The central and western Amazonia underwent several landscape changes during the Quaternary. Whereas the Riverine Barrier Hypothesis is traditionally used to explain the influence of rivers on speciation, processes such as river rearrangements have been overlooked to explain the geographic distribution and evolutionary history of Amazonia biota. Here, we tested how river rearrangements influenced the evolutionary history of uakari monkeys, genus Cacajao , a primate genus primarily associated with seasonally flooded forests in central and western Amazonia.
Location
Central and Western Amazonia.
Taxon
The genus Cacajao , including the black uakaris ( C. melanocephalus , C. ayresi , C. hosomi ); and the bald‐headed uakaris ( C. calvus , C. amuna , C. rubicundus , C. ucayalii , C. novaesi ).
Methods
We performed a continuous phylogeographic analysis using 77 cytochrome b sequences to identify the origin and dispersal of Cacajao lineages. We used genome‐wide SNP variation (ddRADseq) to investigate population structure, gene flow and demographic history in Cacajao populations and used digital elevation models to identify landscape and riverscape characteristics that may have influenced the geographic distribution of Cacajao .
Results
Our continuous phylogeographic reconstruction pointed out that the ancestral Cacajao lineage occupied the flooded forests of the Solimões River, in central Amazonia, at ~1.7 Mya and descendant lineages dispersed throughout central and western Amazonia more recently. We identified gene flow in both black and bald‐headed uakari populations, even across rivers considered barriers (e.g. the Negro River). Landscape analysis showed that river rearrangements influenced the geographic distribution and population structure in Cacajao . Historical demographic analyses suggest varied scenarios of population size changes among Cacajao monkeys consistent with periods of intense dynamism in flooded habitats and the formation of non‐flooded upland forests.
Main Conclusion
Our results support that the river rearrangements have shaped the geographic distribution and divergence of recently diverged Cacajao lineages. Landscape and riverscape changes, along with retractions of the flooded forests, isolated some Cacajao populations in floodplain areas. Our study also suggests that these events led to the recent changes in demographic histories in species with a restricted geographic distribution.
... Eight species have been described in the Cacajao genus, which in turn can be classified into two groups, the bald and the black uakaris 18 . They show contrasting phenotypic (pelage coloration 18 and skin pigmentation 20 ), ecological (habitat preference 21 , geographic distribution 21,22 ) and genomic traits 21,23 . The bald uakaris comprise five species (C. ...
... The bald uakaris comprise five species (C. calvus, C. amuna, C. novaesi, C. rubicundus, C. ucayalii) 22 and black uakaris, three (C. ayresi, C. hosomi, C. melanocephalus) 24 . ...
... They are mostly found in the seasonally flooded forests of Solimões-Japurá and Negro-Branco river systems, and inhabit extensive areas of terra firme forest during some months, including high altitude areas 19 . On the other hand, bald uakaris are mainly flooded-forest specialists found around white water rivers (várzea) and present a red bald face with pelage that ranges from very light-yellowish brown (white bald uakaris) to orange (red bald uakaris) 20,22 . The populations of the five species in bald uakaris are found in the Amazon basin, nearly overlapping at a given point but in general southern to black uakaris' distribution range 25 ( Figure 1A). ...
Uakari monkeys (genus Cacajao ) are endemic to the Amazon rainforest. These have been divided into two main groups: bald and black, mainly based on phenotypic and ecological differences, for which eight taxonomic species have been described. We present 48 geo-localized high coverage whole genomes from uakaris in wild populations across their habitat range. The resolution in terms of sequencing depth provided by this dataset has allowed us to closely explore the structure and evolutionary past of these populations inhabiting the highly dynamic and diverse Amazon rainforest, unavailable until now. Also, we have refined previous phylogenetic estimates by presenting the first whole genome phylogenies available for Cacajao , which were built based on 1Mb and 250kb windows respectively. In this context, bald and black uakaris showed differing genetic diversity ranges, group-specific non-synonymous variation enriched for pathogen-related pathways, and strong population structure, both among and within species. Despite the latter, connectivity was common inside each group whilst strongly shaped by allopatric barriers. Strikingly, even though their habitat ranges partially overlap, no migration was detected between these two groups. Lastly, demographic inference was performed employing a maximum likelihood approach, with which we i) obtained overall higher effective population size estimates for bald extant and ancestral populations than black in agreement with genetic diversity patterns, and ii) found the evolutionary divergence times in the genus were as old as one million years, depicting a quite recent evolutionary history. With this work we increased the representation of wild non-human primates in genomic studies, particularly that of platyrrhine lineages such as Cacajao .
... Cacajao is a genus with distribution limited to western Amazonia, while its sister group, the genus Chiropotes, occupy the upland forests of the Guiana and Brazilian shields in eastern Amazonia (Silva Jr et al., 2013). The two groups diverged by approximately 5.1 Mya (Silva et al., 2022). Specieslevel diversification in Cacajao has occurred since 0.5 Mya and may have been influenced by rivers and flooded forest rearrangements in western Amazonia (Silva et al., 2022). ...
... The two groups diverged by approximately 5.1 Mya (Silva et al., 2022). Specieslevel diversification in Cacajao has occurred since 0.5 Mya and may have been influenced by rivers and flooded forest rearrangements in western Amazonia (Silva et al., 2022). The genus comprises eight species currently recognised, including three species of black uakaris (C. ...
... ayresi, C. hosomi, and C. melanocephalus, and five species of bald-headed uakaris (C. amuna, C. calvus, C. rubicundus, C. ucayalii, and C. novaesi Silva et al., 2022). While the eight Cacajao species were well-delimited lineages in a genome-wide phylogeny, bald-headed uakaris are separated into only two main lineages if the mitochondrial cytochrome b gene is used for phylogenetic inference (Silva et al., 2022). ...
Aim
Western Amazonia is a region that underwent several landscape changes during the Quaternary. While Riverine Barrier Hypothesis is traditionally used to explain the influence of rivers on speciation, processes such as river rearrangements have been overlooked to explain the geographic distribution and evolutionary history of the Amazonia biota. Here we test how river rearrangements in western Amazonia influenced the evolutionary history of uakari monkeys, a primate group most associated with seasonally flooded forests in western Amazonia.
Location
Western Amazonia
Taxon
The uakari monkey (genus Cacajao )
Methods
We performed a continuous phylogeographic analysis using 77 cytochrome b sequences and used digital elevation models to identify the role of landscape and riverscape characteristics in the geographic distribution of Cacajao . Finally, we used genome-wide SNPs variation (ddRADseq) to investigate population structure, gene flow and demographic history in three Cacajao species that were impacted by river rearrangements.
Results
Our continuous phylogeographical reconstruction points that the ancestral Cacajao lineage occupied the flooded forests of the Solimões River at ∼1.7 Mya, and descendant lineages dispersed throughout western Amazonia more recently. We identified gene flow among both black and bald-headed uakari populations, even across rivers considered barriers (e.g., the Negro River). Landscape analysis showed that river rearrangements influenced the geographic distribution and population structure in Cacajao . The demographic analysis indicates that C. calvus, C. amuna , and C. rubicundus went through a population decline in the last 70 Kya and have a low effective population size.
Main conclusion
Our results support that the river rearrangements have shaped the geographic distribution and divergence of recently diverged Cacajao lineages. Landscape and riverscape changes, along with retractions of the flooded forests, isolated some Cacajao populations in floodplain areas. Our study also suggests that these events led to the recent population decline in species with a restricted geographic distribution.
... An integrative analysis using new morphological, phylogenomic, and geographic distribution data, uncovered a new pseudo-cryptic species of an Amazonian marmoset, named as Mico schneideri Costa-Araújo et al. (2021). Silva et al. (2022) provided the most the most complete analysis to date of the evidence for the ranges of the bald uakaris. They described a fifth bald uakari and placed them all as species rather than subspecies. ...
... Bald uacaris have also been subject to taxonomic revision based on genomic research. Silva et al. (2022) found five lineages of bald uacaris using ddRAD data, with species diversifying over the last 300,000 years; all five of these bald uakari species are found within the Brazilian Amazon (Cacajao calvus, C. rubicundus, C. ucayalii (with most of its distribution in Peru), C. novaesi, and the newly described species from the Silva et al. 2022 paper, C. amuna). ...
Our aim is to provide an update about what we know and do not know about primates in Brazilian Amazonia, as well as to highlight key threats and to identify research and conservation priorities. Here, we provide a history of primatology in the Brazilian Amazon and a literature review of primate research locations there between 1968 and 2018. Most of the 558 studies identified occurred along the larger navigable rivers, with interfluvial terra firma forests relatively neglected and insufficiently surveyed. Population surveys are needed in the interfluvia of the larger rivers, such as the Tapajós-Xingu interfluvium, and headwaters of the larger rivers and their tributaries near the borders of Colombia, Peru, and Bolivia, as well as in northern parts of Mato Grosso and Pará. Even noninterfluvial areas such as coastal eastern Amazonia are in urgent need of inventories. Despite much recent progress, we still need to invest in more genetic research along with traditional ecology. The high deforestation rate in the Brazilian Amazon warns that efficient measures to curb forest loss must be implemented in the short to medium term to avoid the extinction of primate populations and species, since 36 primates there are now ranked as threatened with extinction.
