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.
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.
Electronic supplementary material
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The normal sleep patterns of the spider monkey (Ateles geoffroyi) have not been described yet. The objective of this study was to characterize the electrophysiological patterns, sleeping postures, and sleep-wake cycle in semi-restricted spider monkeys. Continuous 24-hr polysomnographic (PSG) recordings, involving simultaneous recording of non-invasive electroencephalographic (EEG), electro-oculographic (EOG), and electromyographic (EMG) activities, were carried out in captive monkeys living in outdoor rainforest enclosures. Electrode placement was done according to the human international 10-20 system. Specific behaviors displayed by monkeys during the sleep-wake cycles were correlated with the PSG recordings. The nycthemeral distribution of the sleep-wake cycle was also calculated. The results show that electrophysiological N-REM sleep patterns in spider monkeys are similar to those observed in other primates, including human beings. Furthermore, a vertical semi-fetal posture was observed during N-REM and REM sleep phases. The amount of nocturnal sleep was significantly higher than that of the diurnal period, showing that the spider monkey is a diurnal primate. An outstanding finding was the absence of muscular atonia during the spider monkey's REM sleep, which suggests that arboreal primates have developed a neuromuscular mechanism specialized for sleeping in a vertical posture.
We describe for the first time the karyotype of the black howler monkey, Alouatta pigra. Conventional staining, G- and C-banding, and fluorescence in situ hybridization (FISH) with a peptide nucleic acid (PNA) pantelomeric probe were performed. Eight free ranging adult individuals, four males and four females, within the natural distribution of the species presented a diploid karyotype with 2n = 58. Mitotic analyses showed an autosomal complement composed of 6 submetacentric, 3 metacentric, and 19 acrocentric chromosome pairs for females, and 6 submetacentric, 3 metacentric, and 18 acrocentric pairs for males. Meiotic analyses in males revealed 27 autosomal bivalents and a quadrivalent composed of a submetacentric X1 and acrocentric X2, Y1, and Y2. The G-banded karyotype allowed us to identify pair #17 as the autosomal pair involved in the rearrangement and the morphology of the quadrivalent components. C-banding technique in metaphase I corroborated the structure of the quadrivalent showing four C+ centromeres. FISH analysis showed telomeric signals at the terminal regions of all chromosomes. No interstitial signals were detected. DNA sequence data were in accordance with those previously published for this species.
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