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The pygmy marmoset, the smallest of the anthropoid primates, has a broad distribution in Western Amazonia. Recent studies using molecular and morphological data have identified two distinct species separated by the Napo and Solimões-Amazonas rivers. However, reconciling this new biological evidence with current taxonomy, i.e., two subspecies, Cebuella pygmaea pygmaea (Spix, 1823) and Cebuella pygmaea niveiventris (Lönnberg, 1940), was problematic given the uncertainty as to whether Spix's pygmy marmoset ( Cebuella pygmaea pygmaea) was collected north or south of the Napo and Solimões-Amazonas rivers, making it unclear to which of the two newly revealed species the name pygmaea would apply. Here, we present the first molecular data from Spix's type specimen of Cebuella pygmaea, as well as novel mitochondrial genomes from modern pygmy marmosets sampled near the type locality (Tabatinga) on both sides of the river. With these data, we can confirm the correct names of the two species identified, i.e., C. pygmaea for animals north of the Napo and Solimões-Amazonas rivers and C. niveiventris for animals south of these two rivers. Phylogenetic analyses of the novel genetic data placed into the context of cytochrome b gene sequences from across the range of pygmy marmosets further led us to re-evaluate the geographical distribution for the two Cebuella species. We dated the split of these two species to 2.54 million years ago. We discuss additional, more recent, subdivisions within each lineage, as well as potential contact zones between the two species in the headwaters of these rivers.

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OBJECTIVES: We investigated the diversity of the pygmy marmoset, Cebuella pygmaea, by comparing genetic, morphological and pelage traits of animals from Peru and Ecuador. MATERIALS AND METHODS: We extracted DNA from museum specimen osteocrusts and from fecal samples collected from free-ranging individuals. We sequenced the mtDNA cytochrome b gene and the control region from samples collected at 13 different sites and used Bayesian inference and Maximum Likelihood to identify distinct clades. We took measurements of the crania of a subset of these specimens (n = 26) and ran a logistic regression to determine if any of the cranial measurements (n = 22) could predict a specimen's clade. In addition, we examined the pelage patterns of the museum specimens and photographs taken of free-ranging individuals and divided them into pelage types based on coloration of the underbelly. RESULTS: We identified two divergent clades, and two distinct groups with clear geographic boundaries within one of those clades. Two measurements of the zygomatic bone perfectly predicted a given individual's mtDNA clade. We found four distinct pelage patterns in our samples, but these patterns are variable within clades and among individuals within the same population. CONCLUSION: These analyses indicate that the two recognized subspecies of pygmy marmoset should be elevated to the species level (C. pygmaea and C. niveiventris) based on molecular and cranial differences but not on pelage patterns. We provide evidence on the geographic limits of the two clades and identify regions where additional sampling is required to better define the geographic distribution of the two clades.

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Genetic diversity provides populations with the possibility to persist in ever-changing environments, where selective regimes change over time. Therefore, the long-term survival of a population may be affected by its level of genetic diversity. The Mexican howler monkey (Alouatta palliata mexicana) is a critically endangered primate restricted to southeast Mexico. Here, we evaluate the genetic diversity and population structure of this subspecies based on 83 individuals from 31 groups sampled across the distribution range of the subspecies, using 29 microsatellite loci. Our results revealed extremely low genetic diversity (HO = 0.21, HE = 0.29) compared to studies of other A. palliata populations and to other Alouatta species. Principal component analysis, a Bayesian clustering method, and analyses of molecular variance did not detect strong signatures of genetic differentiation among geographic populations of this subspecies. Although we detect small but significant FST values between populations, they can be explained by a pattern of isolation by distance. These results and the presence of unique alleles in different populations highlight the importance of implementing conservation efforts in multiple populations across the distribution range of A. p. mexicana to preserve its already low genetic diversity. This is especially important given current levels of population isolation due to the extreme habitat fragmentation across the distribution range of this primate.

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OBJECTIVES: Ecological similarity between species can lead to interspecific trophic competition. However, when ecologically similar species coexist, they may differ in foraging strategies and habitat use, which can lead to niche partitioning. As the body tissues of consumers contain a stable isotope signature that reflects the isotopic composition of their diet, stable isotope analysis is a useful tool to study feeding behavior. We measured the isotopic niche width, which is a proxy for trophic niche width, of mantled (Alouatta palliata) and black (A. pigra) howler monkeys. Specifically, studied populations in allopatry and sympatry to assess whether these species showed niche partitioning. MATERIALS AND METHODS: Between 2008 and 2012, we collected hair samples from 200 subjects (113 black and 87 mantled howler monkeys) and used continuous flow isotope ratio mass spectrometry to estimate δ13 C and δ15 N. We described the isotopic niche width of each species in allopatry and sympatry with the Bayesian estimation of the standard ellipse areas. RESULTS: In allopatry, isotopic niche width and isotopic variation were similar in both species. In sympatry, black howler monkeys had a significantly broader isotopic niche, which was mainly determined by high δ15 N values, and included the majority of mantled howler monkeys' isotopic niche. The isotopic niche of mantled howler monkeys did not differ between sympatry and allopatry. CONCLUSIONS: The coexistence of these ecologically similar species may be linked to trophic niche adjustments by one species, although the particular features of such adjustments (e.g., dietary, spatial, or sensory partitioning) remain to be addressed.

