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Chromosome scale evolution among Hominidae (great apes, humans)

05 Jan
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]

Abstract

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.

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8 responses to “Chromosome scale evolution among Hominidae (great apes, humans)

  1. Marnie

    January 6, 2013 at 1:50 am

    Nice summary. Thanks.

     
  2. Maju

    January 6, 2013 at 3:33 am

    Summary of what I understood, that's it. There's more in the paper but, as I said, it's very technical.

     
  3. terryt

    January 6, 2013 at 8:45 am

    Yes Maju. Nice summary. I find chromosome 12 most interesting. "It is interesting to notice that Pan (chimpanzee) and Gorilla share a derived form of the chromosome 22, indicating that the Hominae split was not too clean, possibly with gorilla introgression into chimpanzees". Do you mean chromosome 12? As you say, it implies that the split between gorillas, chimps and humans may have been almost a triple split with gorillas and chimps on a single line, at least for that chromosome. Or a hybridization event.

     
  4. Maju

    January 6, 2013 at 9:36 am

    Yes, of course that I meant chromosome 12. I'll correct that and also will add a brief note on chromosome 2 which is the one that got fused in the human lineage, while other apes retain the ancestral two chromosomes (so they have 24 pairs in total). "As you say, it implies that the split between gorillas, chimps and humans may have been almost a triple split with gorillas and chimps on a single line, at least for that chromosome. Or a hybridization event". That's what it seems.

     
  5. Marnie

    January 7, 2013 at 7:00 am

    This paper is worth a careful read. There are a number of important recombination processes that are discussed.

     
  6. Maju

    January 7, 2013 at 9:33 am

    Yes, I'm just scratching the surface in the entry.

     
  7. Curious

    June 17, 2013 at 8:40 pm

    Does this, in any way, jeopardize the theory of evolution?

     
  8. Maju

    June 18, 2013 at 8:57 am

    No. Why would it?

     

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