... DNA retrieved from museum specimens has supported studies of species identification and geographic distribution, complementing traditional approaches in taxonomy (Blair et al., 2023;Hawkins, Bailey et al., 2022a, Hawkins, Flores et al., 2022b. Researchers have used historical DNA data to infer the evolutionary relationships of broadly distributed, rare, or inaccessible species, clarifying the taxonomic status of these species and allowing for the resolution of taxonomic problems, taxa distribution range, description of new species, and the elucidation of evolutionary processes underlying speciation (Ennes Silva et al., 2022;Guschanski et al., 2013;Hawkins, Bailey et al., 2022a;Porter et al., 2021;Yao et al., 2020;Jensen et al., 2023). The combination of historical and contemporary samples also has allowed for the characterization of changes in the genetic composition of natural populations over time (Clark et al., 2023). ...
The availability of genetic data from wild populations limits our understanding of primate evolution and conservation, particularly for small nocturnal species such as lorisiforms (galagos, lorises, angwantibos, and pottos). Emerging methods for recovering genomic DNA from historical museum specimens have been rarely used in primate studies. We aimed to optimize extraction and bioinformatics protocols to maximize the recovery of historical DNA to fill important geographic and taxonomic gaps, improve phylogenetic resolution, and inform conservation of Lorisiform primates. First, we compared the performance of two DNA extraction methods by using 238 specimens up to a hundred years old. We then selected 96 samples with the highest DNA yields for shotgun sequencing. To evaluate the impact of phylogenetic divergence in bioinformatic read mapping, we compared coverage depths when using human and three lorisiform reference mitogenomes. Based on whole genomic data, we performed metagenomics and microbial diversity analyses to assess the composition of potentially exogenous content. Lastly, based on the most geographically and taxonomically comprehensive sampling for the West African lorisiforms to date (19/32 currently recognized species), we performed phylogenetic inference using Maximum Likelihood. The results showed that older samples yield lower DNA concentration, with an optimized phenol-chloroform protocol outperforming a commercial kit. However, both extraction methods generated DNA in sufficient amount and quality for phylogenetic inference. Our reference bias comparisons showed that higher phylogenetic proximity between focal species and reference mitogenome increases coverage depth. The metagenomic analysis found human contamination in only one of 96 samples (1%), whereas ten of 96 (11%) samples showed nonnegligible levels of other exogenous contents, among which are certain blood parasites. We inferred low support for the monophyly of Asian and African Lorisids but confirmed the monophyly and previously suggested relationships among Galagid genera. Lastly, we found evidence of cryptic species diversity within the western dwarf galagos (genus Galagoides). Taken together, these results attest to the enormous potential of museomics to advance our understanding of galago evolution, ecology, and conservation, an approach that can be extended to other primate clades.
... Recently, multiple studies have used museum specimens to generate genomiclevel data. For instance, reduced-representation genomic datasets have been generated from 40-year-old olive baboon skin (Papio anubis; Burrell et al., 2015) and bald uakaris (Cacajao spp.; Ennes Silva et al., 2022). van der Valk et al. ...
An accurate representation of species diversity is critical in primatology; most of the questions in evolutionary biology, ecology, and conservation hinge on species as a fundamental unit of analysis. Galagos are among the least-known primates. Because of their cryptic morphology, broad distribution, and sampling challenges arising from elusive habits and political instability, substantial knowledge gaps about their taxonomy, evolutionary history, and biogeography remain. Despite these limitations, recent research that integrated field surveys, acoustic, morphological, and genetic analyses helped us to better understand the taxonomic diversity of this primate group. In this paper, we (1) review the current status of galagid taxonomy; (2) synthesize our current understanding of their phylogenetics, origins, and biogeography; and (3) explore current and future approaches to elucidate galagid cryptic species diversity. The onset of galago systematics dates back to the early 19th century, with taxonomic descriptions following natural history expeditions and comparative anatomy studies. Although morphology has historically dominated systematic research on galagos, the coupling of acoustic analyses with genetic data has revolutionized the field. Taxonomic rearrangements include the discovery of new species in the wild (e.g., Galagoides kumbirensis) and the description of a new genus (Paragalago). Technological advances have allowed the collection of acoustic data in remote areas, and molecular techniques have the potential to help researchers fill important geographic gaps. Improving the resolution of galago species diversity also has implications for the conservation of wild populations, as a better understanding of species boundaries and ranges can aid in the implementation of conservation strategies.
... This number, however, has been increasing year to year, both as a result of refinements in taxonomy and the discovery in the wild of previously unknown forms (Feijó and Brandão 2022). These new species include primates Costa-Araújo et al. 2019Gusmão et al. 2019;Silva et al. 2022;Lopes et al. 2023), rodents (Semedo et al. 2020), opossums (Ferreira et al. 2020), armadillos (Feijó and Anacleto 2021), bats (Pavan et al. 2018), and dolphins (Hrbek et al. 2014). ...
Mammals are highly diverse in their lifestyles (including semi-and fully aquatic, aerial, terrestrial, fossorial, and arboreal forms). They play fundamental roles in the environments in which they live, acting as pollinators, seed dispersers, ecosystem engineers and top predators at the food chain; they are also involved in the transport of nutrients and in the conversion of biomass and carbon storage in the soil. One of the best-known and most studied groups of vertebrates, and also one of the most charismatic types of animals, mammals have a great capacity to raise awareness and motivate people interested in or engaged in conservation, acting as a flagship species for conservation. Despite their importance, we still lack basic information for the vast majority of Amazonian mammal species, even at a time when habitat loss and destruction there have reached unprecedented levels. The destruction of forests, coupled with human-induced climate change, is placing place increasing pressure on wildlife populations. Mammals are one of the most affected groups, especially the larger-bodied species (e.g., tapirs, deer, pigs, cats, and monkeys), which suffer from hunting pressure in addition to the fragmentation and loss of their habitats. Given this scenario, acknowledged experts in biology and ecology have written this book with the aim to identify our areas of lack of knowledge about mammals, and to propose research programs to
... The .xml file was built in BEAUTi using the following settings: unlinked substitution models (HKY+G+I), unlinked molecular clock model (uncorrelated relaxed lognormal; Drummond et al. 2006) and linked tree model. The coalescent Bayesian skyline (Gernhard et al. 2008) was used as the tree prior, because it was used successfully in simulation studies of divergence time estimation including a dataset with both intra-and interspecific samples (Ritchie et al. 2017, Mello et al. 2021, Silva et al. 2022. The monophyly of the family Oedemeridae and that of the subfamily Oedemerinae were constrained based on the wellsupported topology obtained for phylogenetic reconstruction to help run convergence. ...
The false blister beetle tribe Stenostomatini includes only the genus Stenostoma, with four species showing an intriguing distribution: Stenostoma lowei (Madeira), Stenostoma cossyrense (Pantelleria), Stenostoma melitense (Malta and southern Sicily) and Stenostoma rostratum, widely distributed along the Mediterranean and North Atlantic coasts. The evolutionary history leading to this distribution has not been investigated. Here, we explore the phylogeny and evolutionary history of the tribe, adopting an integrative approach that combines morphological and molecular data (mitochondrial COI and nuclear CAD and 28S). Moreover, we propose a new key for species identification and update the knowledge on adult and larval ecology. Finally, we propose the following explanation for the current distribution of the species. The genus originated in the Miocene, with S. lowei belonging to the oldest lineage. The remaining species share a common ancestor, dating to the Messinian Salinity Crisis. Stenostoma melitense and S. cossyrense are well differentiated according to morphology, but not according to molecular analysis. The wide distribution of S. rostratum might be related to its strategy of laying eggs within beached driftwood, where larvae develop, easily transported by the currents. Given that neither morphological nor molecular differentiation was detected between the two subspecies of S. rostratum, we propose the new synonymy Stenostoma rostratum septentrionale Švihla, 2005 = Stenostoma rostratum (Fabricius, 1787) syn. nov.
... This process allows for genome-wide marker discovery and typing at a high coverage and low cost, favoring markers to be genotyped accurately across individuals at different population or taxonomic levels [42][43][44]. RADseq-based methods have been successfully used to discover thousands of SNPs in phylogenetically diverse organisms including fish [45][46][47], insects [48,49], birds [50], and mammals [51,52], including primates [43,[53][54][55]. ...