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Evolutionary research benefits form the integration of laboratory and field components to determine factors and processes that affect the evolutionary trajectories of species. Our shared interest in understanding hybridization with genetic admixture as a process that may impact social, behavioral, and ecological features of primates, brought us together in a collaborative project aimed at addressing how vocal variation in two species of howler monkeys in Mexico affects and is affected by hybridization. To achieve this goal, we joined our academic expertise in studying primate genetics, ecology, and behavior under different natural and experimental conditions. We took advantage of decades of experience studying and handing wild howler monkeys for translocation projects to safely sample and study wild populations for this project. Here, we describe the history of our collaboration highlighting how our different perspectives, academic realities, and individual strengths built the foundation for our successful collaboration. We also share our perspectives on how this collaboration opened up new academic venues, broadened our individual perspectives on the integration of different research approaches to address a complex topic, and allowed us to recognize the strength of international collaboration.

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Interspecific hybridization allows the introgression or movement of alleles from one genome to another. While some genomic regions freely exchange alleles during hybridization, loci associated with reproductive isolation do not intermix. In many model organisms, the X chromosome displays limited introgression compared to autosomes owing to the presence of multiple loci associated with hybrid sterility or inviability (the "large X-effect"). Similarly, if hybrids are produced, the heterogametic sex is usually inviable or sterile, a pattern known as Haldane's rule. We analyzed the patterns of introgression of genetic markers located in the mitochondrial (control region) and nuclear (autosomal microsatellites and sex chromosome genes) genomes of two howler monkey species (Alouatta palliata and A. pigra) that form a natural hybrid zone in southern Mexico, to evaluate whether the large X-effect and Haldane's rule affect the outcomes of hybridization between these sister species. To identify the level of admixture of each individual in the hybrid zone (N = 254) we analyzed individuals sampled outside the hybrid zone (109 A. pigra and 39 A. palliata) to determine allele frequencies of parental species and estimated a hybrid index based on nuclear markers. We then performed a cline analysis using individuals in the hybrid zone to determine patterns of introgression for each locus. Our analyses show that although the hybrid zone is bimodal (with no known F1 s and few recent generation hybrids) and quite narrow, there has been extensive introgression in both directions, and there is a large array of admixed individuals in the hybrid zone. Mitochondrial and most autosomal markers showed bidirectional introgression, but some had biased introgression toward one species or the other. All markers on the sex chromosomes and a few autosomal markers showed highly restricted introgression. This pattern is consistent with the hypothesis that the sex chromosomes make a disproportionate contribution to reproductive isolation, and our results broaden the taxonomic representation of these patterns across animal taxa.

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OBJECTIVES: When closely related species overlap geographically, selection may favor species-specific mate recognition traits to avoid hybridization costs. Conversely, the need to recognize potential same-sex rivals may select for lower specificity, creating the possibility that selection in one domain constrains evolution in the other. Despite a wealth of data on mate recognition, studies addressing rival recognition between hybridizing species are limited to a few bird species. Using naïve populations, we examine the extent to which failed rival recognition might have affected hybridization patterns when two species of howler monkeys (Alouatta pigra and A. palliata) first met after diverging in allopatry. METHODS: We simulated first contact between naïve subjects using playback experiments in allopatric populations of the two purebred species. Using linear mixed models, we compared their look, move, and vocal responses to conspecific and heterospecific loud calls. RESULTS: Although not different in overall response strength to playbacks, the two species differed in reaction to heterospecific callers. Male A. pigra ignored calls from male A. palliata, but the reverse was not true. DISCUSSION: Despite striking differences in vocalizations, A. palliata respond equally to calls from both species whereas A. pigra respond only to conspecifics. This apparent failure of A. pigra males to recognize interspecific rivals might have biased hybridization (F1 hybrids = male A. palliata x female A. pigra), a pattern previously hypothesized based on genetic analysis of hybrids. Given that A. pigra males could be losing reproductive opportunities to heterospecific males, our findings add to growing evidence of potential costs for overly specific species recognition.

