Abstract
The male-specific regions of the Y chromosome (MSY) of the human and the chimpanzee (Pan troglodytes) are fully sequenced. The most striking difference is the dramatic rearrangement of large parts of their respective MSYs. These non-recombining regions include ampliconic gene families that are known to be important for male reproduction,and are consequently under significant selective pressure. However, whether the published Y-chromosomal pattern of ampliconic fertility genes is invariable within P. troglodytes is an open but fundamental question pertinent to discussions of the evolutionary fate of the Y chromosome in different primate mating systems. To solve this question we applied fluorescence in situ hybridisation (FISH) of testis-specific expressed ampliconic fertility genes to metaphase Y chromosomes of 17 chimpanzees derived from 11 wild-born males and 16 bonobos representing seven wild-born males. We show that of eleven P. troglodytes Y-chromosomal lines, ten Y-chromosomal variants were detected based on the number and arrangement of the ampliconic fertility genes DAZ (deleted in azoospermia) and CDY (chromodomain protein Y)—a so-far never-described variation of a species' Y chromosome. In marked contrast, no variation was evident among seven Y-chromosomal lines of the bonobo, P. paniscus, the chimpanzee's closest living relative. Although, loss of variation of the Y chromosome in the bonobo by a founder effect or genetic drift cannot be excluded, these contrasting patterns might be explained in the context of the species' markedly different social and mating behaviour. In chimpanzees, multiple males copulate with a receptive female during a short period of visible anogenital swelling, and this may place significant selection on fertility genes. In bonobos, however, female mate choice may make sperm competition redundant (leading to monomorphism of fertility genes), since ovulation in this species is concealed by the prolonged anogenital swelling, and because female bonobos can occupy high-ranking positions in the group and are thus able to determine mate choice more freely.
Highlights
Published cytogenetic comparisons clearly show size differences among the Y chromosomes of our nearest relatives, the chimpanzee (Pan troglodytes) and the bonobo (Pan paniscus) [1,2]
We mapped human-derived DNA probes specific for DAZ and CDY to metaphase Y chromosomes of 17 chimpanzees derived from 11 wild-born males, and 16 bonobos representing seven wild-born males by fluorescence in situ hybridization (FISH) (Figures S1 and S2; Tables S1 and S2)
Two wild-born chimpanzees, ‘‘Max(1)’’ and ‘‘Moritz’’ (Table S1), exhibited an identical pattern for DAZ and CDY but, importantly, the ‘‘Moritz’’ Y chromosome differed by a pericentromeric inversion as well as by the addition of a DAPIpositive segment on its long arm telomere distal to the pseudoautosomal region (PAR) (Figure S3; see online Text S1); these features are responsible for the submetacentric appearance of the Y chromosome (Figure 1) in this specimen
Summary
Published cytogenetic comparisons clearly show size differences among the Y chromosomes of our nearest relatives, the chimpanzee (Pan troglodytes) and the bonobo (Pan paniscus) [1,2]. The non-recombining ampliconic fertility genes TSPY and RBMY are shown to be highly amplified on the bonobo Y when compared to the chimpanzee Y, while these are significantly rearranged on the human Y [2,3].
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