Robust capuchin monkeys, Sapajus genus, are among the most phenotypically diverse and widespread groups of primates in South America, with one of the most confusing and often shifting taxonomies. We used a ddRADseq approach to generate genome-wide SNP markers for 171 individuals from all putative extant species of Sapajus to access their evolutionary history. Using maximum likelihood, multispecies coalescent phylogenetic inference, and a Bayes Factor method to test for alternative hypotheses of species delimitation, we inferred the phylogenetic history of the Sapajus radiation, evaluating the number of discrete species supported. Our results support the recognition of three species from the Atlantic Forest south of the São Francisco River, with these species being the first splits in the robust capuchin radiation. Our results were congruent in recovering the Pantanal and Amazonian Sapajus as structured into three monophyletic clades, though new morphological assessments are necessary, as the Amazonian clades do not agree with previous morphology-based taxonomic distributions. Phylogenetic reconstructions for Sapajus occurring in the Cerrado, Caatinga, and northeastern Atlantic Forest were less congruent with morphology-based phylogenetic reconstructions, as the bearded capuchin was recovered as a paraphyletic clade, with samples from the Caatinga biome being either a monophyletic clade or nested with the blond capuchin monkey.
Phylogenetic trees are analytic tools used in primate studies to elucidate evolutionary relationships. Because of its relative ease to sequence and rapid evolution compared to nuclear genomes, mitochondrial DNA is frequently used for phylogeny building. This project evaluated the effectiveness of using individual or grouped mitochondrial genes (mtGenes) as a proxy for the mitochondrial genome (mtGenome) in phylogeny building within two nested primate datasets, Cebidae and Platyrrhini, with differing divergence dates. mtGene utility rankings were determined based on congruence values to the mtGenome tree. mtGenes trees were also assessed on tree resolution and ability to sort nested clades. We found that most individual mtGenes, including ribosomal genes (12S and 16S), COX genes, most ND genes, and D-Loop are not appropriate for use as proxies for the mtGenome when tree building in either the Cebidae or Platyrrhini set. On average, grouped mtGenes outperformed individual mtGenes in both sets, and mtGene and grouped mtGene rankings varied between sets. Pairing CYB and COX3 together or pairing ND2 and CYB worked well in both the Cebidae set and the Platyrrhini set. We also found that nucleotide diversity is not a predictor of mtGene performance. Instead, it may be that unique mtGene or mtGene system evolutionary history impacts mtGene performance.
Peru holds a high mammalian diversity in its Amazonian region, with 326 species. However, our knowledge about the actual diversity is still considered incomplete, and the molecular information for those species in genetic databases is even less comprehensive. To assess the availability of genetic information for Peruvian Amazonian mammals relative to known diversity, we surveyed the Amazonian mammals with at least one molecular marker in the most widely used repositories for nucleotide sequences, GenBank and BOLD Systems. Our survey focused on widely used molecular markers in evolutionary biology-cytochrome b [cyt-b], cytochrome oxidase I [COI], 12S ribosomal RNA [12S], and the mitogenome [mit]-derived from Peruvian Amazon mammals. Additionally, to gain insights into the current mammalian sampling effort in Peruvian Amazonia, we generated a map of unique sampling localities and a heat map, utilizing 41951 records, which identified six major information gaps. This comprehensive analysis found 1597 genetic sequences corresponding to 180 mammalian species (55.2% of Peruvian Amazonian species): COI (38 species), cyt-b (167 species), 12S (56 species), and mitogenome (16 species). Taxonomically, Rodentia (53 species, four markers), Chiroptera (63 species, three markers), and Didelphimorphia (27 species, four markers) represented most molecular data, with a concentration of molecular markers in the orders Chiroptera (703) and Rodentia (499). Geographically, the Loreto department has the largest genetic information (530 records, 99 species). These results confirm a worrying underrepresentation of Peruvian Amazonian diversity in molecular databases. Consequently, we advocate for the use of scientific collections as an alternative source to systematically generate genetic information for the Amazonian mammal diversity in Peru to compensate for the current underrepresentation.
KEY WORDS:
Biodiversity; barcoding; bioinformatics; museomics; Neotropics
The database of the IUCN SSC Primate Specialist Group currently (December
2023) registers 218 species and subspecies of Neotropical primates in 24 genera
and five families. In the early 1960s, the diversity of Neotropical primates was
estimated to be around 200 species and subspecies. From then, through the
1970s to the mid-1990s, however, the perception of the region’s primate
diversity dropped, and reached an all-time low at 83 species and subspecies in
1980 (A World List of Mammalian Species, G. B. Corbet and J. E. Hill, British
Museum (Natural History), Comstock Publishing, Cornell University Press,
London and Ithaca). Interest in taxonomy and primate field research in the
Neotropics was subdued up to the late 1970s. Change was sparked by the
burgeoning capture of primates for biomedical research in the 1950s and 1960s,
and the increasing destruction of the Amazon rainforests from the late 1970s.
The numbers increased, at first slowly, but then, in 1995, they leapt back to the
200s in anticipation of a book by C. P. Groves (2001, Primate Taxonomy,
Smithsonian Institution Press, Washington, DC). The species’ counts (not
including subspecies) rose due to the adoption of the Phylogenetic Species
Concept over the Biological Species Concept, the former favoring the category
of species over subspecies. In this article, we discuss the changes in species and
subspecies numbers in the classification of the Neotropical primates, and report
on the taxonomic changes resulting from taxonomic research ongoing since
2012. We emphasize the importance of taxonomic research for an understanding
of the diversity of primates, and for conservation planning, not least in identifying
the populations that are threatened.
Aim
Mining is increasingly pressuring areas of critical importance for biodiversity conservation, such as the Brazilian Amazon. Biodiversity data are limited in the tropics, restricting the scope for risks to be appropriately estimated before mineral licensing decisions are made. As the distributions and range sizes of other taxa differ markedly from those of vertebrates—the common proxy for analysis of risk to biodiversity from mining—whether mining threatens lesser‐studied taxonomic groups differentially at a regional scale is unclear.
Location
Brazilian Amazon.
Methods
We assess risks to several facets of biodiversity from industrial mining by comparing mining areas (within 70 km of an active mining lease) and areas unaffected by mining, employing species richness, species endemism, phylogenetic diversity and phylogenetic endemism metrics calculated for angiosperms, arthropods and vertebrates.
Results
Mining areas contained higher densities of species occurrence records than the unaffected landscape, and we accounted for this sampling bias in our analyses. None of the four biodiversity metrics differed between mining and nonmining areas for vertebrates. For arthropods, species endemism was greater in mined areas. Mined areas also had greater angiosperm species richness, phylogenetic diversity and phylogenetic endemism, although less species endemism than unmined areas.
Main Conclusions
Unlike for vertebrates, facets of angiosperm and arthropod diversity are relatively higher in areas of mining activity, underscoring the need to consider multiple taxonomic groups and biodiversity facets when assessing risk and evaluating management options for mining threats. Particularly concerning is the proximity of mining to areas supporting deep evolutionary history, which may be impossible to recover or replace. As pressures to expand mining in the Amazon grow, impact assessments with broader taxonomic reach and metric focus will be vital to conserving biodiversity in mining regions.
An understanding of a species' geographic distribution is essential to assess, plan, and develop strategies for its conservation. The geographic distribution of the bald uakari, Cacajao calvus, and its component subspecies has been poorly investigated, with disjunct distributions being reported in Brazil and Peru. In this study, we reveal new records of bald uakari occurrence based on multi-year surveys, a literature review, and an examination of vouchers available in six zoological collections , clarifying the geographic distribution of all subspecies. We confirm that C. c. calvus has a disjunct distribution with populations along the rios Tarauacá and Pauini, 250 km away from those on the left bank of middle Rio Juruá and lower Rio Jutaí; and 650 km from the population of the Mamirauá Sustainable Development Reserve (Mamirauá SDR). Cacajao c. rubicundus has a disjunct distribution with three isolated populations 1) inhabiting the flooded forests of the Rio Solimões and the Paraná (channel) Jacurapá, 2) the left bank of the lower Rio Jutaí; and 3) in the Auati-Paraná. Cacajao c. novaesi has the smallest geographic distribution of the bald uakaris, occurring only in the Gregório-Tarauacá interfluvium. Cacajao c. novaesi and C. c. calvus are separated by the Rio Tarauacá, which is also a significant geographic barrier for other primates, including titi and saki monkeys. We also confirm the occurrence of Cacajao c. ucayalii in Brazil in the Serra do Divisor National Park. This Peruvian subspecies has the most extensive range, with isolated populations found in areas completely separated from the lowlands. The patchy distribution of Cacajao calvus provides a unique opportunity to understand how local environmental variation may have promoted ecological flexibility for the successful establishment of isolated populations.
