Reduced Introgression of Sex Chromosome Markers in the Mexican Howler Monkey (Alouatta palliata × A. pigra) Hybrid Zone

International Journal of Primatology, Sep 2018

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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Reduced Introgression of Sex Chromosome Markers in the Mexican Howler Monkey (Alouatta palliata × A. pigra) Hybrid Zone

International Journal of Primatology pp 1–18 | Cite as Reduced Introgression of Sex Chromosome Markers in the Mexican Howler Monkey (Alouatta palliata × A. pigra) Hybrid Zone AuthorsAuthors and affiliations Liliana Cortés-OrtizMarcella D. NidifferJavier Hermida-LagunesFrancisco García-OrduñaAriadna Rangel-NegrínDawn M. KitchenThore J. BergmanPedro A. D. DiasDomingo Canales-Espinosa Open Access Article First Online: 14 September 2018 Received: 13 November 2017 Accepted: 07 June 2018 2 Shares 325 Downloads Abstract 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. KeywordsHaldane’s rule Hybridization Large X-effect Reproductive isolation  Liliana Cortés-Ortiz and Marcella D. Nidiffer have contributed equally to this article. Handling Editor: Joanna M. Setchell. Electronic supplementary material The online version of this article ( https://doi.org/10.1007/s10764-018-0056-4) contains supplementary material, which is available to authorized users. Introduction Hybridization is the crossing of genetically distinct taxa that produces some viable offspring (Arnold 1997; Mallet 2005). In nature, this occurs in areas where two genetically divergent lineages meet and interbreed, creating regions referred to as hybrid zones (Barton and Hewitt 1985; Harrison 1990). In a hybrid zone, hybridization and recombination over many generations shuffle divergent genomes, and selection acts on the recombined genotypes, allowing the mixture of some genomic regions from the two parental lineages while preventing other regions from intermixing. This process produces individuals with distinct levels of admixture across their genome (Barton and Hewitt 1985; Harrison 1990; Hewitt 1988; Payseur 2010) and implies that genomes of hybridizing species are semipermeable to introgression (the movement of alleles from one gene pool into another through admixture; Parchman et al. 2013), with permeability depending on the characteristics of different genomic regions (Larson et al. 2013). It is expected that alleles that are advantageous in both parental genomes should easily spread through the hybrid zone, and neutral alleles should be freely exchanged between species. However, genomic regions that contribute to local adaptation or reproductive isolation should have restricted levels of introgression (Carneiro et al. 2013; Larson et al. 2013; Payseur 2010; Poelstra et al. 2014) and present relatively steep clines when plotted across a gradient of hybridization, either across a geographic transect or as a function of a hybrid index (i.e., the proportion of ancestry from each parental species) for admixed individuals (see Larson et al. 2013). Two features are broadly documented when hybridization occurs among divergent lineages. First, individuals of the heterogametic sex (males in mammals) are more likely to be sterile or inviable than individuals of the homogamet (...truncated)


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Liliana Cortés-Ortiz, Marcella D. Nidiffer, Javier Hermida-Lagunes, Francisco García-Orduña, Ariadna Rangel-Negrín, Dawn M. Kitchen, Thore J. Bergman, Pedro A. D. Dias, Domingo Canales-Espinosa. Reduced Introgression of Sex Chromosome Markers in the Mexican Howler Monkey (Alouatta palliata × A. pigra) Hybrid Zone, International Journal of Primatology, 2018, pp. 1-18, DOI: 10.1007/s10764-018-0056-4