Category Archives: orangutan

Chromosome scale evolution among Hominidae (great apes, humans)

I won’t surely be able to make justice here to this most interesting but highly technical paper but mention must be done of it in any case:
Marta Farré et al., Recombination Rates and Genomic Shuffling in Human and Chimpanzee—A New Twist in the Chromosomal Speciation Theory. Molecular Biology and Evolution, 2012. Open accessLINK [doi: 10.1093/molbev/mss272]


A long-standing question in evolutionary biology concerns the effect of recombination in shaping the genomic architecture of organisms and, in particular, how this impacts the speciation process. Despite efforts employed in the last decade, the role of chromosomal reorganizations in the human–chimpanzee speciation process remains unresolved. Through whole-genome comparisons, we have analyzed the genome-wide impact of genomic shuffling in the distribution of human recombination rates during the human–chimpanzee speciation process. We have constructed a highly refined map of the reorganizations and evolutionary breakpoint regions in the human and chimpanzee genomes based on orthologous genes and genome sequence alignments. The analysis of the most recent human and chimpanzee recombination maps inferred from genome-wide single-nucleotide polymorphism data revealed that the standardized recombination rate was significantly lower in rearranged than in collinear chromosomes. In fact, rearranged chromosomes presented significantly lower recombination rates than chromosomes that have been maintained since the ancestor of great apes, and this was related with the lineage in which they become fixed. Importantly, inverted regions had lower recombination rates than collinear and noninverted regions, independently of the effect of centromeres. Our observations have implications for the chromosomal speciation theory, providing new evidences for the contribution of inversions in suppressing recombination in mammals. 

Maybe most interesting, at least for the casual reader, is this graph:

Fig. 1.

Evolutionary history of human chromosomes superimposed on the phylogeny of great apes. Black lines within the phylogenetic tree represent the ancestral state of the chromosomes, whereas red and orange lines represent the rearranged forms. Orangutan maintains the ancestral form for orthologous chromosomes 3 and 11, whereas human, chimpanzee, and gorilla forms are derived. Orthologous chromosomes 1, 2, and 18 have been rearranged in the lineage leading to humans, whereas orthologous chromosomes 4, 9, 15, 16, and 17 are rearranged in the lineage leading to chimpanzee. Ancestral chromosome 5 has been maintained in orangutan and human but has suffered two independent inversions in chimpanzee and gorilla, respectively. Chromosome 7 has suffered one inversion, which has been fixed in gorilla, and another inversion has been fixed in the lineage leading to human and chimpanzee. Chromosome 10 underwent one inversion that was fixed in human and chimpanzee, and a new inversion fixed in gorilla. Finally, chromosome 12 has maintained the ancestral form in humans and orangutans but has undergone an inversion that has been fixed in chimpanzee and gorilla, therefore, the polymorphic state has persisted across multiple speciation nodes (gorilla–human–chimpanzee and human–chimp).

large original version

No changes at this scale happened in the other eight autosomes (6, 8, 13, 14, 19, 20, 21, and 22) in any of the four genera. 
Warning must be done about the timeline, which should be twice as old at least for the Pan-Homo split.
It is interesting to notice that Pan (chimpanzee) and Gorilla share a derived form of the chromosome 12, indicating that the Homininae split was not too clean, possibly with gorilla introgression into chimpanzees. 
It is also interesting to realize that orangutans (Pongo) are extremely conservative in the genome (all 22 chromosomes, what means that surely the common ancestor of all Hominidae was more similar to modern orangutans than to any other branch. 
Finally I find notable that our chimpanzee cousins are actually more evolved than us, literally, a blunt numerical truth that is strongly counterintuitive for our anthropocentric vision of biology and evolution. While us humans have conserved 15 ancestral chromosomes (almost as many as gorillas: 16), chimpanzees only conserved 11, evolving one step (red lines) 9 chromosomes (humans 6, gorillas 5) and two steps (orange lines) two chromosomes (humans and gorillas just one).

PS- On the other hand, our Homo branch has a peculiar chromosomal rearrangement that puts up quite apart from the rest of Hominidae: two ancestral chromosomes got fused into a single one (chromosome 2) in our line. This may well have been decisive in our reproductive divergence from Pan and even maybe Gorilla, crafting a very impassable biological barrier. (Not in the paper, just my afterthought).

Incidentally, a 2006 study (Wainwright 2006) claimed to have found some strong correlation between cognitive abilities (not just IQ but also other more creative aspects of the mind) and areas of chromosome 2. With the usual caution I guess it is worth mentioning here.


Hominid speciation: sudden or gradual?

