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What does the history of human hybridization share with some of our closest relatives?

 

About the author: Marcella is an NSF postdoctoral fellow currently working in David Toews’ lab on the genetics of speciation and hybridization. Her current projects involve evolutionary genomics of adaptation, species divergence, and gut microbiome structure in wood warblers. Marcella received her PhD and MS in Ecology and Evolutionary Biology at the University of Michigan. Find Marcella on Twitter @marcella_baiz.

 

 

 

When different species hybridize, why don’t they collapse back into a single population? Which genomic regions prevent this from happening, and are certain regions more prone to be involved than others? In our recent study (Baiz et al. 2020), we investigated these questions by looking for similarities between howler monkeys and humans.

Hybridization occurs when reproductive barriers are incomplete and divergent taxa interbreed, producing admixed offspring. It is a natural process thought to be rare in some taxonomic groups, but more frequent in others. In certain primate taxa, for example, hybridization is estimated to occur in up to 40% of the species (Tung & Barreiro 2017).

Hybrid genomes can be thought of as porous, allowing adaptive and neutral alleles to pass from one species to another after many generations of backcrossing (i.e., via introgression). However, introgression of alleles that are incompatible or deleterious on the genetic background of the other species is blocked. This occurs at particular regions of the genome that are resistant to introgression, generally referred to as “barrier loci”.

Figure 1. A male Alouatta pigra in Tabasco, Mexico. Photograph by Carolina Carvajal.

This process leaves a signature in the genomes of hybridizing species. Until ~40 thousand years ago our species co-existed with closely-related hominin lineages, like Neanderthals and Denisovans, and genomic and fossil evidence point to multiple waves of hybridization with humans. In contemporary human genomes, we see regions enriched for alleles from these extinct hominins, possibly because they conferred a selective advantage in our ancestors. We also see regions—predominately near genes expressed in the testis, and on the X chromosome—depleted of this ancestry (i.e., “deserts”) (Sankararaman et al. 2016). From these signatures, we infer that hominin hybrids were less fit than non-admixed individuals, hybrid males may have suffered from infertility, and the X chromosome may have been especially important in species barriers.

Our recent study identified candidate barrier loci in howler monkey hybrids and tested whether they shared introgression deserts with humans. This project was part of my dissertation, which investigated gene introgression in the hybrid zone between mantled howler monkeys (Alouatta palliata) and the Mexican black howler monkey (A. pigra), a system that my former advisor, L. Cortés-Ortiz has developed over the past twenty years. We used whole genome sequencing on a subset of individuals to identify X chromosome sequence, and then used reduced-representation sequencing of a wider set of individuals to test patterns of introgression across the genome.

We found reduced introgression for X chromosome markers compared to autosomal markers, and interestingly one marker on the X chromosome with a particularly strong signal also occurred in the middle of one of the human deserts. This human desert is one of the few large genomic regions resistant to introgression from both Neanderthals and Denisovans (Sankararaman et al. 2016), and the fact that we found a similar signal in howler monkeys suggests that this particular region may contain sequence important for species barriers in both primate lineages.

A shared genomic architecture of X chromosomal reproductive isolation in howler monkeys and humans is intriguing on several fronts. Previous studies suggest barrier traits have a complex genetic basis (e.g., Larson et al. 2018). But if some of the same loci are recruited in different systems, it implies that certain genomic regions are more prone than others to underlie speciation. Given that a common barrier between animal species is hybrid male sterility (or female sterility in species with ZW sex chromosomes), genes in the spermatogenesis pathway are plausible suspects. Such a picture of reproductive isolation would parallel findings from genomic studies of some adaptive traits, like coloration, which have found repeated evolution in the same gene regions (Funk & Taylor 2019). Finally, although our study found support for a shared signature of reproductive isolation in humans and howler monkeys, there is evidence for substantial gene flow of X chromosomal regions in macaques (Evans et al. 2017) and guenons (Tosi & Hirai 2017). Current evidence is not sufficient to demonstrate whether specific barrier loci are shared across primates, and genomic studies of multiple primate hybrid zone systems could help to test this hypothesis.

Understanding the genetic basis of species barriers in howler monkeys, including potential parallels in humans, will require linking candidate barrier loci to specific phenotypes and isolating mechanisms. Our work on the Alouattahybrid zone is following up by asking how ecological and behavioral differences between species shape their hybridization, and what are the selective forces acting on barrier loci?

References

Baiz, M. D., Tucker, P. K., Mueller, J. L., & Cortés-Ortiz, L. (2020). X-linked signature of reproductive isolation in humans is mirrored in a howler monkey hybrid zone. Journal of Heredity 111: 419-428.

Tung, J., & Barreiro, L. B. (2017). The contribution of admixture to primate evolution. Current opinion in genetics & development 47: 61-68.

Sankararaman, S., Mallick, S., Patterson, N., & Reich, D. (2016). The combined landscape of Denisovan and Neanderthal ancestry in present-day humans. Current Biology 26: 1241-1247.

Larson, E. L., Vanderpool, D., Sarver, B. A., Callahan, C., Keeble, S., Provencio, L. L., … & Good, J. M. (2018). The evolution of polymorphic hybrid incompatibilities in house mice. Genetics 209: 845-859.

Funk, E. R., & Taylor, S. A. (2019). High-throughput sequencing is revealing genetic associations with avian plumage color. The Auk 136: ukz048.

Evans, B. J., Tosi, A. J., Zeng, K., Dushoff, J., Corvelo, A., & Melnick, D. J. (2017). Speciation over the edge: gene flow among non-human primate species across a formidable biogeographic barrier. Royal Society open science 4: 170351.

Tosi, A. J., & Hirai, H. (2017). X chromosome introgression and recombination in the cephus group of Cercopithecus monkeys. Cytogenetic and genome research 153: 29-35.

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