MHC class I diversity in chimpanzees and bonobos

Abstract

Major histocompatibility complex (MHC) class I genes are critically involved in the defense against intracellular pathogens. MHC diversity comparisons among samples of closely related taxa may reveal traces of past or ongoing selective processes. The bonobo and chimpanzee are the closest living evolutionary relatives of humans and last shared a common ancestor some 1 mya. However, little is known concerning MHC class I diversity in bonobos or in central chimpanzees, the most numerous and genetically diverse chimpanzee subspecies. Here, we used a long-read sequencing technology (PacBio) to sequence the classical MHC class I genes A, B, C, and A-like in 20 and 30 wild-born bonobos and chimpanzees, respectively, with a main focus on central chimpanzees to assess and compare diversity in those two species. We describe in total 21 and 42 novel coding region sequences for the two species, respectively. In addition, we found evidence for a reduced MHC class I diversity in bonobos as compared to central chimpanzees as well as to western chimpanzees and humans. The reduced bonobo MHC class I diversity may be the result of a selective process in their evolutionary past since their split from chimpanzees.Electronic supplementary materialThe online version of this article (doi:10.1007/s00251-017-0990-x) contains supplementary material, which is available to authorized users.

Comparative genetics of the major histocompatibility complex in humans and nonhuman primates

“…Some chimpanzee MHC haplotypes may have an additional HLA‐A ‐like gene, named Patr‐AL (Adams, Cooper, & Parham, 2001;Geller et al., 2002). This gene, however, encodes molecules that have features resembling those of nonclassical HLA molecules (Goyos et al., 2015), and its evolutionary history seems to be complex (Maibach et al., 2017). In gorillas, the orthologues of HLA‐A , HLA‐B and HLA‐C are also present and are named Gogo‐A , Gogo‐B and Gogo‐C (Figure 2a).…”

“…The IPD‐IMGT/HLA database (Robinson et al., 2015) currently comprises data on 5,907 HLA‐A , 7,126 HLA‐B , 5,709 ‐C , 168 HLA‐DPA1 , 1,537 HLA‐DPB1 , 229 HLA‐DQA1 , 1,795 HLA‐DQB1 , 29 HLA‐DRA and 3,331 HLA‐DRB alleles (numbers are according release 3.39.0). For common chimpanzees, individuals of P.t.verus , P.t.troglodytes and P.t.schweinfurthii populations were studied for their MHC repertoire (de Groot et al., 2000;Maibach et al., 2017;Otting, de Groot, & Bontrop, 2019;Wroblewski et al., 2015). One has to realize, however, that for NHP no commercial MHC typing kits are available, and the MHC genes are studied independently.…”

“…MHC research in nonhuman primates (NHP) is carried out because of the important role that several different NHP species may serve as preclinical models for human diseases such as AIDS, malaria, tuberculosis, multiple sclerosis and rheumatoid arthritis, but also in transplantation research (Fitch et al., 2019;Nakamura, Shirouzu, Nakata, Yoshimura, & Ushigome, 2019;t Hart, Bogers, Haanstra, Verreck, & Kocken, 2015;Watkins, Burton, Kallas, Moore, & Koff, 2008). In addition, the MHC in NHP receives increasingly more attention due to issues related to conservation biology (Arguello‐Sanchez et al., 2018;Cao et al., 2015;Hans, Bergl, & Vigilant, 2017;Maibach, Hans, Hvilsom, Marques‐Bonet, & Vigilant, 2017). True orthologues of the human MHC class I and II genes may be present in different NHP species.…”

Flexible mixture model approaches that accommodate footprint size variability for robust detection of balancing selection

“…Furthermore, KLRD1 (CD94) has been shown to play an important role in combating viral infections such as cytomegalovirus (CMV; Cerwenka and Lanier, 2016) and influenza (Bongen et al, 2018) in humans, as well as the mousepox virus in mice (Fang et al, 2011). The involvement in viral defense of KLRD1 presents an especially intriguing case for bonobos, because they have been recently shown to have reduced level of polymorphism in MHC class I genes (Maibach et al, 2017;Wroblewski et al, 2017), and were predicted to have lower ability to bind with viral peptides when compared with chimpanzees (Maibach and Vigilant, 2019). The genes encoding another regulator of MHC class I molecules, the Killer cell Immunoglobin-like Receptors (KIR), were also found to have contracted short haplotypes in bonobos (Rajalingam et al, 2001;Walter, 2014;Wroblewski et al, 2019), and with the lineage III KIR genes serving reduced functions (Wroblewski et al, 2019).…”

“…In addition to their unique behavior, the immune genes in bonobos are also intriguingly more reduced than in humans and chimpanzees, both in their lower diversity of MHC-I repertoires (de Groot et al, 2017;Maibach et al, 2017;Wroblewski et al, 2017), and in the reduction in the number of both KIR genes and their allotypes (Rajalingam et al, 2001). These features are unlikely the natural consequences of demographic factors even after considering the harsher bottlenecks bonobos have undergone compared with chimpanzees; many studies have speculated potential selective sweeps in bonobos on these regions (Prüfer et al, 2012;Walter, 2014;Maibach et al, 2017;Wroblewski et al, 2017Wroblewski et al, , 2019. Specifically, de Groot et al (2002) suggest that an ancient selective sweep, potentially due to simian immunodeficiency virus (SIV; de Groot et al, 2010;Prüfer et al, 2012), may have occurred in the ancestors of bonobos and chimpanzees around two to three million years ago, reducing the MHC-I diversity in both species.…”