It depends apparently: bonobos may have diverged quite suddenly while in other cases, including the Pan-Homo split, the process of speciation appears to have been more gradual.

Thomas Mailund et al., A New Isolation with Migration Model along Complete Genomes Infers Very Different Divergence Processes among Closely Related Great Ape Species. PLoS ONE 2012. Open access LINK [doi:10.1371/journal.pgen.1003125]


We present a hidden Markov model (HMM) for inferring gradual isolation
between two populations during speciation, modelled as a time interval
with restricted gene flow. The HMM describes the history of adjacent
nucleotides in two genomic sequences, such that the nucleotides can be
separated by recombination, can migrate between populations, or can
coalesce at variable time points, all dependent on the parameters of the
model, which are the effective population sizes, splitting times,
recombination rate, and migration rate. We show by extensive simulations
that the HMM can accurately infer all parameters except the
recombination rate, which is biased downwards. Inference is robust to
variation in the mutation rate and the recombination rate over the
sequence and also robust to unknown phase of genomes unless they are
very closely related. We provide a test for whether divergence is
gradual or instantaneous, and we apply the model to three key divergence
processes in great apes: (a) the bonobo and common chimpanzee, (b) the
eastern and western gorilla, and (c) the Sumatran and Bornean
orang-utan. We find that the bonobo and chimpanzee appear to have
undergone a clear split, whereas the divergence processes of the gorilla
and orang-utan species occurred over several hundred thousands years
with gene flow stopping quite recently. We also apply the model to the Homo/Pan speciation event and find that the most likely scenario involves an extended period of gene flow during speciation.


Tandem repeat accumulation drives evolution in great apes

Tandem repeats (also known as mini-/microsatellites) used to be considered ‘neutral’ junk genome, yet they are proving themselves quite more than just that.
Among other things, this paper is a great manual to better understanding the differences between great apes (including humans) chromosome by chromosome:
Chromosome 1.

Human chromosome 1 is considered to be the derived form, showing a pericentric inversion when compared to chimpanzee and orangutan chromosome 1. The human tandem repeat landscape also differs from the other two great apes (HSA vs PTR: p-value = 0.006; HSA vs PPY: p-value = 0.000).

Chromosome 2.

It is well known that human chromosome 2 derives from the ancestral form by a fusion of two hominoid homolog chromosomes [1]. The ancestral 2a form corresponds to HSA2pq and also has suffered a pericentric inversion in the human form, whereas the ancestral 2b form has not suffered further reorganizations. The tandem repeat contour is different between human and the other great apes regarding chromosome 2a form (HSA vs PTR: p-value = 0.000; HSA vs PPY: p-value = 0.000) but is maintained in the homologous chromosome 2b form (HSA vs PTR: p-value = 0.738; HSA vs PPY: p-value = 0.192).

Chromosome 3.

Human and chimpanzee chromosomes are the derived forms, with an inverted region compared to orangutan chromosome. The tandem repeats distribution confirms this pattern (HSA vs PTR: p-value = 0.062; HSA vs PPY: p-value = 0.009).