Simultaneous molecular dating of population and species divergences is essential in many biological investigations, including phylogeography, phylodynamics, and species delimitation studies. In these investigations, multiple sequence alignments consist of both intra‐ and inter‐species samples (mixed samples). As a result, the phylogenetic trees contain inter‐species, inter‐population, and within‐population divergences. Bayesian relaxed clock methods are often employed in these analyses, but they assume the same tree prior for both inter‐ and intra‐species branching processes and require specification of a clock model for branch rates (independent vs. autocorrelated rates models). We evaluated the impact of a single tree prior on Bayesian divergence time estimates by analyzing computer‐simulated datasets. We also examined the effect of the assumption of independence of evolutionary rate variation among branches when the branch rates are autocorrelated. Bayesian approach with coalescent tree priors generally produced excellent molecular dates and highest posterior densities with high coverage probabilities. We also evaluated the performance of a non‐Bayesian method, RelTime, which does not require the specification of a tree prior or a clock model. RelTime's performance was similar to that of the Bayesian approach, suggesting that it is also suitable to analyze datasets containing both populations and species variation when its computational‐efficiency is needed.
An updated and annotated checklist of mammals occurring in Brazil is presented. A total of 751 native species, distributed in 249 genera, 51 families and 11 orders were recorded to the country. The Brazilian mammalian fauna shows an elevated rate of endemism (30%; 223 species). Among the species evaluated by IUCN (668 species; 90%), a total of 80 (10.6% of total mammalian fauna) are Threatened, 28 (3.9%) are considered as Near Threatened, two species (0.3%) are presumable Extinct, 96 (12.8%) are considered with Defi cient Data for conservation and 462 (61.6%) are considered as Least Concern. Fifteen new species were described since the last national compilation (published in 2017), which associated to new records to the country and synonimizations resulted in an increment of 30 species. Eight non-native species were introduced to the country, including the recently established Asiatic cervids Rusa unicolor (sambar) and Axis axis (chital). Seven native species (fi ve primates and two hystricomorph rodents) have been translocated from their areas of natural occurrence to other areas inside the country.
Mouse lemurs (Microcebus) are a radiation of morphologically cryptic primates distributed throughout Madagascar for which the number of recognized species has exploded in the past two decades. This taxonomic revision has prompted understandable concern that there has been substantial oversplitting in the mouse lemur clade. Here, we investigate mouse lemur diversity in a region in northeastern Madagascar with high levels of microendemism and predicted habitat loss. We analyzed RADseq data with multispecies coalescent (MSC) species delimitation methods for two pairs of sister lineages that include three named species and an undescribed lineage previously identified to have divergent mtDNA. Marked differences in effective population sizes, levels of gene flow, patterns of isolation-by-distance, and species delimitation results were found among the two pairs of lineages. Whereas all tests support the recognition of the presently undescribed lineage as a separate species, the species-level distinction of two previously described species, M. mittermeieri and M. lehilahytsara is not supported - a result that is particularly striking when using the genealogical discordance index (gdi). Non-sister lineages occur sympatrically in two of the localities sampled for this study, despite an estimated divergence time of less than 1 Ma. This suggests rapid evolution of reproductive isolation in the focal lineages, and in the mouse lemur clade generally. The divergence time estimates reported here are based on the MSC calibrated with pedigree-based mutation rates and are considerably more recent than previously published fossil-calibrated relaxed-clock estimates. We discuss the possible explanations for this discrepancy, noting that there are theoretical justifications for preferring the MSC estimates in this case.
The Critically Endangered Peruvian yellow-tailed woolly monkey Lagothrix flavicauda was presumed to only occur in the tropical montane cloud forests between the Marañón and Huallaga rivers in northern Peru. Here we report the discovery of a population to the south of its previously known range, in the Región Junín. During September–December 2018 we carried out transect surveys to record large mammals present near the village of San Antonio in the district of Pampa Hermosa, at 1,287–2,015 m altitude. We recorded five primate species during transect surveys. Lagothrix flavicauda was seen four times, and appeared phenotypically distinct from populations to the north, with notable white patches above each eye and a reduced yellow patch at the end of the tail. The presence of L. flavicauda in Junín extends its known geographical range over 200 km southwards from the closest previously known population in the Huánuco region, and presents a unique opportunity for the conservation of this Critically Endangered species.
The riverine barrier hypothesis is a central concept in Amazonian biogeography. It states that large rivers limit species distributions and trigger vicariant speciation. Although the hypothesis has explanatory power, many recent biogeographical observations addressing it have produced conflicting results. We propose that the controversies arise because tributary arrangements in the Amazon river system have changed in geologically recent times, such that large tracts of forest that were on the same side of a river at one time got separated to different sides at another. Based on topographical data and sediment dating, we map about 20 major avulsion and river capture events that have rearranged the river network in central Amazonia during the late Pleistocene and Holocene. We identify areas where past riverine barrier effects might still linger in the absence of a major river, as well as areas where such effects may not yet have accumulated across an existing river. These results call for a reinterpretation of previous biogeographical studies and a reorientation of future works to take into account the idiosyncratic histories of individual rivers.
Elaboration of Bayesian phylogenetic inference methods has continued at pace in recent years with major new advances in nearly all aspects of the joint modelling of evolutionary data. It is increasingly appreciated that some evolutionary questions can only be adequately answered by combining evidence from multiple independent sources of data, including genome sequences, sampling dates, phenotypic data, radiocarbon dates, fossil occurrences, and biogeographic range information among others. Including all relevant data into a single joint model is very challenging both conceptually and computationally. Advanced computational software packages that allow robust development of compatible (sub-)models which can be composed into a full model hierarchy have played a key role in these developments. Developing such software frameworks is increasingly a major scientific activity in its own right, and comes with specific challenges, from practical software design, development and engineering challenges to statistical and conceptual modelling challenges. BEAST 2 is one such computational software platform, and was first announced over 4 years ago. Here we describe a series of major new developments in the BEAST 2 core platform and model hierarchy that have occurred since the first release of the software, culminating in the recent 2.5 release.
The wisent or European bison is the largest European herbivore and is completely cross-fertile with its American relative. However, mtDNA genome of wisent is similar to that of cattle, which suggests that wisent emerged as a hybrid of bison and an extinct cattle-like species. Here, we analyzed nuclear whole-genome sequences of the bovine species, and found only a minor and recent gene flow between wisent and cattle. Furthermore, we identified an appreciable heterogeneity of the nuclear gene tree topologies of the bovine species. The relative frequencies of various topologies, including the mtDNA topology, were consistent with frequencies of incomplete lineage sorting (ILS) as estimated by tree coalescence analysis. This indicates that ILS has occurred and may well account for the anomalous wisent mtDNA phylogeny as the outcome of a rare event. We propose that ILS is a possible explanation of phylogenomic anomalies among closely related species.
Until recently, most phylogenetic and population genetics studies of nonhuman primates have relied on mitochondrial DNA and/or a small number of nuclear DNA markers, which can limit our understanding of primate evolutionary and population history. Here, we describe a cost-effective reduced representation method (ddRAD-seq) for identifying and genotyping large numbers of SNP loci for taxa from across the New World monkeys, a diverse radiation of primates that shared a common ancestor ~20–26 mya. We also estimate, for the first time, the phylogenetic relationships among 15 of the 22 currently-recognized genera of New World monkeys using ddRAD-seq SNP data using both maximum likelihood and quartet-based coalescent methods. Our phylogenetic analyses robustly reconstructed three monophyletic clades corresponding to the three families of extant platyrrhines (Atelidae, Pitheciidae and Cebidae), with Pitheciidae as basal within the radiation. At the genus level, our results conformed well with previous phylogenetic studies and provide additional information relevant to the problematic position of the owl monkey (Aotus) within the family Cebidae, suggesting a need for further exploration of incomplete lineage sorting and other explanations for phylogenetic discordance, including introgression. Our study additionally provides one of the first applications of next-generation sequencing methods to the inference of phylogenetic history across an old, diverse radiation of mammals and highlights the broad promise and utility of ddRAD-seq data for molecular primatology.
Information on the wildlife of the middle and upper reaches of the Purus in Brazil is scarce, and this region is one of the major remaining gaps in our understanding of the distributions and population status of mammals in the Brazilian Amazon. In this paper, we present information on the diversity of mammals of the middle Purus, in the south of Amazonas State, Brazil. Based on rapid inventories in four protected areas, and line-transect censuses in one of them, we provide locality records that indicate expansions of the known range of six primate species and a squirrel. Species more frequently seen during censuses were small and mid-sized primates and rodents, while records of larger mammals, which are more sensitive to subsistence hunting, were infrequent or lacking. Deforestation in the area is relatively low, but the area is close to the so-called “arc of deforestation” that is moving north and west from the north of the state of Mato Grosso into the states of Acre and Amazonas. The middle and upper Purus basin has been little explored, but is far from pristine, and populations of most of the species that are vulnerable to forest degradation and hunting are already reduced, especially close to the major rivers.
