Liliana Cortés-Ortiz

Hybridization in Large-Bodied New World Primates

Well-documented cases of natural hybridization among primates are not common. In New World primates, natural hybridization has been reported only for small-bodied species, but no genotypic data have ever been gathered that confirm these reports. Here we present genetic evidence of hybridization of two large-bodied species of neotropical primates that diverged ∼3 MYA. We used species-diagnostic mitochondrial and microsatellite loci and the Y chromosome Sry gene to determine the hybrid status of 36 individuals collected from an area of sympatry in Tabasco, Mexico. Thirteen individuals were hybrids. We show that hybridization and subsequent backcrosses are directionally biased and that the only likely cross between parental species produces fertile hybrid females, but fails to produce viable or fertile males. This system can be used as a model to study gene interchange between primate species that have not achieved complete reproductive isolation.

Impact of Intrasexual Selection on Sexual Dimorphism and Testes Size in the Mexican Howler Monkeys Alouatta palliata and A. pigra

One of the goals of physical anthropology and primatology is to understand how primate social systems influence the evolution of sexually selected traits. Howler monkeys provide a good model for studying sexual selection due to differences in social systems between related species. Here, we examine data from the sister howler monkey species Alouatta palliata and A. pigra inhabiting southeastern Mexico and northern Guatemala. We use a resampling approach to analyze differences in sexual dimorphism of body and canine size. In addition, we compare testes size as a way of gauging the intensity of sperm competition in both species. Morphometric data were collected from wild-caught individuals, including body mass and length, and dental data were obtained from casts from wild individuals and from museum specimens. Although A. pigra individuals are larger than their A. palliata counterparts, we find that both species exhibit similar levels of sexual dimorphism for all of the variables considered. Testicular volume results indicate that A. palliata male testes are on average twice as large as those of A. pigra males, suggesting more intense sperm competition in the former species. Our study shows that A. pigra is not highly sexually dimorphic as was once thought, and testes size differences suggest the need for a clearer understanding of howler monkey social systems.

The Taxonomy of Howler Monkeys: Integrating Old and New Knowledge from Morphological and Genetic Studies

The taxonomic history of the howler monkeys, genus Alouatta, has been long, complex, and filled with omissions and mistakes. This has created confusion over the validity of different taxa. Here we review the taxonomic history of the genus and evaluate the validity of the different taxa based on current knowledge generated through morphological and genetic studies. We recognize nine species of howlers (A. palliata, A. pigra, A. seniculus, A. arctoidea, A. sara, A. macconnelli, A. guariba, A. belzebul, A. caraya) and three more taxa that we tentatively consider full species (A. nigerrima, A. ululata, A. discolor), but for which genetic and/or morphological studies are required to confirm this status. We recognize five subspecies in A. palliata (A. p. mexicana, A. p. palliata, A. p. coibensis, A. p. trabeata, and A. p. aequatorialis), three in A. seniculus, (A. s. seniculus, A. s. juara, and A. s. puruensis), two in A. guariba (A. g. guariba and A. g. clamitans), and acknowledge the possibility that A. pigra may have two subspecies (A. p. pigra and A. p. luctuosa). Most species and subspecies require field studies to determine their actual distribution ranges. Furthermore, a combination of morphological and genetic analyses is needed to confirm the validity of several taxa. Given the broad presence of howler monkeys in the Neotropics, these studies would require the collaboration of a multidisciplinary network of researchers across the range of distribution of the genus.

Howler monkeys : behavior, ecology, and conservation

PART 1. INTRODUCTION.- Chapter 1. Why is it Important to Continue Studying the Behavioral Ecology and Conservation Management of Howler Monkeys?.- PART 2: BEHAVIORAL ECOLOGY.- Chapter 2. Diets of Howler Monkeys.- Chapter 3. Insights into Reproductive Strategies and Sexual Selection in Howler Monkeys.- Chapter 4. Evidence of Alternative Dietary Syndromes and Nutritional Goals in the Genus Alouatta.- Chapter 5. Seed Dispersal by Howler Monkeys: Current Knowledge, Conservation Implications, and Future Directions.- Chapter 6. Interactions of Howler Monkeys with Other Vertebrates: A Review.- Chapter 7. Solving the Collective Action Problem During Intergroup Encounters: The Case of Black and Gold Howler Monkeys.- Chapter 8. Howler Monkey Positional Behavior.- Chapter 9. Ranging Behavior and Spatial Cognition of Howler Monkeys.- PART 3: CONSERVATION AND MANAGEMENT.- Chapter 10. The Ethnoprimatology of Howler Monkeys (Alouatta spp.): From Past to Present.- Chapter 11. Anthropogenic Habitat Modification, Tourist Interactions and Crop-Raiding in Howler Monkeys.- Chapter 12. Health and Welfare of Howler Monkeys in Captivity.- Chapter 13. Fruit as a Key Factor in Howler Monkey Population Density: Conservation Implications. Chapter 14. Conservation of Alouatta: Social and Economic Drivers of Habitat Loss, Information Vacuum and Mitigating Population Declines.- PART 4: CONCLUSION.- Chapter 15. New Challenges in the Study of Howler Monkey Behavioral Ecology and Conservation: Where we are and where we need to go?.