Chromosome 4.
All the great apes have a derivative chromosome 4 that evolved differently since their common ancestor. We found a different tandem repeats distribution between human and chimpanzee forms but the same distribution between human and orangutan forms (HSA vs PTR: p-value = 0.022; HSA vs PPY: p-value = 0.272).
Chromosome 5.
Human chromosome is considered the ancestral form, whereas the chimpanzee and the orangutan have derived forms due to pericentric inversions. The tandem repeats landscape is consistent with this pattern (HSA vs PTR: p-value = 0.031; HSA vs PPY: p-value = 0.001).
Chromosome 6.
The three species shared the same chromosome form, which is considered to be ancestral. We found the same tandem repeat profile between human and chimpanzee (HSA vs PTR: p-value = 0.069) but it differs between human and orangutan (HSA vs PPY: p-value = 0.003).
Chromosome 7.
The orangutan chromosome represents the ancestral form, while human and chimpanzee share a pericentric inversion. We found the same tandem repeats pattern in human and chimpanzee (HSA vs PTR: p-value = 0.203) but this was different in orangutan (HSA vs PPY: p-value = 0.050) (Fig. 4a).
Chromosome 8.
The three hominoid species share the same form but we detected an insertion of ~3Mb in the orangutan chromosome 8 (Table 2). This difference is reflected in the tandem repeats landscape, being equal between human and chimpanzee (p-value = 0.128) but different in orangutan (p-value = 0.009) (Fig. 4b).
Chromosome 9.
All three species have different chromosomal forms, being the orangutan chromosome the ancestral one. Tandem repeats distribution is consistent with these differences (HSA vs PTR: p-value = 0.002; HSA vs PPY: p-value = 0.000).
Chromosome 10.
Orangutan chromosome 10 is considered to be the ancestral form, which differs from human and chimpanzee forms by a paracentric inversion. We found that human and orangutan have a different tandem repeat pattern (p-value = 0.001) as well as human and chimpanzee (p-value = 0.010), although the same pattern between these two species was expected.
Chromosome 11.
The ancestral chromosome form is conserved in orangutan, which differs from the human chromosome by a pericentric inversion and from chimpanzee by a pericentric inversion and an insertion of ~400 Kb (Table 2). These differences are also reflected in the tandem repeat distribution (HSA vs PTR: p-value = 0.016; HSA vs PPY: p-value = 0.000).
Chromosome 12.
Human and orangutan share the same form, which is considered the ancestral. Chimpanzee differs from them by a pericentric inversion. In this case, the tandem repeats landscape is different between human and chimpanzee (p-value = 0.050) and between human and orangutan (p-value = 0.004).
Chromosome 13.
Human and chimpanzee share the same form and have the same tandem repeats pattern (p-value = 0.072), while orangutan have a ~100Kb insertion (Table 2) and shows a different tandem repeats pattern (p-value = 0.003).
Chromosome 14.
All great apes share the same chromosome form and also the same tandem repeats landscape (HSA vs PTR: p-value = 0.051; HSA vs PPY: p-value = 0.051).
Chromosome 15.
All great apes have different chromosome forms and different tandem repeats profile (HSA vs PTR: p-value = 0.004; HSA vs PPY: p-value = 0.001).
Chromosome 16.
All great apes have different chromosome forms and different tandem repeats profile (HSA vs PTR: p-value = 0.001; HSA vs PPY: p-value = 0.000).
Chromosome 17.
Human and orangutan share the same ancestral form, while chimpanzee suffered a pericentric inversion. This pattern is in agreement with the tandem repeats distribution (HSA vs PTR: p-value = 0.030; HSA vs PPY: p-value = 0.106).
Chromosome 18.
Chimpanzee and orangutan share a chromosome form ancestral to great apes, which differs from the human by a pericentric inversion. This is not observed in the tandem repeats profile, given that all the species share the same distribution (HSA vs PTR: p-value = 0.095; HSA vs PPY: p-value = 0.206).
Chromosome 19, 20, 21 and 22.
All great apes share the same chromosome form and also the same tandem repeats landscape [HSA19 (PTR: p-value = 0.127; PPY: p-value = 0.161) HSA20 (PTR: p-value = 0.138; PPY: p-value = 0.051) HSA21 (PTR: p-value = 0.106; PPY: p-value = 0.111) HSA22 (PTR: p-value = 0.082; PPY: p-value = 0.051)].
Chromosome X.
Human and chimpanzee share the same ancestral form while orangutan has a ~2Mb insertion (Table 2). Tandem repeat pattern is in agreement with human-orangutan evolution (p-value = 0.021) but not with human-chimpanzee history (p-value = 0.000).

But while this is most interesting, it is not the only or main finding of this paper: the authors find that tandem repeats accumulate in the evolutionary breakpoint regions (EBRs) at higher rate than expected under neutrality conditions. Instead the homologous synteny blocks (HSB), highly conserved areas, display lower rate of tandem repeats than expected. 

Although no specific repeat motif was exclusively present in EBRs or HSBs, 17 different microsatellites motifs were significantly accumulated in EBRs. Notably, out of these overrepresented tandem repeats, the AAAT was the most frequently detected. It has been described that this motif could form single-stranded coils [24], favoring chromatin instability and increasing the likelihood to break.


Orangutans and us

There is a couple of genetic stories on those our red-haired cousins from Indonesia and their genomes, and ours…

On one side A. Hobolth and colleagues call our attention to the fact that parts of our genome are closer to orangutans than to chimpanzees or bonobos, our closest relatives. This does not change anything in regards to our degree of relatedness just tells us of some genes that have evolved in the Pan genus and not in the Homo one.

Refs.: Science Daily story, paper at Genome Research (pay per view).

Meanwhile D. P. Locke and colleagues argue that Orangutan genome has evolved much less than ours or that of our Pan cousins. This is particularly true in regards to Alu elements, which have accumulated very fast in our species, at half that rhythm in Chimpanzees and almost not at all in Orangutans.

Refs. Science Daily story, article at Nature (open).

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Posted by on January 28, 2011 in biology, human evolution, human genetics, orangutan