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Distribution map for putative subspecies of Ateles geoffroyi and for A. fusciceps (adapted from Rylands et al., 2006 and spatial data provided by the IUCN, http:// www.iucnredlist.org/), with sample locations used in this study indicated by stars. The number of samples used from each site is indicated above the symbol. Black stars indicate samples with well-documented provenience, while white stars indicate that the sample came from a confiscated or captive animal with uncertain provenience that has been only assigned rough geographic coordinates. Where multiple samples are indicated at these rough coordinates (e.g., for A. g. vellerosus from Veracruz, México), they likely represent individuals collected from several locations around that general area. The samples of A. f. fusciceps were collected by the first author at the indicated coordinates in the Darien region of Panama. Although those coordinates fall within the distribution of A. geoffroyi griscesens included in IUCN maps, the animals clearly belong to the species A. fusciceps, both phenotypically and genetically.
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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...
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Context 1
... hair, and/or fecal samples of Mesoamerican spider monkeys from across the taxon's known geographic range were either collected in the field by the first author or were obtained by donation from in-country collaborators (Fig. 2). Following Rylands et al.'s (2006) classification of subspecies names (as it represents the taxonomy currently utilized by the IUCN: Cuarón et al., 2008), and based on the geographic provenance of samples, our dataset of 50 samples includes five of seven putative subspecies of A. geoffroyi as well as samples of the two putative ...
Context 2
... A. fusciceps, and A. paniscus (outgroup) used in this study, along with the sample ID, putative taxonomic assignment based on pelage, and country of origin. Coordinates included in brackets [ ] reflect those samples for which we do not have precise locations. For these, we use the coordinates of the general area of origin, as indicated in Fig. 2 prior for the root of the tree -i.e., for the divergence of A. paniscus from A. geoffroyi + A. fusciceps -at 3.50 ± 0.86 mya, which again covers the 95% HPD estimated for this divergence in our broader study (Morales-Jimenez et al., 2015). Finally, we also constrained all of the clades within A. geoffroyi and A. fusciceps that were ...
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... spite of the lack of concordance between phylogenetic position and the subspecific assignments of some haplotypes, the phylogenetic relationships among different mtDNA haplotypes of A. geoffroyi in Mesoamerica are generally consistent with the country and broader geographic regions from which the samples originated (Fig. 2): the A clade comprised samples from Mexico, Belize and Guatemala; the B clade comprised samples from El Salvador, southwestern Nicaragua and northwestern Costa Rica; and the C clade included only samples from Panama, but no samples from that country or elsewhere assigned to A. fusciceps (Fig. 3). Based on our HV1 control region ...
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... Genomic analysis confirmed species identification of A. geoffroyi; however, the few population-level genetic studies of A. geoffroyi have focused on mitochondrial markers (88,89), limiting the available data for comparative analyses. The two possible subspecies are not monophyletic with the available mitochondrial markers (SI Appendix, Fig. S7) (89); as such, subspecies could only be narrowed down to A. geoffroyi vellerosus or A. geoffroyi yucatanensis with genetic data. ...
... Genomic analysis confirmed species identification of A. geoffroyi; however, the few population-level genetic studies of A. geoffroyi have focused on mitochondrial markers (88,89), limiting the available data for comparative analyses. The two possible subspecies are not monophyletic with the available mitochondrial markers (SI Appendix, Fig. S7) (89); as such, subspecies could only be narrowed down to A. geoffroyi vellerosus or A. geoffroyi yucatanensis with genetic data. Genomic data support zooarchaeological assessment that the spider monkey was female. ...
... The sample and negatives were dual-indexed and sequenced on a 2 × 150 NextSeq run. Raw reads were quality filtered with AdapterRemoval2 and mapped with bwa using parameters for aDNA to the A. geoffroyi genome (GenBank assembly: GCA_004024785.1) and competitively mapped to publicly available spider monkey mitochondrial sequences (89,96,97). A section of the CytB gene was isolated from the competitively mapped alignment and compared to the regional spider monkey dataset (SI Appendix, Supplementary Text) for phylogenetic analysis. ...
A multimethod archaeometry study (zooarchaeological, isotopic, ancient DNA, paleobotanical, and radiocarbon dating) of a spider monkey sacrificed in the ceremonial center of Teotihuacan, Mexico (1 to 550 CE) is interpreted as a diplomatic gift exchange with neighboring Maya. Not only does this spider monkey provide the earliest known instance of primate translocation and captivity in Mesoamerica, it helps date incipient modes of interregional diplomacy between two major powers during Early Classic Mesoamerica: Teotihuacan and the Maya. Details of human-primate interaction include age at capture and transport (before ∼3 y of age), captive duration (over 2 y), anthropogenic diet (staple was maize, though secondary resources unique to anthropogenic diet including arrowroot and chili pepper were also found), context of sacrifice (tethered and associated with complete golden eagle and an array of other statecrafts), and general site context (including presence of Maya vessels and Maya-style murals). The timing of the spider monkey's sacrifice (250 to 300 CE) and its life history suggest a reconsideration of epigraphically attested militaristic involvement of Teotihuacan at certain Maya sites. We propose that a period of more multilateral and fluid ritual exchange with Maya dignitaries preceded the Teotihuacan state's eventual ascent to prominence.
