The small apes (gibbons) are one of the most dramatic examples
of extremely rapid karyotype evolution, and it is intriguing
in this respect to note that among the apes (superfamily
Hominoidea) the hylobatids have the highest number of species.
There is little agreement on the exact numbers, but there
are from 14 to 19 living gibbon species. Chromosomal changes
in gibbons are up to 20 times that of the average mammalian
rate and are only surpassed by some muroid rodents. The importance
of understanding their rapid genome evolution is also
provided by their phylogenetic affinity to humans. Gibbons and
humans diverged about 17–23 million years ago (Matsudaira
and Ishida 2010) and are classified in the same superfamily
Hominoidea.
Yet, a satisfactory explanation of why gibbons experienced
such an accelerated rate of evolution has escaped our understanding.
One reason is that the full extent of their chromosomal
changes is not yet well-documented, even at the molecular cytogenetic
level. Because the rearrangements are so complex, chromosome
painting, the mostly widely applied molecular cytogenetic
technique (Muller et al. 2003), did not allow final conclusions
about the number of rearrangements and about the steps that led
to the four existing karyomorphs that typify each genus of small
apes: Hoolock (2n = 38), Hylobates (2n = 44), Symphalangus (2n = 50),
and Nomascus (2n = 52). Molecular cytogenetic techniques now
allow a significantly higher resolution than chromosome painting
through the use of hybridization of precisely mapped BAC
clones, microarrays, and selective sequencing. Using these approaches
we recently defined the chromosomal changes and
synteny block organization of Hylobates lar (HLA, lar gibbon) and
Nomascus leucogenys (NLE, white-cheeked gibbon) (Carbone et al.
2006; Roberto et al. 2007; Misceo et al. 2008; Girirajan et al.
2009). Yet, the reconstruction of the evolutionary history of rearrangements
is only as complete as the taxonomic array of relevant
species. Here, we report a comparable detailed analysis of
the chromosomes of the two remaining karyomorphs, Hoolock
leuconedys (HLE, eastern hoolock gibbon) and Symphalangus syndactylus
(SSY, siamang gibbon). For the first time, we provide an
analysis involving the complete taxon set of the four small ape
karyomorphs. These data permit a more complete and accurate
reconstruction of their ancestral genome and provides the basis
to understand the steps that led to the amazing chromosomal
diversity found today among small apes. This study provides the
most comprehensive insight into the evolutionary origins of chromosome
rearrangements involved in transforming the genome in
small apes. In addition, the close evolutionary relationship between
small apes, Hominidae, and OldWorld monkeys also means
that the results are set against the detailed evolutionary history of
these species, the human genome in particular. The comparison
provides exquisite resolution to understand the flow of chromosome
rearrangements and to place each rearrangement on a phylogenetic
tree.
The small apes (gibbons) are one of the most dramatic examples
of extremely rapid karyotype evolution, and it is intriguing
in this respect to note that among the apes (superfamily
Hominoidea) the hylobatids have the highest number of species.
There is little agreement on the exact numbers, but there
are from 14 to 19 living gibbon species. Chromosomal changes
in gibbons are up to 20 times that of the average mammalian
rate and are only surpassed by some muroid rodents. The importance
of understanding their rapid genome evolution is also
provided by their phylogenetic affinity to humans. Gibbons and
humans diverged about 17–23 million years ago (Matsudaira
and Ishida 2010) and are classified in the same superfamily
Hominoidea.
Yet, a satisfactory explanation of why gibbons experienced
such an accelerated rate of evolution has escaped our understanding.
One reason is that the full extent of their chromosomal
changes is not yet well-documented, even at the molecular cytogenetic
level. Because the rearrangements are so complex, chromosome
painting, the mostly widely applied molecular cytogenetic
technique (Muller et al. 2003), did not allow final conclusions
about the number of rearrangements and about the steps that led
to the four existing karyomorphs that typify each genus of small
apes: Hoolock (2n = 38), Hylobates (2n = 44), Symphalangus (2n = 50),
and Nomascus (2n = 52). Molecular cytogenetic techniques now
allow a significantly higher resolution than chromosome painting
through the use of hybridization of precisely mapped BAC
clones, microarrays, and selective sequencing. Using these approaches
we recently defined the chromosomal changes and
synteny block organization of Hylobates lar (HLA, lar gibbon) and
Nomascus leucogenys (NLE, white-cheeked gibbon) (Carbone et al.
2006; Roberto et al. 2007; Misceo et al. 2008; Girirajan et al.
2009). Yet, the reconstruction of the evolutionary history of rearrangements
is only as complete as the taxonomic array of relevant
species. Here, we report a comparable detailed analysis of
the chromosomes of the two remaining karyomorphs, Hoolock
leuconedys (HLE, eastern hoolock gibbon) and Symphalangus syndactylus
(SSY, siamang gibbon). For the first time, we provide an
analysis involving the complete taxon set of the four small ape
karyomorphs. These data permit a more complete and accurate
reconstruction of their ancestral genome and provides the basis
to understand the steps that led to the amazing chromosomal
diversity found today among small apes. This study provides the
most comprehensive insight into the evolutionary origins of chromosome
rearrangements involved in transforming the genome in
small apes. In addition, the close evolutionary relationship between
small apes, Hominidae, and OldWorld monkeys also means
that the results are set against the detailed evolutionary history of
these species, the human genome in particular. The comparison
provides exquisite resolution to understand the flow of chromosome
rearrangements and to place each rearrangement on a phylogenetic
tree.
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