The information is not actually "compressed".

What happened in the human lineage was a fusion of two chromosomes into one. In other words, we human have one chromosome that is homologous to two chromosomes in chimps and gorilas. We already know each one was and were it fused (I don't remember from the top of my head, though).

This way, a mutation that fuse cromossomes is not letal, because the cell can still pair the fused chromosomes with the original two. This is not strange to mammals. There are various chromosomal fusions recorded (there is a species of ungulate that have reduced by half their number of chromosomes). We also have intermediaries: some rodent species have a polymorphic number of chromosomes, including uneven numbers. Akodon cursor, for example, can have 16, 17 or 18 chromosomes.

that is not to say that genome reduction is not possible. If i'm not mistaken, birds and bats (and pterosaur, some speculate) have a greatly reduced genome size.

The main point, I guess, is the distinction between genome size (usually called C-value, for diploid organisms) and kariotype number. And neither of those are equal to the amount of functional genes.

Hello. 24 pair of chromosomes go to 23 pairs by an end-to-end fusion of two ancestral chromosomes. That is, two chromosomes joint tail to tail to make up one chromosome.

I think this is a tricky one especially if one considers plant species as well as primates. There seem to be lots of examples in which closely related plant species have different chromosome numbers (e.g . species within the genus Arabidopsis). One can also find examples in the ferns of species with thousands (or at least hundreds) of chromosomes. In plants one also finds lots of examples of (fertile) auto- and allopolyploids, which in its simplest form, means that there are four or six copies of genes that were only represented by two ciopied in an ancestral form.

I am not sure that this is helping much, but I suppose I am saying that plant geneticists may have a handle on some of the key concepts here.

The reduction of chromosome number within the primate lineage leading to modern humans results from chromosome fusion.

It is my understanding that evolution does not have much regard for the number of chromosomes an organism has or how the genome is broken up amongst chromosomes, this seems to be stochastic. That being said, having a different number of chromosomes from great apes only implies that our lineages have been separated for some time and therefore different stochastic events have effected the separate lineages differently. The most parsimonious explanation would be that something occurred in human history since we diverged from apes seeing as humans are unusual among the other apes in regards to their chromosome count. There are several molecular events which can result in the repositioning of sections of DNA from one location to another. These events can lead to the fusion of existing chromosomes or chromosome fragments onto other chromosomes or can result in the formation of entirely new chromosomes.

The information is not actually "compressed".

What happened in the human lineage was a fusion of two chromosomes into one. In other words, we human have one chromosome that is homologous to two chromosomes in chimps and gorilas. We already know each one was and were it fused (I don't remember from the top of my head, though).

This way, a mutation that fuse cromossomes is not letal, because the cell can still pair the fused chromosomes with the original two. This is not strange to mammals. There are various chromosomal fusions recorded (there is a species of ungulate that have reduced by half their number of chromosomes). We also have intermediaries: some rodent species have a polymorphic number of chromosomes, including uneven numbers. Akodon cursor, for example, can have 16, 17 or 18 chromosomes.

that is not to say that genome reduction is not possible. If i'm not mistaken, birds and bats (and pterosaur, some speculate) have a greatly reduced genome size.

The main point, I guess, is the distinction between genome size (usually called C-value, for diploid organisms) and kariotype number. And neither of those are equal to the amount of functional genes.

To answer your question, “How does evolution compress genetic information into fewer chromosomes ?”, I illustrate my answer by using plant datas (most of which comes from our recent paper : Charon C, Bruggeman Q, Thareau V, Henry Y, 2012 Gene duplication within the Green Lineage: the case of TEL genes. Journal of Experimental Botany 63(14): 5061–5077). 1) Genome size is reduced by eliminating DNA (genes,….), and 2) chromosome number is reduced by chromosome fusions (translocations) :

1) During evolution, all the duplicated gene copies were rarely maintained. Indeed, after a polyploidy event, the chromosome content behaves rapidly like a diploid genome in the sense that, in the prophase of meiosis, the chromosomes are going to combine (bivalent), and not be grouped by three or four (tri- and tetravalent). This process is called ‘diploidization’ (Wolfe, 2001).

Very quickly, too, epigenetic mechanisms in the new polyploidy species seem to be used to control the expression of duplicated genes, some copies of which are being turned off (Chen, 2007). For example, in nascent allohexaploid wheats, Zhao et al. (2011) detected extensive and heritable remodelling of DNA methylation at A, B, and D gene loci, coupled with genome stability. The fast elimination of duplicated genes from the new polyploidy genome contributed to genome down-sizing. This ranges from deletion to degradation, illustrated by the presence of elements from the old sequence in a background of different nucleotides (‘ghosts’). For example, in the Arabidopsis thaliana genome, only 28% of genes duplicated by the most recent alpha polyploidy event (30 Mya), have been preserved. Similarly, more than 80% of genes duplicated 50–70 Mya in wheat were lost or diverged in their expression, compared with only 54% for recent (1.5–3 Mya) duplicates (Pont et al., 2011).