... Inbreeding is another imminent risk for El Salvador's spider monkeys, due to the lack of connectivity and low number of individuals in some forest patches. Local reproduction between consanguineous monkeys is a concern for their conservation (Hagell et al., 2013), since it has been linked to congenital malformations (Charpentier et al., 2007) and child mortality in other primate species (Rails and Ballou, 1982 -Jimenez et al., 2015). This knowledge would be useful to propose better conservation and management actions, especially for confiscated spider monkeys of unknown origin. ...
... frontatus), and Panama (A.g. azuerensis and A.g. ornatus)(Morales-Jimenez et al., 2015). Overall, there is a lack of phylogenetic studies including wild spider monkeys' samples from Guatemala, Honduras, and El Salvador (pers. ...
Spider monkeys (genus Ateles) are distributed across rainforests from southern Mexico to northern Bolivia, but at risk of extinction across much of their range. Like most members of the genus, the black-handed spider monkey, or the Central American spider monkey, Ateles geoffroyi is particularly vulnerable to anthropogenic threats, due to its inability to persist in disturbed and/or isolated forest patches and is categorized as "Endangered" by the IUCN. Within its range in El Salvador, the smallest country in Central America, the spider monkey has now been restricted to isolated patches of semi-deciduous forests, including four fragments that lie within a disturbed agricultural landscape in Jiquilisco Bay, in Southeast El Salvador. We analyzed 73 noninvasive fecal samples from spider monkeys in this region, and we were able to identify 55 individuals. We evaluated the genetic diversity and structure of the four populations using microsatellite markers. Our results show higher observed than expected heterozygosity, but low genetic diversity compared to published data on other spider monkey populations (Ho = 0.50-0.57 and He = 0.39-0.51; allelic richness with rarefaction = 2.71-3.22; private alleles with rarefaction = 0.18-0.61). We also found significant differentiation across fragments (Fst = 0.2, P < 0.001) and two genetically different groups. These findings suggest the need for conservation action to reconnect forest patches, to improve the unfavorable situation of the only non-human primate in El Salvador.
Resumen Los monos araña (género Ateles) están distribuidos por las selvas tropicales desde el sur de México hasta el norte de Bolivia, pero están en peligro de extinción en gran parte de su área de distribución. Como la mayoría de los miem-bros del género, el mono araña de manos negras, o el mono araña centroamericano, Ateles geoffroyi es particularmente vulnerable a las amenazas antropogénicas, debido a su incapacidad para persistir en parches de bosque perturbados y/o aislados, y está categorizado como "En peligro" por la UICN. Dentro de su área de distribución en El Salvador, el país más pequeño de Centroamérica, el mono araña se ha restringido a parches aislados de bosques semicaducifolios, incluyendo cuatro fragmentos que se encuentran dentro de un paisaje agrícola perturbado en la Bahía de Jiquilisco, en el sureste de El Salvador. Analizamos 73 muestras fecales no invasivas de monos araña en esta región, y pudimos iden-tificar 55 individuos. Evaluamos la diversidad y estructura genética de las cuatro poblaciones utilizando marcadores de microsatélites. Nuestros resultados muestran una heterocigosidad observada superior a la esperada, pero una baja diversidad genética en comparación con los datos publicados sobre otras poblaciones de monos araña (Ho = 0,50-0,57 y He = 0,39-0,51; riqueza alélica con rarefacción = 2,71-3,22; alelos privados con rarefacción = 0,18-0,61). También en-contramos una diferenciación significativa entre fragmentos (Fst = 0,2, P < 0,001) y dos grupos genéticamente diferentes. Estos hallazgos sugieren la necesidad de acciones de conservación para reconectar los parches de bosque, para mejorar la situación desfavorable del único primate no humano en El Salvador. Palabras clave: Microsatélites, muestras no invasivas, estructura genética, fragmentos de bosque, Áreas Naturales Protegidas.
