Androgen receptor and monoamine oxidase polymorphism in wild bonobos

Abstract

Androgen receptor gene (AR), monoamine oxidase A gene (MAOA) and monoamine oxidase B gene (MAOB) have been found to have associations with behavioral traits, such as aggressiveness, and disorders in humans. However, the extent to which similar genetic effects might influence the behavior of wild apes is unclear. We examined the loci AR glutamine repeat (ARQ), AR glycine repeat (ARG), MAOA intron 2 dinucleotide repeat (MAin2) and MAOB intron 2 dinucleotide repeat (MBin2) in 32 wild bonobos, Pan paniscus, and compared them with those of chimpanzees, Pan troglodytes, and humans. We found that bonobos were polymorphic on the four loci examined. Both loci MAin2 and MBin2 in bonobos showed a higher diversity than in chimpanzees. Because monoamine oxidase influences aggressiveness, the differences between the polymorphisms of MAin2 and MBin2 in bonobos and chimpanzees may be associated with the differences in aggression between the two species. In order to understand the evolution of these loci and AR, MAOA and MAOB in humans and non-human primates, it would be useful to conduct future studies focusing on the potential association between aggressiveness, and other personality traits, and polymorphisms documented in bonobos.

Keywords: AR, androgen receptor gene; ARG, repeat locus coding glycine in androgen receptor gene; ARQ, repeat locus coding glutamine in androgen receptor gene; Androgen receptor; Bonobo; Genetic variation; MAOA, monoamine oxidase A gene; MAOB, monoamine oxidase B gene; MAin2, repeat locus in intron 2 of monoamine oxidase A gene; MBin2, repeat locus in intron 2 of monoamine oxidase B gene; Monoamine oxidase; PCR, polymerase chain reaction..

Fig. 1

Comparison of AR CAG repeats among bonobo, chimpanzee and human. Bo bonobo, Ch chimpanzee, Hu human. The number following CAG represents the repeat number of CAG trinucleotide. In the nucleotide sequence a: the preceding sequence that is common in bonobos, chimpanzees and humans, b: the preceding CTG repeats, c: the CAG repeats, d: a following sequence that is common in the three species, e indicates a second, non-polymorphic CAG repeat region, f: the following sequence that is common in the three species. GenBank accession numbers: human CAG21 NM_000044, chimpanzee CAG21 NM_001009012, bonobo CAG15–CAG18 AB970511–AB970514AB970511AB970512AB970513AB970514.

Fig. 2

Comparison of AR GGN repeats among bonobo, chimpanzee and human. Bo bonobo, Ch chimpanzee, Hu human. The number following GGN represents the repeat number of GGN trinucleotide. In the nucleotide sequence a: the preceding sequence that is common in bonobos, chimpanzees and humans, b, c, d and e: the GGN repeat region, b: (GGT)₂, c: (GGG)₂ in the Pan genus and GGTGGG in human, d: (GGT)₂, e: (GGC)_n, f: the following sequence that is common in the three species. GenBank accession numbers: human GGN23 NM_000044, chimpanzee GGN17 NM_001009012, bonobo GGN18 AB970515, GGN19 AB970516.

Fig. 3

Comparison of MAOA CN repeats among bonobo, chimpanzee and human. Bo bonobo, Ch chimpanzee, Hu human. The number following CN represents the repeat number of CN dinucleotide. In the nucleotide sequence a: the preceding sequence that is identical in the three species with the exception of a C/T SNP in bonobos (underlined) and a monomorphic G → T single nucleotide change in humans (boxed), b: the CA repeat region, c: CGCA in the Pan genus with a G/A SNP in bonobo (circled), (CGCA)₂ in human, d: (CA)₂ in the three species, e: the following sequence that is common in the three species. GenBank accession numbers: human CN20 AB302097, CN24 AB302098, chimpanzee CN15 AB302099, CN16 AB302100, bonobo CN17–CN19, CN22 AB970517–AB970520AB970517AB970518AB970519AB970520.

Fig. 4

Comparison of MAOB GN repeats among bonobo, chimpanzee and human. Bo bonobo, Ch chimpanzee, Hu human. The number following GN represents the repeat number of GN dinucleotide. In the nucleotide sequence a: the preceding sequence that is common in bonobos, chimpanzees and humans, b: (TG)₄ with a T/C SNP in bonobos (boxed), c: common in the three species, d: the GN repeat region, e: CA(GA)₄, f: the following sequence that is common in the three species. GenBank accession numbers: human GN24 X63276, GN27 AB302115, chimpanzee GN24 AB302116, GN25 AB2117, bonobo GN20–GN24 AB970521–AB970525AB970521AB970522AB970523AB970524AB970525.