Howler Monkeys: Adaptive radiation, systematics, and morphology

Part 1. Introduction.- Chapter 1. Why is it Important to Continue Studying the Anatomy, Physiology, Sensory Ecology, and Evolution of Howler Monkeys?.- Part 2. Taxonomy, Genetics, Morphology and Evolution.- Chapter 2. Fossil Alouattines and the Origins of Alouatta: Craniodental Diversity and Interrelationships.- Chapter 3. The Taxonomy of Howler Monkeys: Integrating Old and New Knowledge from Morphological and Genetic Studies.- Chapter 4. Cytogenetics of Howler Monkeys.- Chapter 5. Hybridization in Howler Monkeys: Current Understanding and Future Directions.- Chapter 6. Morphology of Howler Monkeys: A Review and Quantitative Analyses.- Part 3. Physiology.- Chapter 7. Hematology and Serum Biochemistry in Wild Howler Monkeys.- Chapter 8. Endocrinology of Howler Monkeys: Review and Directions for Future Research.- Chapter 9. The Howler Monkey as a Model for Exploring Host-Gut Microbiota Interactions in Primates.- Chapter 10. Ecological Determinants of Parasitism in Howler Monkeys.- Part 4. Ontogeny and Sensory Ecology.- Chapter 11. An Ontogenetic Framework for Alouatta: Infant Development and Evaluating.- Chapter 12.The Sensory Systems of Alouatta: Evolution with an Eye to Ecology.- Chapter 13. Production of Loud and Quiet Calls in Howler Monkeys.- Chapter 14. Function of Loud Calls in Howler Monkeys.- Part 5. Conclusions.- Chapter 15. New Challenges in the Study of Howler Monkey Anatomy, Physiology, Sensory Ecology, and Evolution: Where we are and where we need to go?.

Morphological variation of genetically confirmed Alouatta Pigra × A. palliata hybrids from a natural hybrid zone in Tabasco, Mexico

While hybridization has been reported for a large number of primate taxa, there is a general lack of data on hybrid morphology for wild individuals with known genetic ancestry. A confirmed hybrid zone for the closely related Neotropical primates Alouatta palliata and A. pigra has provided a unique opportunity to study primate hybrid morphological variation. Here we used molecular evidence based on mitochondrial, Y-chromosome, and autosomal data to assess hybrid ancestry. We conducted univariate and multivariate statistical comparisons of morphometric data collected from individuals both outside and within the hybrid zone in Tabasco, Mexico. Our results show that of all the hybrids detected (N = 128), only 12% of them were approximately genetically intermediate, and none of them were first generation hybrids. Univariate pairwise comparisons among parental individuals, multigenerational backcrossed hybrids, and intermediate hybrids showed that overall, multigenerational backcrossed hybrids resemble the parental species with which they share most of their alleles. Conversely, intermediates were highly variable. Similarly, principal component analysis depicts an overlap between the parental species and their backcrosses when considering overall morphological differences. Finally, discriminant function analysis of the morphological variables was overall unreliable for classifying individuals into their assigned genotypic classes. Taken together, our results suggest that primate natural hybridization studies should incorporate molecular methods for determining ancestry, because morphology may not always be a reliable indicator of hybrid status. Hybrid zones could comprise a large number of multigenerational backcrossed hybrids that are indistinguishable from the parental species. The implications for studying hybridization in the primate fossil record are discussed.

