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

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

Liliana Cortés-Ortiz et al. Int J Primatol. 2019.

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.

Keywords: Haldane’s rule; Hybridization; Large X-effect; Reproductive isolation.

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Figures

Fig. 1

Fig. 1

Distribution of Alouatta palliata (light gray) and A. pigra (dark gray) (based on IUCN 2008) showing location of sampled groups (circles) within and outside the hybrid zone. The inset is a close-up of groups in the hybrid zone. N = number of sampled individuals. Primate drawings by Stephen Nash.

Fig. 2

Fig. 2

Genotypes of individuals in the Alouatta palliata × A. pigra hybrid zone in Tabasco, Mexico. Individuals are in columns arranged by their hybrid index as calculated using the codominant markers (0 = A. palliata, 1 = A. pigra) and markers are in rows. Black indicates homozygous A. pigra genotype, light gray is homozygous A. palliata genotype, dark gray is heterozygous genotype, and white is missing data. a Autosomal microsatellite genotypes (N = 254). b Mitochondrial DNA (N = 251). c Y-linked marker (N = 91). d X-linked markers (N = 85, i.e., reduced dataset).

Fig. 3

Fig. 3

a Distribution of admixed genotypes in the Alouatta palliata × A. pigra hybrid zone in Tabasco, Mexico (N = 254). b Hybrid index plotted against interspecific heterozygosity for each individual in the hybrid zone. Hybrid index is represented as the proportion of alleles inherited from A. pigra (i.e., 0 = A. palliata and 1 = A. pigra) and interspecific heterozygosity is the proportion of loci that are heterozygous with an allele from each parental species. Individuals are coded by sex, where females (F) are represented as black dots and males (M) are gray triangles.

Fig. 4

Fig. 4

Geographic distribution of admixed and nonadmixed individuals in the Alouatta palliata (Apa) × A. pigra (Api) hybrid zone in Tabasco, Mexico (N = 254). The proportion of genotypes are represented for each sampling site, where Apa in brown is nonadmixed A. palliata, Apa BC in yellow represents backcrossed A. palliata hybrids, Api in black is nonadmixed A. pigra, Api BC in gray represents backcrossed A. pigra, and intermediate hybrids (Int) are in purple. The size of the pie is proportional to the number of individuals sampled at each site. The figure covers approximately the same area labeled as Hybrid Zone in Fig. 1. The zoomed-in area allows a clearer observation of the distribution of genotypes in each sampled group.

Fig. 5

Fig. 5

Genomic clines for 24 microsatellite (23 autosomal and one X-linked) markers and two X-linked genes, plotted as the probability of having a homozygous Alouatta palliata (Apa/Apa) genotype as a function of hybrid index, for individuals in the A. palliata × A. pigra hybrid zone in Tabasco, Mexico. Each line represents a cline for a single locus and the shaded gray area is the neutral expectation. Different line styles identify loci showing cline shape patterns consistent with particular types selection (thin solid line = neutral introgression; dashed line = directional selection; thick solid line = underdominance; dotted line = overdominance).

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