... Groves (2001) reconoció cinco subespecies: A. g. yucatanensis, A. g. vellerosus (= pan), A. g. geoffroyi (= frontatus), A. g. ornatus (= azuerensis y panamensis) y A. g. grisescens. Rylands et al. (2006) mantuvieron esencialmente la taxonomía de Kellogg y Goldman (1944) pero Morales-Jimenez et al. (2015) sugirieron reconsiderar la clasificación de A. geoffroyi en Mesoamérica, ya que es importante determinar si los taxones actualmente incluidos en A. geoffroyi deberían dividirse en más de una especie o subespecie reconocida. Debido a esto aún no hay un número definido de especies y subespecies para Mesoamérica. ...
... Debido a esto aún no hay un número definido de especies y subespecies para Mesoamérica. Por ejemplo, Morales-Jimenez et al. (2015) sugieren que especímenes de El Salvador deben considerarse distintos de A. g. vellerosus; los del suroeste de Nicaragua y noroeste de Costa Rica diferentes de A. g. frontatus; los de Nicaragua considerados A. g. geoffroyi podrían ser diferentes a los del suroeste de Nicaragua y el noroeste de Costa Rica; y los de México, Guatemala y Belice (vellerosus y yucatanensis) deben consolidarse en A. g. vellerosus. Además, la identidad filogenética de los individuos de Honduras, el este de Costa Rica y el centro y oeste de Panamá aún no se ha determinado. ...
... Sin embargo, queremos enfatizar que el cautiverio de este individuo se debe al tráfico ilegal de fauna silvestre. Autoridades de "El Ocotal" informan que este individuo ha permanecido en dicho lugar durante 15 años, y considerando la distribución de A. g. geoffroyi, la especie está restringida a Nicaragua (Morales-Jimenez et al., 2015). Este espécimen puede ser evidencia del tráfico ilegal de fauna silvestre entre Honduras y Nicaragua desde la década del 2000 o puede estar identificado de manera incorrecta. ...
... We obtained 30 blood samples collected from wild and captive individuals, including ten Alouatta pigra and ten Alouatta palliata wild adults sampled in Mexico and Guatemala, two Ateles fusciceps and one Cebus capucinus sampled at the Summit Zoo in Panama and seven Ateles geoffroyi yucatanensis sampled from wild individuals in Cancun, Mexico [see Cortés-Ortiz et al. (2003); Morales-Jiménez et al. (2015); Baiz et al. (2018) for details on sample collection]. Samples from wild howler monkey individuals were collected under the University of Michigan's Institutional Animal Care and Use Program protocol #09319. ...
Oxytocin is a mammalian neuropeptide hormone that mediates behaviours important to reproduction. Despite almost universal amino acid sequence conservation across most groups of mammals, several unique forms have been reported across Neotropical primates. To explore sequence diversity, we investigated the genes encoding oxytocin and its receptor across the Atelidae, which was known to contain at least three unique oxytocin sequences. Additionally, we included the genus Cebus, within the Cebidae, to further explore the ubiquity of the Pro8 variant in this family. We found a novel amino acid variant (Val3) within the Atelidae radiation, bringing the total number of oxytocin sequences within Neotropical primates to seven. Analyses of physicochemical properties revealed conservative substitutions that are likely tolerated within the selective constraints imposed by receptor binding. Furthermore, we report radical substitutions at the eighth codon and evidence for co-evolution between Pro8 and a ligand-binding region of the oxytocin receptor in the Atelidae, supporting the notion that this variant may affect binding specificity. Overall, we suggest that selective constraint on binding specificity may maintain proper oxytocin function and that the diversification of amino acid sequence is likely due to a variety of processes such as relaxed constraint, neutral mutation, positive selection and coevolution.
... Morphological and genetic variations of these primates are found along their range, with 5 recognized subspecies of Al. palliata (Alouatta palliata mexicana; Alouatta palliata palliata; Alouatta palliata aequatorialis; Alouatta palliata coibensis; Alouatta palliata trabeata) and allegedly 7 subspecies of At. geoffroyi (Ateles geoffroyi vellerosus; Ateles geoffroyi yucatanensis; Ateles geoffroyi geoffroyi; Ateles geoffroyi frontatus; Ateles geoffroyi ornatus; Ateles geoffroyi grisescens; Ateles geoffroyi azuerensis) (Rylands et al., 2006); all of them inhabiting different biogeographic areas across Mexico and Central America (Ford, 2006) (distribution shown in Supplementary Material S1). A recent assessment of the phylogenetic relationships among Mesoamerican spider monkeys showed that the recognized subspecies of At. geoffroyi were not monophyletic, suggesting the need for a taxonomic revision of this group (Morales-Jimenez et al., 2015). ...
... Molecular phylogenetic analyses of Central American spider monkeys through a multilocus approach of mtDNA have shown a lack of distinction between At. g. vellerosus and At. g. yucatanensis, and thus they should be considered as the same subspecies, At. g. vellerosus (Morales-Jimenez et al., 2015). The resulting genetic patterns of the parasites unveiled in this study constitute additional evidence supporting this proposal. ...