Bayesian inference of phylogeny using Markov chain Monte Carlo (MCMC) (Drummond et al., 2002; Mau et al., 1999; Rannala and Yang, 1996) flourishes as a popular approach to uncover the evolutionary relationships among taxa, such as genes, genomes, individuals or species. MCMC approaches generate samples of model parameter values - including the phylogenetic tree -drawn from their posterior distribution given molecular sequence data and a selection of evolutionary models. Visualising, tabulating and marginalising these samples is critical for approximating the posterior quantities of interest that one reports as the outcome of a Bayesian phylogenetic analysis. To facilitate this task, we have developed the Tracer (version 1.7) software package to process MCMC trace files containing parameter samples and to interactively explore the high-dimensional posterior distribution. Tracer works automatically with sample output from BEAST (Drummond et al., 2012), BEAST2 (Bouckaert et al., 2014), LAMARC (Kuhner, 2006), Migrate (Beerli, 2006), MrBayes (Ronquist et al., 2012), RevBayes (Höhna et al., 2016) and possibly other MCMC programs from other domains.
Lepidothrix is the most diverse genus of the family Pipridae, with eight recognized species. Although the genus' monophyly has been supported by both molecular and morphological characters, phylogenetic relationships and species limits within Lepidothrix remain uncertain. In the present study, we combined molecular sequences of mitochondrial (ND2 and COI) and nuclear (MYO, G3PDh and I5BF) markers in a multilocus analysis, to evaluate relationships and inter-specific limits among L. iris, L. nattereri, and L. vilasboasi, which are known to hybridize in eastern Amazonia. The results revealed a complex pattern, whereby events of secondary contact and gene flow after isolation and genetic and phenotypic differentiation prevented the recuperation of reciprocal monophyly among the studied taxa. The mitochondrial data indicate that L. nattereri is divided into two non-sister groups, one monophyletic, and the other, paraphyletic, with L. iris iris being more closely related to one of the two L. nattereri groups, while L. iris eucephala forms an undifferentiated clade with L. vilasboasi, probably resulting from an extensive process of mitochondrial introgression. In agreement with a previous study based on Single Nucleotide Polymorphism (SNP) data, mitochondrial haplotype networks also support that L. vilasboasi does not represent a recent "hybrid swarm" between L. iris and L. nattereri, but instead a genetically divergent lineage with a separate species status. Finally, the sister relationship recovered herein between L. iris iris and some western populations of L. nattereri currently in allopatry is also apparently explained by mitochondrial introgression, as also supported for nuclear genes by SNP data, indicating a complex scenario of past contact and gene flow between currently geographically distant Lepidothrix lineages.
Populations of two forms of uacaries, red and white, are found at the Mamirauá Sustainable Development Reserve (MSDR). Ayres (1986) notes that two skins of red uacaries were brought to Tefé (Amazonas state) from Auati-Paraná area, northern bank of Solimões river, inside the known geographical distribution of white uacaries, suggesting that a zone of contact between these two forms. The objective of this study was to gather information on the distribution of C. calvus at MSDR, both with interviews and direct observation. Parallel transects for active search were made at sites indicated by the inhabitants of the local communities. Nine communities confirmed the presence of white uacaries, while red uacaries were confirmed at seven communities. A small area of complete absence of the species was reported between Auati-paraná channel and Japurá river. A zone of contact between the two forms was indicated at Paraná do Aiupiá. For direct observation of the animals, 82.5 km were covered along Aiupiá channel, where white uacaries were observed in seven occasions, all at the right bank. Red uacaries were also spoted seven times, at the left bank. Further investigations at this area are being conducted in order to define the peripatry of both taxa, with big consequences to the conservation of the species.
The standard bootstrap (SBS), despite being computationally intensive, is widely used in maximum likelihood phylogenetic analyses. We recently proposed the ultrafast bootstrap approximation (UFBoot) to reduce computing time while achieving more unbiased branch supports than SBS under mild model violations. UFBoot has been steadily adopted as an efficient alternative to SBS and other bootstrap approaches.
Here, we present UFBoot2, which substantially accelerates UFBoot and reduces the risk of overestimating branch supports due to polytomies or severe model violations. Additionally, UFBoot2 provides suitable bootstrap resampling strategies for phylogenomic data. UFBoot2 is 778 times (median) faster than SBS and 8.4 times (median) faster than RAxML rapid bootstrap on tested datasets. UFBoot2 is implemented in the IQ-TREE software package version 1.6 and freely available at http://www.iqtree.org.
This article describes several features in the MAFFT online service for multiple sequence alignment (MSA). As a result of recent advances in sequencing technologies, huge numbers of biological sequences are available and the need for MSAs with large numbers of sequences is increasing. To extract biologically relevant information from such data, sophistication of algorithms is necessary but not sufficient. Intuitive and interactive tools for experimental biologists to semiautomatically handle large data are becoming important. We are working on development of MAFFT toward these two directions. Here, we explain (i) the Web interface for recently developed options for large data and (ii) interactive usage to refine sequence data sets and MSAs.
In many regions primates are an important dietary resource for isolated human populations, and they are among the most hunted species by traditional and indigenous communities in the Neotropics. Little is known about the characteristics or the spatial and temporal patterns of hunting, which limits a more detailed evaluation of its impact. We describe, quantify and analyse the spatial dynamics of primate hunting in the várzea (seasonally flooded forest) and paleovárzea (characterized by a series of low-lying ridges interspersed with flooded depressions, which result from cyclical depositional processes) environments of Central Amazonia, based on the monitoring of riverine communities at the Amanã and Mamirauá Sustainable Development Reserves over an 11-year period. During this time 402 primate hunting events were recorded, involving the harvesting of 541 individuals of nine species: Alouatta juara, Aotus cf. vociferans , Ateles chamek, Cacajao ouakary, Callicebus lucifer , Cebus albifrons, Saguinus inustus, Saimiri cassiquiarensis and Sapajus macrocephalus . Two hundred and forty of these hunts occurred in the paleovárzea and 162 in the várzea. The distances travelled by the hunters from their communities to the kill sites were significantly different between the environments, with longer distances being covered in the paleovárzea. Hunters in the paleovárzea also hunted across significantly larger areas than those in the várzea. The continuous monitoring of hunting areas and the gathering of data on the exploitation of species are necessary to understand the effects of hunting, as well as to support decision making in the management of the local fauna by traditional communities, and the development of effective conservation strategies for the local game species.
This article presents W-IQ-TREE, an intuitive and user-friendly web interface and server for IQ-TREE, an efficient phylogenetic
software for maximum likelihood analysis. W-IQ-TREE supports multiple sequence types (DNA, protein, codon, binary and morphology)
in common alignment formats and a wide range of evolutionary models including mixture and partition models. W-IQ-TREE performs
fast model selection, partition scheme finding, efficient tree reconstruction, ultrafast bootstrapping, branch tests, and
tree topology tests. All computations are conducted on a dedicated computer cluster and the users receive the results via
URL or email. W-IQ-TREE is available at http://iqtree.cibiv.univie.ac.at. It is free and open to all users and there is no login requirement.
The Loricariinae belong to the Neotropical mailed catfish family Loricariidae, the most species-rich catfish family. Among loricariids, members of the Loricariinae are united by a long and flattened caudal peduncle and the absence of an adipose fin. Despite numerous studies of the Loricariidae, there is no comprehensive phylogeny of this morphologically highly diversified subfamily. To fill this gap, we present a molecular phylogeny of this group, including 350 representatives, based on the analysis of mitochondrial and nuclear genes (8426 positions). The resulting phylogeny indicates that Loricariinae are distributed into two sister tribes: Harttiini and Loricariini. The Harttiini tribe, as classically defined, constitutes a paraphyletic assemblage and is here restricted to the three genera Harttia, Cteniloricaria, and Harttiella. Two subtribes are distinguished within Loricariini: Farlowellina and Loricariina. Within Farlowellina, the nominal genus formed a paraphyletic group, as did Sturisoma and Sturisomatichthys. Within Loricariina, Loricaria, Crossoloricaria, and Apistoloricaria are also paraphyletic. To solve these issues, and given the lack of clear morphological diagnostic features, we propose here to synonymize several genera (Quiritixys with Harttia; East Andean members of Crossoloricaria, and Apistoloricaria with Rhadinoloricaria; Ixinandria, Hemiloricaria, Fonchiiichthys, and Leliella with Rineloricaria), to restrict others (Crossoloricaria, and Sturisomatichthys to the West Andean members, and Sturisoma to the East Andean species), and to revalidate the genus Proloricaria.
Subject Areas: evolution/health and disease and epidemiology/ecology In social species, such as primates, facial appearances transmit a variety of social signals. Although it is suggested that the intense red colour of the face of the bald uakari monkey might be an indicator of health, this hypothesis still has not been verified. This study describes the histological structure of the skin of the face in the bald uakari, compared with other non-red neotropical primates, to better understand the maintenance of its colour. The facial skin of the bald uakari monkey is characterized by a thinner epidermis, absence of melanin pigments and a high density of vascular capillaries that spread below the epidermis. These vascular capillaries are larger and more tortuous than in other neotropical primates. The skin of the face of the bald uakari monkey allows a direct external assessment of haematological status, suggesting that the colour of the face would be an honest indicator of health, but could also signal sexual or behavioural states.