Causier et al. (2005) showed that, depending on the species, this may be one of the two copies, not always the ancestral gene, which retains the original function. Surprisingly, the retained duplicated genes were not randomly distributed among different functional categories (Blanc and Wolfe, 2004; Seoighe and Gehring, 2004). On the other hand, ‘duplication-resistant’ genes, i.e. genes that are usually restored to a singleton state after genome duplication, were identified in many species (Paterson et al., 2006).

Reduction of the chromosome number

Superposition of the chromosome numbers of Brassicaceae species with their phylogeny showed unequivocally that the A. thaliana ancestor genome underwent a reduction in chromosome number from n=8 to n=5 (Koch et al., 1999, 2000). This occurred after divergence with its closest relatives (A. halleri and A. lyrata) 4 My to 5 Mya (Kuittinen et Aguade, 2000), and compacted the genome of Arabidopsis thaliana, reducing its chromosome number from n=8 to the current number of n=5. There is a significant amount of evidence indicating that chromosomal fusions were involved. For example, markers distributed along chromosome 4 of A. thaliana form two linkage groups in Capsella rubella (n=8) (Schmidt et al., 2001).

Chromosome painting analyses on Brassicaceae species (Lysak et al., 2006) support the view that the present-day A. thaliana chromosome 4 results from the fusion of two ancestral chromosomes, accompanied by a pericentric inversion. Comparative mapping analyses between the A. thaliana and C. rubella genomes (Boivin et al., 2004) highlighted that each of the five A. thaliana chromosomes are split into two (or three for chromosome 5) different C. rubella linkage groups or segments thereof. Other research groups later confirmed and refined (Koch et Kiefer, 2005 ; Kuittinen et al., 2004 ; Yogeeswaran et al., 2005) this analysis by comparing the genomes of A. thaliana and Arabidopsis lyrata. They also concluded that translocations and inversions explain most differences between the genetic maps of A. thaliana and A. lyrata. These chromosomal reorganizations, including the merger of chromosomes, were dated after the divergence between A. lyrata and A. thaliana, less than 5 Mya (Koch et Kiefer, 2005). The DNA content of the A. lyrata genome is higher than that of A. thaliana (Kuittinen et Aguade, 2000), suggesting substantial DNA losses in the A. thaliana lineage. Large regions of the A. lyrata genetic map do not match any counterpart on the A. thaliana chromosomes (Yogeeswaran et al., 2005), providing additional evidence that chromosome fragments were lost during the A. thaliana genome evolution.

Current data make possible the assumption that the highly dynamic genomes of Brassicaceae or Glycine max, for example, may result from successive rounds (Henry et al., 2006) each including:

first, a polyploidy event that doubles the amount of genetic information;

second, mechanisms preventing homeologous pairing to allow a return to a diploid state;

third, a differential turning off, pseudogenization or the elimination of copies of the duplicated genes;

and, fourth, but simultaneously, chromosomal rearrangements that affect genome organization including the merger of chromosomes reducing their number (Lysak et al., 2006, 2009).

Such successive rounds have created an ancestor of the Brassicaceae with n=4 chromosomes, after successively the hexaploidisation (γ1–γ2) from an Eurosid ancestor possessing n=7, the beta event, and last the alpha event in an ancestral Brassicaceae.

Blanc G, Wolfe KH 2004 Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. The Plant Cell 16: 1679–1691

Boivin K, Acarkan A, Mbulu RS, Clarenz O, Schmidt R. 2004 The Arabidopsis genome sequence as a tool for genome analysis in Brassicaceae. A comparison of the Arabidopsis and Capsella rubella genomes. Plant Physiology 135: 735–744

Causier B, Castillo R, Zhou J, Ingram R, Xue Y, Schwarz-Sommer Z, Davies B 20 Evolution in action: following function in duplicated floral homeotic genes. Current Biology 15(16):1508-12.

Chen ZJ 2007 Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annual Review of Plant Biology 58: 377–406

Henry Y, Bedhomme M, Blanc G 2006 History, protohistory and prehistory of the Arabidopsis thaliana chromosome complement. Trends in Plant Science 11: 267-273

Koch M, Bishop J, Mitchell-Olds T 1999 Molecular systematics and evolution of Arabidopsis and Arabis. Plant Biol. 1: 529–537

Koch M, Haubold B, Mitchell-Olds T 2000 Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis and related genera (Brassicaceae). Mol. Biol. Evol. 17: 1483–1498

Koch,MA, Kiefer M 2005 Genome evolution among cruciferous plants: a lecture from the comparison of the genetic maps of three diploid species – Capsella rubella, Arabidopsis lyrata subsp. tetraea, and A. thaliana. Am. J. Bot. 92: 761–767

