Population genetics and evolutionary history of the black howler monkey Alouatta pigra and hybrid populations in Mexico

Ella Vázquez-Domínguez^1*Brenda Solórzano-García²Mariana Reyes-Vázquez¹Diego Zubillaga-Martín¹

• ¹Institute of Ecology, National Autonomous University of Mexico, Mexico City, Mexico
• ²ENES-Mérida, Universidad Nacional Autónoma de México, Mérida, Yucatán, Mexico

Genetic diversity is of prime importance for biological diversity and for the long-term conservation and survival of species and populations. The conservation of hybrid individuals originating from natural hybridization is still controversial; nearly every hybrid system is different and general conservation rules are not effective. The black howler monkey (Alouatta pigra) is and endangered primate endemic to the Yucatán peninsula. It hybridizes with the mantled howler, Alouatta palliata, in a narrow contact zone located in southern Mexico. We evaluated the genetic diversity and structure patterns in natural populations of A. pigra across its distribution range in Mexico (16 localities), including the hybrid populations, and estimated the overall time of divergence of the hybrid individuals. We successfully genotyped 12 microsatellite loci and obtained a 587 bp cytochrome-b fragment alignment for 222 and 107 individuals, respectively. We identified 33 hybrids, three A. palliata and 186 non-admixed A. pigra. Our results showed the highest diversification for A. pigra in Mexico occurring at ~1.4 My, while identifying a more recent diversification event including A. palliata and hybrids (~0.56 My), supporting different diversification events along these primates’ evolutionary history. Divergence of hybrid individuals is not a contemporary process in the evolutionary history of these sister species, suggesting they came into contact at the zone of sympatry at least some ~0.8 My ago. Hybrids exhibited higher mitochondrial diversity in comparison with non-admixed individuals; notably, hybrids with A. pigra mitochondria exhibited both higher diversity and number of unique haplotypes than those with A. palliata mitochondria. Comparatively, hybrid nuclear genetic diversity was higher compared with A. palliata but not with A. pigra. Regarding the A. pigra populations, we found moderate diversity values, being highest in the most conserved and continuous habitat. We also found significant genetic differentiation (five genetic clusters) and limited gene flow between them, and potential inbreeding signals, which render A. pigra prone to drift effects and increased extinction risk. Our study provides novel information regarding the historical and contemporary genetic patterns of black howler monkey and hybrid populations in Mexico, key for developing strategies for conserving and ensuring the survival of viable primate populations.