Howler monkey genetics study shows similarities to archaic gene flow between humans and Neanderthals
Marcella Baiz (U-M EEB Ph.D. 2019) published part of her dissertation investigating a primate hybrid zone to try to understand the genetic basis of reproductive isolation of two closely related species: the mantled howler monkey and the Mexican black howler monkey. A hybrid zone is a place where two species coexist and occasionally interbreed in a process called hybridization.
The paper, “X-Linked Signature of Reproductive Isolation in Humans is Mirrored in a Howler Monkey Hybrid Zone,” published July 29, 2020 in the Journal of Heredity, was selected as the cover story and an Editor’s Choice. Baiz, a recent alumnus of the University of Michigan Department of Ecology and Evolutionary Biology is a postdoctoral researcher at Penn State University. Along with first author Baiz, coauthors were her former advisors, EEB Professors Liliana Cortés Ortiz and Priscilla Tucker, and Professor Jacob Mueller, Department of Human Genetics.
“We used whole genome sequencing to identify X-chromosome sequence in our study species, and showed that the X chromosome exhibits reduced gene flow across the species boundary compared to the autosomes (any non-sex chromosomes), suggesting the X chromosome plays a large role in speciation (the formation of a new and distinct species in the course of evolution). We also identified similarities in the pattern we observed in howler monkeys to the pattern observed for archaic gene flow between humans and Neanderthals and Denisovans.”
The mantled howler monkey (Alouatta palliata) and the Mexican black howler monkey (Alouatta pigra) form a stable hybrid zone in Tabasco, Mexico, a system Cortés Ortiz has studied for 20 years. “During hybridization, the genomes of two species are combined, but not all combinations produce individuals equally capable of surviving or producing offspring. Hybrid zones serve as natural experiments where individuals carrying different genomic combinations of the two species are produced. By analyzing the genomes of these individuals we can detect the parts of the genome of one species that do not work well when combined with parts of the genome from the other species,” Cortés Ortiz explained.
They previously used a small set of genetic markers to characterize the hybrid zone and found that early generation hybrids are rare, suggesting reproductive isolation is strong. They also observed that the few markers representing the X chromosome showed consistently less introgression (gene flow from one species to another) than markers on autosomes, suggesting the X chromosome may have been especially important in forming species barriers.
“In this study, we expanded our sequencing across the genome with the goal to identify genomic regions that exhibit reduced introgression,” Baiz said. “We wanted to explicitly test whether compared to autosomes, the X indeed has reduced introgression, and whether there were any similarities in introgression patterns between howler monkeys and humans.”
Their analysis of over 10,000 SNPs supported the importance of the X chromosome — they again found that compared to markers on the autosomes, markers on the X chromosome had reduced introgression in the hybrid zone. (SNPs, single nucleotide polymorphisms, pronounced “snips,” are single-letter differences in DNA sequences, and the specific combinations of multiple SNPs are unique for each individual.)
“Interestingly, one of the X-linked markers with a strong signal of reduced introgression overlaps a region in the human genome that was previously identified as having reduced introgression from Neanderthals and Denisovans,” Baiz added.
Their results imply that genes important for reproductive isolation may disproportionately occur on the X chromosome, which has also been observed in other model systems like mice and Drosophila.
“A possible explanation for this is that in males (who only have one copy of the X chromosome), recessive deleterious alleles on the sex chromosomes are exposed to selection,” said Baiz. “Our results also imply that since we observed in howler monkeys a similar signature to the human system that the genetic basis of reproductive isolation may be shared across primate lineages.”
“One of the next steps in our research is to generate more fine-grained genomic data that allow us to pinpoint specific genes or genomic regions that may be responsible for the observed levels of reproductive isolation in our howler monkey hybrid system,” said Cortés Ortiz.
The work was supported by the National Science Foundation, the American Society of Mammalogists, the U-M Department of Ecology and Evolutionary Biology, the U-M Genetics Training Program and by the National Institutes of Health.
Read more in a Michigan News press release on a previous study