Y Chromosomal Variation Tracks the Evolution of Mating Systems in Chimpanzee and Bonobo

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.

Y-chromosome structural diversity in the bonobo and chimpanzee lineages

“…This finding represents an important step in our understanding of the evolution of sex chromosomes, specifically in the early stages of primate speciation. As a point of comparison, there are no subspecies classifications for bonobos and here we find limited amplicon copy number diversity between individuals, consistent with a previous report (Schaller, et al 2010). This is a surprising observation in light of the high level of nucleotide diversity we detect on the bonobo Y-chromosome ( Figure 1) and may suggest that amplicon CNV may be the result of selection of male-fertility in the chimpanzee lineages.…”

“…However, comparative analysis of the bordering palindrome sequences reveals that these are the result of independent amplifications in chimpanzee and human (Hughes, et al 2010;. As noted in a previous study, copy number of DAZ is polymorphic amongst the common chimpanzees (Schaller, et al 2010). Here we find that Eastern chimpanzees and bonobos each have two copies of DAZ and the red amplicon, while Western and Nigerian-Cameroon have four copies.…”

“…Copy number variation (CNV) of ampliconic genes has been observed in chimpanzees and humans by florescence in situ hybridization (FISH) experiments (Repping, et al 2006;Schaller, et al 2010). Pan species exhibit polyandrous mating behavior, which can drive sperm competition among males (Good, et al 2013).…”

Great ape Y Chromosome and mitochondrial DNA phylogenies reflect subspecies structure and patterns of mating and dispersal

“…However, Figure 1B shows clearly the general retention of sequence content in the XDG regions, including the shared gametologous genes, while also highlighting some intergenic speciesspecific deletions and duplications with respect to the human reference. The only example of large-scale structural variation within species is seen in the Ptr2 structure found in the chimpanzees, Tommy and Moritz; we note that unusual cytogenetically detectable variation, including a pericentromeric inversion, has already been reported in Moritz (Schaller et al 2010). Some MSY rearrangements are associated with reduced male fertility (Carvalho et al 2011); although we do not have direct information on the fertility of Tommy and Moritz, the fact that they share the rearrangement and also a common paternal ancestor over 1000 generations ago, suggests that the Ptr2 structure is unlikely to have a deleterious effect on spermatogenesis.…”

Multicopy gene family evolution on primate Y chromosomes

“…Gene copy number on the msrY is variable between Old World Primate species [ 35 , 36 ], and AG copy number polymorphism is also observed within species [ 37 – 39 ], including humans (reviewed in [ 40 ]). TSPY copy number variation affects male fertility in humans [ 41 – 43 ] and bulls [ 44 ] (but see [ 45 ]), suggesting that copy number of this locus is subject to natural selection [ 20 , 46 ].…”