... The time at which At. g. vellerosus and At. g. frontatus diverged from the common ancestor has been estimated ∼1.5 Ma (Morales-Jimenez et al., 2015), and this might be considered a relatively recent date for the accumulation of the observed genetic differences in these pinworm populations. Moreover, specimens of T. atelis have been previously obtained and sequenced from different primate species of the family Atelidae, all from captive populations in Japan, including the spider monkey, At. geoffroyi (unknown subspecies), the yellow-bellied spider monkey, At. belzebuth, and the brown woolly monkey, Lagothrix lagotricha (Hasegawa et al., 2012) (Fig. 2). ...
Patterns of genetic variation among populations can reveal the evolutionary history of species. Pinworm parasites are highly host specific and form strong co-evolutionary associations with their primate hosts. Here, we describe the genetic variation observed in four Trypanoxyuris species infecting different howler and spider monkey subspecies in Central America to determine if historical dispersal processes and speciation in the host could explain the genetic patterns observed in the parasites. Mitochondrial ( cox1 ) and ribosomal ( 28S ) DNA were analysed to assess genetic divergence and phylogenetic history of these parasites. Sequences of the 28S gene were identical within pinworms species regardless of host subspecies. However, phylogenetic analyses, haplotype relationships and genetic divergence with cox1 showed differentiation between pinworm populations according to host subspecies in three of the four Trypanoxyuris species analysed. Haplotype separation between host subspecies was not observed in Trypanoxyuris minutus, nor in Trypanoxyuris atelis from Ateles geoffoyi vellerosus and Ateles geoffoyi yucatanensis. Levels of genetic diversity and divergence in these parasites relate with such estimates reported for their hosts. This study shows how genetic patterns uncovered in parasitic organisms can reflect the host phylogenetic and biogeographic histories.
... Boubli et al. (2012) indicate well-supported monophyly in C. imitator (unlike in C. capucinus). Recent molecular analyses have also upheld the monotypic status of Ateles geoffroyi (despite the need for subspecific revision; Morales-Jimenez et al. 2015), Alouatta palliata, and Alouatta pigra (Cortés-Ortiz et al. 2003). Thus, we contend that the taxa included are appropriate for the analysis. ...
The high degree of dietary breadth and flexibility in capuchins (Cebus and Sapajus), coupled with their advanced cognitive abilities, is well documented. Owing to these characteristics, capuchins may be considered highly adaptable generalists, capable of occupying a wide range of habitats. The Panamanian white-throated capuchin (Cebus (capucinus) imitator) coexists with several other primate genera in Mesoamerica. Some taxa, such as the mantled howler monkey (Alouatta palliata) and Geoffroy’s spider monkey (Ateles geoffroyi), have broader geographic ranges than C. imitator. This may be due to historical biogeography (e.g. earlier colonization of the region by Ateles and Alouatta) or, alternatively, because some habitats may be less suitable for capuchins. We investigated the latter hypothesis using ecological niche models (ENMs) to predict range extent based on climate and elevation, as well as niche breadth. Our results suggest a narrow climate niche relative to the more wide-ranging Ateles geoffroyi, as well as Alouatta spp. Precipitation in the coldest quarter and temperature seasonality were the two most important climate variables for determining C. imitator habitat suitability. These findings may have implications for capuchins’ ability to persist through environmental changes (climate change and forest degradation, and loss) and warrant consideration in assessing their extinction risk.
... However, the taxonomic status of both species was reviewed by and Morales-Jiménez et al. (2015), who consider that both are valid and different species. Preliminary genetic analyses of samples from the south of Colombia and the north of Ecuador show two different monophyletic clades (Morales-Jimenez et al. 2015). Two subspecies are recognized: ...
... However, the taxonomic status of both species was reviewed by and Morales-Jiménez et al. (2015), who consider that both are valid and different species. Preliminary genetic analyses of samples from the south of Colombia and the north of Ecuador show two different monophyletic clades (Morales-Jimenez et al. 2015). Two subspecies are recognized: ...
... However, the taxonomic status of both species was reviewed by and Morales-Jiménez et al. (2015), who consider that both are valid and different species. Preliminary genetic analyses of samples from the south of Colombia and the north of Ecuador show two different monophyletic clades (Morales-Jimenez et al. 2015). Two subspecies are recognized: ...
... However, the taxonomic status of both species was reviewed by and Morales-Jiménez et al. (2015), who consider that both are valid and different species. Preliminary genetic analyses of samples from the south of Colombia and the north of Ecuador show two different monophyletic clades (Morales-Jimenez et al. 2015). Two subspecies are recognized: ...