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Comparing vocalizations across species is useful for understanding acoustic variation at mechanistic and evolutionary levels. Here, we take advantage of the divergent vocalizations of two closely related howler monkey species (Alouatta pigra and A. palliata) to better understand vocal evolution. In addition to comparing multiple acoustic and temporal features of roars and the calling bouts in which they are produced, we tested several predictions. First, A. pigra should have roars with lower fundamental frequency and lower formant dispersion because they are larger than A. palliata and have a larger hyoid apparatus. Second, A. pigra should have faster calling rates, longer roars, longer bouts, and exaggerated call features linked to vocal effort (e.g., nonlinear phenomena and emphasized frequencies) because they are the more aggressive species during intergroup encounters. We found significant interspecific differences supporting our predictions in every tested parameter of roars and bouts, except for roar duration and barking rate. Stepwise discriminant function analyses identified the best features for differentiating roars (acoustic features: formant dispersion followed by highest frequency; temporal features: longest syllable duration followed by number of syllables). Although resembling each other more than they resemble South American howler monkeys, our comparison revealed striking differences in the vocalizations of the two Mesoamerican species. While we cannot completely rule out the influence of body size or the environmental conditions in which the two species evolved, vocal differences were likely influenced by sexual selection. The exaggerated roars and intense calling patterns in A. pigra seem more suitable for intergroup competition, whereas A. palliata calls may be better suited for mate attraction and competition within groups. With interspecific acoustic differences quantified, we will now be able to examine how vocalizations contribute to the evolutionary dynamics of the A. palliata × A. pigra hybrid zone in southern Mexico. Am. J. Primatol. 78:755-766, 2016. © 2016 Wiley Periodicals, Inc.

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Mesoamerican spider monkeys (Ateles geoffroyi sensu lato) are widely distributed from Mexico to northern Colombia. This group of primates includes many allopatric forms with morphologically distinct pelage color and patterning, but its taxonomy and phylogenetic history are poorly understood. We explored the genetic relationships among the different forms of Mesoamerican spider monkeys using mtDNA sequence data, and we offer a new hypothesis for the evolutionary history of the group. We collected up to ∼800 bp of DNA sequence data from hypervariable region 1 (HV1) of the control region, or D-loop, of the mitochondrion for multiple putative subspecies of Ateles geoffroyi sensu lato. Both maximum likelihood and Bayesian reconstructions, using Ateles paniscus as an outgroup, showed that (1) A. fusciceps and A. geoffroyi form two different monophyletic groups and (2) currently recognized subspecies of A. geoffroyi are not monophyletic. Within A. geoffroyi, our phylogenetic analysis revealed little concordance between any of the classifications proposed for this taxon and their phylogenetic relationships, therefore a new classification is needed for this group. Several possible clades with recent divergence times (1.7-0.8 Ma) were identified within Ateles geoffroyi sensu lato. Some previously recognized taxa were not separated by our data (e.g., A. g. vellerosus and A. g. yucatanensis), while one distinct clade had never been described as a different evolutionary unit based on pelage or geography (Ateles geoffroyi ssp. indet. from El Salvador). Based on well-supported phylogenetic relationships, our results challenge previous taxonomic arrangements for Mesoamerican spider monkeys. We suggest a revised arrangement based on our data and call for a thorough taxonomic revision of this group.

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New research presented in this special issue of Molecular Phylogenetics and Evolution on the "Phylogeny and Biogeography of Neotropical Primates" greatly improves our understanding of the evolutionary history of the New World monkeys and provides insights into the multiple platyrrhine radiations, diversifications, extinctions, and recolonizations that have taken place over time and over space in the Neotropics. Here, we synthesize genetic and biogeographic research from the past several years to construct an overarching hypothesis for platyrrhine evolution. We also highlight continuing controversies in Neotropical primate biogeography, such as whether the location of origin of platyrrhines was Africa or Asia; whether Patagonian fossil primates are stem or crown platyrrhines; and whether cis- and trans-Andean Neotropical primates were subject to vicariance through Andes mountain building, or instead diversified through isolation in mountain valleys after skirting around the Andes on the northwestern coast of South America. We also consider the role of the Amazon River and its major tributaries in shaping platyrrhine biodiversity, and how and when primates from the Amazon reached the Atlantic Forest. A key focus is on primate colonizations and extirpations in Central America, the Andes, and the seasonally dry tropical forests and savannas (such as the Llanos, Caatinga, and Cerrado habitats), all ecosystems that have been understudied up until now for primates. We suggest that most primates currently inhabiting drier open habitats are relatively recent arrivals, having expanded from rainforest habitats in the Pleistocene. We point to the Pitheciidae as the taxonomic group most in need of further phylogenetic and biogeographic research. Additionally, genomic studies on the Platyrrhini are deeply needed and are expected to bring new surprises and insights to the field of Neotropical primate biogeography.

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