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 The online version of this article (10.1007/s10764-018-0056-4) contains supplementary material, which is available to authorized users.
The degree of genetic relatedness among group members is influenced by dispersal, group formation and composition, mating systems, and other socioecological factors. Making inferences about differences between species in their socio-genetic structure is difficult because studies rarely compare multiple species. In this study, we use multilocus microsatellite genotype data to analyze intragroup genetic relatedness in two howler monkey species (Alouatta palliata and A. pigra). We test the prediction that their patterns of intragroup genetic relatedness will be distinct based on expectations derived from their distinct social systems. Alouatta palliata is expected to have low levels of intragroup relatedness, given that both males and females are reported to disperse from their natal groups, and to join groups with no close kin. Levels of relatedness among A. pigra group members are expected to be variable according to the history of group formation, with new groups formed by unrelated individuals and well-established groups having close kin due to female nepotism and sometimes by takeovers by coalitions of related males. Our results indicate that in both species, most groups contain closely related same-sex and/or inter-sex dyads. This suggests that philopatry in A. palliata may be more common than reported or that individuals are using alternative strategies to reside with close kin. We found greater variation among groups in female-female relatedness in A. palliata than in A. pigra, implying that these species have distinct socio-genetic structures. Further studies including both long-term observational and genetic data are necessary to understand the mechanisms that determine the degree of variation in intragroup genetic relatedness within and among populations for both species. Ecological and demographic data are also necessary to determine the importance of other factors, especially habitat loss and fragmentation, in determining the degree of relatedness in howler monkey groups.
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