Large phylogenomics data sets require fast tree inference methods, especially for maximum-likelihood (ML) phylogenies. Fast
programs exist, but due to inherent heuristics to find optimal trees, it is not clear whether the best tree is found. Thus,
there is need for additional approaches that employ different search strategies to find ML trees and that are at the same
time as fast as currently available ML programs. We show that a combination of hill-climbing approaches and a stochastic perturbation
method can be time-efficiently implemented. If we allow the same CPU time as RAxML and PhyML, then our software IQ-TREE found
higher likelihoods between 62.2% and 87.1% of the studied alignments, thus efficiently exploring the tree-space. If we use
the IQ-TREE stopping rule, RAxML and PhyML are faster in 75.7% and 47.1% of the DNA alignments and 42.2% and 100% of the protein
alignments, respectively. However, the range of obtaining higher likelihoods with IQ-TREE improves to 73.3–97.1%. IQ-TREE
is freely available at http://www.cibiv.at/software/iqtree.
The black-faced uacaris are a poorly known group of platyrrhine monkeys from the Rio Negro basin in northwestern Amazonia. Originally described as two distinct species-Cacajao melanocephalus (Humboldt 1812) and Cacajao ouakary (Spix 1823)-from opposite banks of the Negro, they were treated as a single species until the end of the twentieth century, when molecular studies reconfirmed their status as true species. One of these studies not only nominated a third (northern) species, Cacajao ayresi Boubli et al. 2008, but also identified C. ouakary as a junior synonym of C. melanocephalus, resulting in the introduction of a new nomen, Cacajao hosomi Boubli et al. 2008. In the present study, additional evidence on morphological and zoogeographic variables is analyzed, which indicates that C. ouakary should be reinstated, and supports the nomination of a neotype of C. melanocephalus. The molecular and zoogeographic data on the species status of the ayresi form are also re-assessed, leading to the conclusion that, on the basis of the evidence available at the present time, this form should be considered a subspecies of C. melanocephalus. A new taxonomic arrangement is proposed, which recognizes two species, C. ouakary and C. melanocephalus, the latter with two subspecies, C. m. melanocephalus and C. m. ayresi.
Motivation:
Increasing attention has been devoted to estimation of species-level phylogenetic relationships under the coalescent model. However, existing methods either use summary statistics (gene trees) to carry out estimation, ignoring an important source of variability in the estimates, or involve computationally intensive Bayesian Markov chain Monte Carlo algorithms that do not scale well to whole-genome datasets.
Results:
We develop a method to infer relationships among quartets of taxa under the coalescent model using techniques from algebraic statistics. Uncertainty in the estimated relationships is quantified using the nonparametric bootstrap. The performance of our method is assessed with simulated data. We then describe how our method could be used for species tree inference in larger taxon samples, and demonstrate its utility using datasets for Sistrurus rattlesnakes and for soybeans.
Availability and implementation:
The method to infer the phylogenetic relationship among quartets is implemented in the software SVDquartets, available at www.stat.osu.edu/∼lkubatko/software/SVDquartets.
Here we report on the discovery of a new population of red uakaris in the mountains of northern San Martin, north-eastern Peru. This population is isolated from the other known uakari populations in the eastern lowlands, which raises questions concerning their taxonomic status and biogeographical history. This follows a recent range extension of this taxon west of the Ucayali River. Previously, the Peruvian red uakari (Cacajao calvus ucayalii) was only known in Peru from the lowlands between the Amazon, Ucayali and Yavarí Rivers.
Ursine bears are a mammalian subfamily that comprises six morphologically and ecologically distinct extant species. Previous phylogenetic analyses of concatenated nuclear genes could not resolve all relationships among bears, and appeared to conflict with the mitochondrial phylogeny. Evolutionary processes like incomplete lineage sorting and introgression can cause gene tree discordance and complicate phylogenetic inferences, but are not accounted for in phylogenetic analyses of concatenated data. We generated a high-resolution data set of autosomal introns from several individuals per species and of Y-chromosomal markers. Incorporating intraspecific variability in coalescence-based phylogenetic and gene flow estimation approaches, we traced the genealogical history of individual alleles. Considerable heterogeneity among nuclear loci and discordance between nuclear and mitochondrial phylogenies were found. A species tree with divergence time estimates indicated that ursine bears diversified within less than two million years. Consistent with a complex branching order within a clade of Asian bear species, we identified unidirectional gene flow from Asian black into sloth bears. Moreover, gene flow detected from brown into American black bears can explain the conflicting placement of the American black bear in mitochondrial and nuclear phylogenies. These results highlight that both incomplete lineage sorting and introgression are prominent evolutionary forces even on time scales up to several million years. Complex evolutionary patterns are not adequately captured by strictly bifurcating models, and can only be fully understood when analyzing multiple independently inherited loci in a coalescence framework. Phylogenetic incongruence among gene trees hence needs to be recognized as a biologically meaningful signal.
The neotropical primate family Pitheciidae consists of four genera Cacajao (uacaris), Callicebus (titis), Chiropotes (bearded sakis) and Pithecia (sakis), whose 40+ species display a range of sizes, social organisations, ecologies and habitats. Few are well known and the future survival of many is threatened, yet pitheciines have been little studied. This book is the first to review the biology of this fascinating and diverse group in full. It includes fossil history, reviews of the biology of each genus and, among others, specific treatments of vocalisations and foraging ecology. These studies are integrated into considerations of current status and future conservation requirements on a country-by-country basis for each species. A state-of-the-art summary of current knowledge, Evolutionary Biology and Conservation of Titis, Sakis and Uacaris is a collective effort from all the major researchers currently working on these remarkable animals.
Four species of spotted skunks (Carnivora, Mephitidae, Spilogale) are currently recognized: Spilogale angustifrons, S. gracilis, S. putorius, and S. pygmaea. Understanding species boundaries within this group is critical for effective conservation given that regional populations or subspecies (e.g., S. p. interrupta) have experienced significant population declines. Further, there may be currently unrecognized diversity within this genus as some taxa (e.g., S. angustifrons) and geographic regions (e.g., Central America) never have been assessed using DNA sequence data. We analyzed species limits and diversification patterns in spotted skunks using multilocus nuclear (ultraconserved elements) and mitochondrial (whole mitogenomes and single gene analysis) data sets from broad geographic sampling representing all currently recognized species and subspecies. We found a high degree of genetic divergence among Spilogale that reflects seven distinct species and eight unique mitochondrial lineages. Initial divergence between S. pygmaea and all other Spilogale occurred in the Early Pliocene (∼ 5.0 million years ago). Subsequent diversification of the remaining Spilogale into an “eastern” and a “western” lineage occurred during the Early Pleistocene (∼1.5 million years ago). These two lineages experienced temporally coincident patterns of diversification at ∼0.66 and ∼0.35 million years ago into two and ultimately three distinct evolutionary units, respectively. Diversification was confined almost entirely within the Pleistocene during a timeframe characterized by alternating glacial-interglacial cycles, with the origin of this diversity occurring in northeastern Mexico and the southwestern United States of America. Mitochondrial-nuclear discordance was recovered across three lineages in geographic regions consistent with secondary contact, including a distinct mitochondrial lineage confined to the Sonoran Desert. Our results have direct consequences for conservation of threatened populations, or species, as well as for our understanding of the evolution of delayed implantation in this enigmatic group of small carnivores.
ipyrad is a free and open source tool for assembling and analyzing restriction-site associated DNA sequence (RADseq) datasets using de novo and/or reference-based approaches. It is designed to be massively scalable to hundreds of taxa and thousands of samples, and can be efficiently parallelized on high performance computing clusters. It is available as both a command line interface (CLI) and as a Python package with an application programming interface (API), the latter of which can be used interactively to write complex, reproducible scripts, and implement a suite of downstream analysis tools.
Availability and implementation:
ipyrad is a free and open source program written in Python. Source code is available from the GitHub repository (https://github.com/dereneaton/ipyrad/), and Linux and MacOS installs are distributed through the conda package manager.
Supplementary information:
Complete documentation, including numerous tutorials, and Jupyter notebooks demonstrating example assemblies and applications of downstream analysis tools are available online: https://ipyrad.readthedocs.io/.
For half a century population genetics studies have put type II restriction endonucleases to work. Now, coupled with massively‐parallel, short‐read sequencing, the family of RAD protocols that wields these enzymes has generated vast genetic knowledge from the natural world. Here we describe the first software natively capable of using paired‐end sequencing to derive short contigs from de novo RAD data. Stacks version 2 employs a de Bruijn graph assembler to build and connect contigs from forward and reverse reads for each de novo RAD locus, which it then uses as a reference for read alignments. The new architecture allows all the individuals in a meta population to be considered at the same time as each RAD locus is processed. This enables a Bayesian genotype caller to provide precise SNPs, and a robust algorithm to phase those SNPs into long haplotypes – generating RAD loci that are 400‐800bp in length. To prove its recall and precision, we test the software with simulated data and compare reference‐aligned and de novo analyses of three empirical datasets. We show that the latest version of Stacks is highly accurate and outperforms other software in assembling and genotyping paired‐end de novo datasets.