Isolation and characterization of microsatellite loci for the study of mexican howler monkeys, their natural hybrids, and other neotropical primates

Here we present 26 microsatellite markers that can be used for the study of Alouatta palliata, A. pigra and their natural hybrids. Sixteen of these markers were isolated for other species of primates and some of these have been previously tested in A. palliata and/or A. pigra individuals. The other 10 loci were isolated from either A. palliata or A. pigra through enriched genomic libraries. Sixteen loci were polymorphic for A. palliata and 24 for A. pigra. To explore the potential use of these primers in other primate species, we attempted cross-amplification in six other Neotropical primate taxa. Twenty-five loci amplified for at least one other species of Neotropical primate.

Molecular Phylogenetics of the Callitrichidae with an Emphasis on the Marmosets and Callimico

In the last two decades analyses of DNA sequence data have significantly increased our understanding of the phylogenetic relationships among callitrichid primates. The current taxonomic synthesis includes seven genera within the family Callitrichidae: Saguinus, Leontopithecus, Callimico, Mico, Cebuella, Callibella and Callithrix. The relationships among genera are relatively well defined by molecular data and can be described as follows: (Saguinus (Leontopithecus (Callimico (Callithrix (Callibella (Cebuella/Mico)))))). Nonetheless, relationships among Leontopithecus, Callimico, and Saguinus are less clear and show different patterns depending on the data utilized to infer these relationships; this could reflect the relatively rapid divergence of these lineages. The sister relationship of Callimico to the marmosets (Callithrix, Callibella, Cebuella, and Mico) is highly supported by molecular and cytogenetic studies. Within this clade (Callimico/marmosets), only a few studies have focused on determining relationships at the intrageneric level, with only two genera analyzed to date. These studies have produced uncertain results concerning the taxonomic distinctiveness of the putative species and their phylogenetic relationships. In this chapter I review, synthesize, and analyze the molecular evidence that has been used to elucidate the taxonomy within the Callitrichidae.

Hybridization in Howler Monkeys: Current Understanding and Future Directions

Hybridization, or the process by which individuals from genetically distinct populations (e.g., species, subspecies) mate and produce at least some offspring, is of great relevance to understanding the basis of reproductive isolation and, in some cases, the origins of biodiversity. Natural hybridization among primates has been well documented for a few taxa, but just recently the genetic confirmation of hybridization for a number of taxa has produced new awareness of the prevalence of this phenomenon within the order and its importance in primate evolution. The study of hybridization of Alouatta pigra and A. palliata in Mexico was among the first to genetically confirm the current occurrence of hybridization in primates. Following this study, other reports of hybridization have shown that this phenomenon is more widespread among primates than previously anticipated. Within the genus Alouatta, there have been reports on the presence of hybridization between A. caraya and A. guariba in a number of contact zones in Brazil and Argentina, and various studies are currently ongoing in some of these sites to understand the extent and patterns of hybridization between these species. In this chapter, we evaluate the extent of hybridization in the genus Alouatta, revise the current knowledge of the genetic and morphological aspects of these hybrid systems, and identify future directions in the study of hybridization within this genus, to understand the possible implications of the hybridization process in the evolutionary history of howler monkeys.

Effect of ancestry on behavioral variation in two species of howler monkeys (Alouatta pigra and A. palliata) and their hybrids

Social differences between primate species may result from both flexible responses to current conditions or fixed differences across taxa, yet we know little about the relative importance of these factors. Here, we take advantage of a naturally occurring hybrid zone in Tabasco, Mexico to characterize the variation in social structure among two endangered howler monkey species, Alouatta pigra and A. palliata, and their hybrids. Work in pure populations has suggested that A. pigra females maintain closer proximity, exhibit higher rates of affiliation, and lower rates of agonism than A. palliata females, but we do not know what accounts for this difference. Using identical data collection and analysis methods across three populations, we first seek to confirm previously reported interspecific differences in social structure across all sexes. We next examine: (1) how female social relationships changed with ancestry (by comparing pure and hybrid individuals); (2) how female social relationships changed with group size (A. pigra have smaller groups than A. palliata); and (3) whether female social relationships differed between two taxonomic groups within a single forest fragment (thus controlling for ecological variation). We confirmed previously described species differences, including closer proximity among females than among males in all populations. We also found that smaller groups maintained closer proximity. However, even after accounting for variation in group size, A. pigra females had closer proximity and more affiliation than A. palliata females. Furthermore, differences between pigra‐like and palliata‐like hybrids paralleled differences between pure populations and persisted even after controlling for ecological variation. Together, our results suggest that flexibility cannot account for all of the social differences between A. pigra and A. palliata and indicate an important genetic component in primate social behavior. Am. J. Primatol. 76:855–867, 2014.