Restriction site‐associated DNA sequencing (RADseq) has emerged as a useful tool in systematics and population genomics. A common feature of RADseq data sets is that they contain missing data that arise from multiple sources including genealogical sampling bias, assembly methodology and sequencing error. Many RADseq studies have demonstrated that allowing sites (single nucleotide polymorphisms, SNPs) with missing data can increase support for phylogenetic hypotheses. Two non‐mutually exclusive explanations for this observation are that (a) larger data sets contain more phylogenetic information; and (b) excluding missing data disproportionally removes sites with the highest mutation rates, causing the exclusion of characters that are likely variable and informative. Using a RADseq data set derived from the East African banana frog, Afrixalus fornasini (up to 1.1 million SNPs), we found that missing data thresholds were positively correlated with the proportion of parsimony‐informative sites and mean branch support. Using three proxies for estimating site‐specific rate, we found that the most conservative missing data strategies excluded rapidly evolving sites, with four‐state sites present only when allowing ≥60% missing data per SNP. Topological similarity among estimated phylogenies was highest for the data sets with ≥60% missing data per SNP. Our results suggest that several desirable phylogenetic qualities were observed when allowing ≥60% missing data per SNP. However, at the highest missing data thresholds (80% and 90% missing data per SNP), we observed differences in performance between high‐ and mixed‐weight DNA extraction samples, which may indicate there are trade‐offs to consider when using degraded genomic template with RADseq protocols.
We reconstruct the molecular phylogeny of Near Eastern mountain brook newts of the genus Neurergus (family Salamandridae) based on newly determined RADseq data, and compare the outcomes of concatenation-based phylogenetic reconstruction with species-tree inference. Furthermore, we test the current taxonomy of Neurergus (with four species: Neurergus strauchii, N. crocatus, N. kaiseri, and N. derjugini) against coalescent-based species-delimitation approaches of our genome-wide genetic data set. While the position of N. strauchii as sister species to all other Neurergus species was consistent in all of our analyses, the phylogenetic relationships between the three remaining species changed depending on the applied method. The concatenation approach, as well as quartet-based species-tree inference, supported a topology with N. kaiseri as the closest relative to N. derjugini, while full-coalescent species-tree inference approaches supported N. crocatus as sister species of N. derjugini. Investigating the individual signal of gene trees highlighted an extensive variation among gene histories, most likely resulting from incomplete lineage sorting. Coalescent-based species-delimitation models suggest that the current taxonomy might underestimate the species richness within Neurergus and supports seven species. Based on the current sampling, our analysis suggests that N. strauchii, N. derjugini and N. kaiseri might each be subdivided into further species. However, as amphibian species are known to be composed of deep conspecific lineages that do not always warrant species status, these results need to be cautiously interpreted in an integrative taxonomic framework. We hypothesize that the rather shallow divergences detected within N. kaiseri and N. derjugini likely reflect an ongoing speciation process and thus require further investigation. On the contrary, the much deeper genetic divergence found between the two morphologically and geographically differentiated subspecies of N. strauchii leads us to propose that N. s. barani should be considered a distinct species, N. barani (Öz 1994).
This article provides a phylogenetic analysis of five nuclear and mitochondrial cytochrome b genes of palaearctic serotines. Nuclear data yield five monophyletic clades: Botta’s serotine and the South African long-tailed house bat E. hottentottus; the common serotine bat (including all studied E. serotinus subspecies and andersoni form of undefined status) and the meridional serotine E. isabellinus; the Gobi serotine, including Bobrinski’s serotine; the northern bat; and New World serotines. We found latest taxonomic decisions regarding mirza and pachyomus questionable and needing further revision. The significant inconsistency between mitochondrial and nuclear phylogenies obtained for genes of different inheritance systems suggests repetitive introgression events in the evolution of the genus.
Model-based molecular phylogenetics plays an important role in comparisons of genomic data, and model selection is a key step in all such analyses. We present ModelFinder, a fast model-selection method that greatly improves the accuracy of phylogenetic estimates by incorporating a model of rate heterogeneity across sites not previously considered in this context and by allowing concurrent searches of model space and tree space.
Uakari monkeys from the Amazon River basin are the most specialized primates in the Neotropical region. Their short tails, peculiar dentition and external morphology are strikingly divergent from most other platyrrhines. Furthermore, their geographical range is small and restricted to the forests in the floodplains of Amazonian Rivers. It is the only frugivorous primate able to live within the young (white-water river floodplain) of the Amazon. A 20-month study of the ecology of the white uakaris was carried out in the floodplain located between the Japur and Amazon Rivers in Brazilian Amazonia. The vegetation is unique in the way that it is able to cope with a 12-metre annual change in water level. This annual variation in water level is probably the most important overall ecological mechanism in , influencing the temporal and spatial patterns of distribution of fruits. Several aspects of the ecology and ranging behaviour of the uakaris are associated with the temporal and spatial patterns of distribution of potential food sources: the seeds of immature fruits. Subdividing fruits into separate morphological classes is of fundamental importance for understanding this variation, which is largely influenced by the changes in water level. Foods of high quality, high energetic value and low in secondary compounds, are extremely important at most times of the year due to the Uakari's gut structure, metabolic requirements, use of space and, especially the topography of their habitat. Comparisons are made with another pithecine of similar morphology and diet, but which lives in the dry terra firrne forests. Based on their present distribution and ecological preferences, an attempt is made to trace the evolutionary history of these two largest pithecines. Furthermore, the role of riverine habitats in the zoogeographic and speciation patterns of primates within Amazonia is discussed.
In Bayesian phylogenetic analyses of genetic data, prior probability distributions need to be specified for the model parameters, including the tree. When Bayesian methods are used for molecular dating, available tree priors include those designed for species-level data, such as the pure-birth and birth-death priors, and coalescent-based priors designed for population-level data. However, molecular dating methods are frequently applied to data sets that include multiple individuals across multiple species. Such data sets violate the assumptions of both the speciation and coalescent-based tree priors, making it unclear which should be chosen and whether this choice can affect the estimation of node times. To investigate this problem, we used a simulation approach to produce data sets with different proportions of within- and between-species sampling under the multispecies coalescent model. These data sets were then analysed under pure-birth, birth-death, constant-size coalescent, and skyline coalescent tree priors. We also explored the ability of Bayesian model testing to select the best-performing priors. We confirmed the applicability of our results to empirical data sets from cetaceans, phocids, and coregonid whitefish. Estimates of node times were generally robust to the choice of tree prior, but some combinations of tree priors and sampling schemes led to large differences in the age estimates. In particular, the pure-birth tree prior frequently led to inaccurate estimates for data sets containing a mixture of inter- and intraspecific sampling, whereas the birth-death and skyline coalescent priors produced stable results across all scenarios. Model testing provided an adequate means of rejecting inappropriate tree priors. Our results suggest that tree priors do not strongly affect Bayesian molecular dating results in most cases, even when severely misspecified. However, the choice of tree prior can be significant for the accuracy of dating results in the case of data sets with mixed inter- and intraspecies sampling.
The neotropical primate family Pitheciidae consists of four genera Cacajao (uacaris), Callicebus (titis), Chiropotes (bearded sakis) and Pithecia (sakis), whose 40+ species display a range of sizes, social organisations, ecologies and habitats. Few are well known and the future survival of many is threatened, yet pitheciines have been little studied. This book is the first to review the biology of this fascinating and diverse group in full. It includes fossil history, reviews of the biology of each genus and, among others, specific treatments of vocalisations and foraging ecology. These studies are integrated into considerations of current status and future conservation requirements on a country-by-country basis for each species. A state-of-the-art summary of current knowledge, Evolutionary Biology and Conservation of Titis, Sakis and Uacaris is a collective effort from all the major researchers currently working on these remarkable animals.
This article reviews changes in primate taxonomy, especially those pertaining to the meaning of the term species, since its inception two and a half centuries ago. Despite continuing discoveries and the involvement of competent practitioners, the adoption of the polytypic species concept, especially underpinned by the biological species concept, ensured that primate taxonomy was in a sorry state by the middle of the twentieth century. In the latter half of the twentieth century, a gradual rethinking of the nature of species took place, and many different species concepts were proposed. The phylogenetic species concept has been widely adopted over the past ∼20 years, sustained by a gradual realization that species are evolutionary lineages. This review provides examples of how the old way of thinking about species hampered our understanding of primate biodiversity and of how the phylogenetic species concept (or the diagnosability criterion under the general lineage concept) has clarified matters, opening them up for discussion. The adoption of this evolutionary view of species has implications for conservation, particularly because it increases recognition of biodiversity.
In a 1935 paper and in his book Theory of Probability, Jeffreys developed a methodology for quantifying the evidence in favor of a scientific theory. The centerpiece was a number, now called the Bayes factor, which is the posterior odds of the null hypothesis when the prior probability on the null is one-half. Although there has been much discussion of Bayesian hypothesis testing in the context of criticism of P-values, less attention has been given to the Bayes factor as a practical tool of applied statistics. In this article we review and discuss the uses of Bayes factors in the context of five scientific applications in genetics, sports, ecology, sociology, and psychology. We emphasize the following points:
The squirrel monkey, Saimiri, is a pan-Amazonian Pleistocene radiation. We use statistical phylogeographic methods to create a mitochondrial DNA-based timetree for 118 squirrel monkey samples across 68 localities spanning all Amazonian centers of endemism, with the aim of better understanding (1) the effects of rivers as barriers to dispersal and distribution; (2) the area of origin for modern Saimiri; (3) whether ancestral Saimiri was a lowland lake-affiliated or an upland forest taxa; and (4) the effects of Pleistocene climate fluctuation on speciation. We also use our topology to help resolve current controversies in Saimiri taxonomy and species relationships. The Rondônia and Inambari centers in the southern Amazon were recovered as the most likely areas of origin for Saimiri. The Amazon River proved a strong barrier to dispersal, and squirrel monkey expansion and diversification was rapid, with all speciation events estimated to occur between 1.4 and 0.6 Ma, predating the last three glacial maxima and eliminating climate extremes as the main driver of squirrel monkey speciation. Saimiri expansion was concentrated first in central and western Amazonia, which according to the "Young Amazon" hypothesis was just becoming available as floodplain habitat with the draining of the Amazon Lake. Squirrel monkeys also expanded and diversified east, both north and south of the Amazon, coincident with the formation of new rivers. This evolutionary history is most consistent with a Young Amazon Flooded Forest Taxa model, suggesting Saimiri has always maintained a lowland wetlands niche and was able to greatly expand its range with the transition from a lacustrine to a riverine system in Amazonia. Saimiri vanzolinii was recovered as the sister group to one clade of Saimiri ustus, discordant with the traditional Gothic versus Roman morphological division of squirrel monkeys. We also found paraphyly within each of the currently recognized species: S. sciureus, S. ustus, and S. macrodon. We discuss evidence for taxonomic revision within the genus Saimiri, and the need for future work using nuclear markers.
There is a lack of consensus on how next-generation sequence data should be considered for phylogenetic and phylogeographic estimates, with some studies excluding loci with missing data, while others include them, even when sequences are missing from a large number of individuals. Here we use simulations, focusing specifically on RAD sequences, to highlight some of the unforeseen consequence of excluding missing data from next-generation sequencing. Specifically, we show that in addition to the obvious effects associated with reducing the amount of data used to make historical inferences, the decisions we make about missing data (such as the minimum number of individuals with a sequence for a locus to be included in the study) also impact the types of loci sampled for a study. In particular, as the tolerance for missing data becomes more stringent, the mutational spectrum represented in the sampled loci becomes truncated such that loci with the highest mutation rates are disproportionately excluded. This effect is exacerbated further by factors involved in the preparation of the genomic library (i.e., the use of reduced representation libraries, as well as the coverage) and the taxonomic diversity represented in the library (i.e., the level of divergence among the individuals). We demonstrate that the intuitive appeals about being conservative by removing loci may be misguided.
Restriction-site associated genomic markers are a powerful tool for investigating evolutionary questions at the population level, but are limited in their utility at deeper phylogenetic scales where fewer orthologous loci are typically recovered across disparate taxa. While this limitation stems in part from mutations to restriction recognition sites that disrupt data generation, an additional source of data loss comes from the failure to identify homology during bioinformatic analyses. Clustering methods that allow for lower similarity thresholds and the inclusion of indel variation will perform better at assembling RADseq loci at the phylogenetic scale.
PyRAD is a pipeline to assemble de novo RADseq loci with the aim of optimizing coverage across phylogenetic data sets. It utilizes a wrapper around an alignment-clustering algorithm which allows for indel variation within and between samples, as well as for incomplete overlap among reads (e.g., paired-end). Here I compare PyRAD with the program Stacks in their performance analyzing a simulated RADseq data set that includes indel variation. Indels disrupt clustering of homologous loci in Stacks but not in PyRAD, such that the latter recovers more shared loci across disparate taxa. I show through re-analysis of an empirical RADseq data set that indels are a common feature of such data, even at shallow phylogenetic scales. PyRAD utilizes parallel processing as well as an optional hierarchical clustering method which allow it to rapidly assemble phylogenetic data sets with hundreds of sampled individuals.
Software is written in Python and freely available at http://www.dereneaton.com/software/ SUPPLEMENT: Scripts to completely reproduce all simulated and empirical analyses are available in the Supplementary Materials.
The way we view the Species category in Primates, as in other animals, especially other vertebrates, has been going through a revolution over the past 20 years or so. Much is wrong with the idea that we can define species according to whether or not they are "reproductively isolated": this concept, the so-called Biological Species Concept, has never offered any guidelines in the case of allopatric populations; this has now been shown to be simply wrong. Although other ways of looking at species - the Evolutionary, Recognition, Cohesion and Genetic Species Concepts - have all provided particular insights, the only proposal to offer a repeatable, falsifiable definition of species is the Phylogenetic Species Concept. This has been criticised for increasing the number of species to be recognised, although it is not clear why this should be a problem: indeed, it tells us that the world is far richer in biodiversity than we had conceived. Am. J. Primatol. 74:687-691, 2012. © 2012 Wiley Periodicals, Inc.
The white bald uakari (Cacajao calvus calvus) is among the least studied of the Amazonian primates and is found exclusively in remote areas of the central Amazon. The geographic distribution of this subspecies is still uncertain, and information on current threats and its conservation status is sparse. In this paper, we identify new locations of occurrence and propose range expansion of the Cacajao calvus calvus. Between 2008 and 2010, six field expeditions were undertaken in the middle Solimões region to search for the subspecies and to conduct interviews with local residents regarding its presence. The presence of the white bald uakari was confirmed in the lower courses of the Juruá and lower Jutaí rivers, in addition to areas inside the Mamirauá Reserve, where its presence was expected. Results indicate an expansion and new limits on the geographic range of the subspecies, including its detection in areas in which it had not previously been reported and its exclusion from areas where white bald uakaris were assumed to occur. The new information provided by this study and the remaining shortcomings regarding the distribution of the calvus group point to the urgent need for further research on the geographic distribution and habitat use of this group, especially along the lower courses of the Juruá and Jutaí rivers, which remain little explored.
Biodiversity conservation in the Amazonian várzea depends heavily on the protection of large portions of this threatened environment. In the Brazilian Amazon there is a handful
of protected areas with significant portions of várzea, but only one large protected area entirely formed by this particular ecosystem, the Mamirauá Sustainable Development Reserve
(MSDR), created by the Amazonas State government in the early 1990’s. This reserve has been comanaged by a Brazilian NGO since
its creation, in continuing cooperation between public and private efforts for the conservation of the várzea and its biodiversity. Here, we present the trajectory of this protected area, and a special emphasis is given for one of
the most relevant elements of Mamirauá, the involvement of different social actors interested and concerned with local protection
and conservation. In the case of the Mamirauá Reserve, this involvement was crucial to deal with the many challenges related
to the protection of such a large portion of the territory. The combined efforts of government, NGOs, and the local population,
among other actors, also made possible a strong positive impact on the maintenance of local livelihoods and the improvement
of the quality of life for the local inhabitants. Possibly as a consequence of that improvement, increasing population growth
rates may now pose a threat for the near future of the reserve, and require new, enhanced forms of sustainable use for local
biodiversity. Besides that, it is important to maintain the widespread distribution of benefits from these conservation practices
for all social actors involved.
The two known species of uacaries, inhabitants of the upper Amazonian region, are the black head Cacajao melanocephalus with subspecies C. m. melanocephalus Humboldt and C. m. ouakary Spix, and the larger bald head uacari C. calvus with subspecies C. c. ucayalii Thomas, C. c. rubicundus I. Geoffroy and Deville, C. c. calvus I. Geoffroy, and C. c. novaesi described as new. The diagnostic generic characters described are the external, cranial, dental, some postcranial, and cytogenetic. The species are described and compared and their geographic distribution plotted with those of their subspecies delimited. Sexual differences are outlined. Apart from size-related characters, the species and subspecies are distinguished by pelage pattern of head and coloration in general. It is shown that both species could have diverged from a hairy-headed melanistic ancestral form. Pelage divergence in the descendants was expressed by the more pilose head of C. melanocephalus, and less pilose of C. calvus. Coloration differentiation was geographic and followed metachromic lines with mutation from eumelanism to partial pheomelanism (reddish or golden) in C. melanocephalus and to virtually complete pheomelanism in C. calvus. The subspecies of each species are distinguished by color patterns resulting from selective bleaching or dilution of the pheomelanin fields. The most saturate pheomelanic subspecies of C. calvus is C. c. ucayalii and the most dilute is the albinotic C. c. calvus. Correlation between coloration and environment is not evident. A gazetteer identifies all locality records plotted by numbers on the geographic distribution maps.