Kuittinen H, Aguade M 2000 Nucleotide variation at the chalcone isomerase locus in Arabidopsis thaliana. Genetics 155: 863–872

Kuittinen H, de Haan AA, Vogl C, Oikarinen S, Leppälä J, Koch M, Mitchell -Olds T, Langley CH, Savolainen O 2004 Comparing the linkage maps of the close relatives Arabidopsis lyrataand A. thaliana. Genetics 168: 1575–1584

Lysak MA, Berr A, Pecinka A, Schmidt R, McBreen K, Schubert I, 2006 Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proceedings of the National Academy of Sciences, USA 103: 5224–5229

Lysak MA, Koch MA, Beaulieu JM, Meister A, Leitch IJ, 2009 The dynamic ups and downs of genome size evolution in Brassicaceae. Molecular Biology and Evolution 26: 85–98

Paterson AH, Chapman BA, Kissinger JC, Bowers JE, Feltus FA, Estill JC 2006 Many gene and domain families have convergent fates following independent whole-genome duplication events in Arabidopsis, Oryza, Saccharomycesand Tetraodon. Trends in Genetics 22: 597–602

Pont C, Murat F, Confolent C, Balzergue S, Salse J 2011 RNA-seq in grain unveils fate of neo- and paleopolyploidization events in bread wheat (Triticum aestivum L). Genome Biology 12, R119

Schmidt R, Acarkan A, Boivin K 2001 Comparative structural genomics in the Brassicaceae family. Plant Physiol. Biochem. 39: 253–262

Seoighe C, Gehring C 2004 Genome duplication led to highly selective expansion of the Arabidopsis thaliana proteome. Trends in Genetics 20: 461–464

Wolfe KH 2001 Yesterday's polyploids and the mystery of diploidization. Nature Reviews Genetics 2: 333–341

Yogeeswaran K, Frary A, York TL, Amenta A, Lesser AH, Nasrallah JB, Tanksley SD, Nasrallah ME 2005 Comparative genome analyses of spp.: inferring chromosomal rearrangement events in the evolutionary history of A. thaliana. Genome Research 15: 505–515

Zhao N, Zhu B, Li M, Wang L, Xu L, Zhang H, Zheng S, Qi B, Han F, Liu B 2011 Extensive and heritable epigenetic remodeling and genetic stability accompany allohexaploidization of wheat. Genetics 188: 499–510

Chromosome fusion, of course, is fine, as most people suggested already. Still, the reshaping of two fused chromosomes into one functioning is amazing; it requires the rebuilding of one centromer (therefore loss of centromeric repetitive elements and telomer structures - here obviously remnant sequences are found, e.g. in chromosome 2 of humans. - The question is: at which stage of human evolution did this fusion happen? At the beginning of Homo sapiens or earlier?

Deer species are the most important example in the mammalian chromosome reduction. Muntiacus reevesi has 46 chromosomes and a similar species Muntiacus muntjac has 6 chromosomes in females and 7 in males. The 46 chromosomes from M. reevesi are compressed in these 6 chromosomes of M. muntjac. This "compression" is generated by center and tandem fusions of the chromosomes during the evolutionary process. Then the question is: What is the importance of this reduction of chromosome number? The reduction of chromosome number has an influence in the genetic variability by recombination. Animals with high chromosome number have more potential recombination probabilities and variability in their gametes. In some species using specific habitats, the chromosome reduction will help to mold the species in the habitat loosing variability. In the chromosome reduction by fusions the major part of the chromosomes are preserved, and all genetic information are maintained. As stated by Fabio, the information is not compressed but grouped in derived chromosomes.

I think the answer lies not so much in loss or "compression of genetic information but in the genetic rearrangement that results from chromosomal fusions leading to inactivation or activation of various transcriptional pathways.

As said before, such a reduction of the number of chromosomes is relatively common in some species of mammals, which is due to centric fusions. Another inetresting and well-studied case is that of the house mouse, Mus musculus domesticus, in which the diploid number can be reduced from 40 to 22 chromosomes. But the interesting thing in this cases is the role that this chromosomal reorganizations can play in the speciation process. Has this chromosome reduction appeared parallel to the speciation process, or has "triggered" it somehow? Very interesting studies reveal that chromosomal regions close to such reorganizations tend to accumulate genetic differences at higher rates than not reorganized chromosomal regions. So, this reorganizations could facilitate the accumulation of mutations and the differentiation between chromosomally divergent populations.

The ancient chromosome fusion leading to 2n=48 to 2n=46 karyotypes must have been accompanied by significant loss of genetic material since the modern chimpanzee genome is 6-7% larger than that of human. Perhaps, repeats forming telomeres and centromeres were preferentially eliminated from a newly formed chromosome, the question raised by Vera. This must have happened relatively recently, after the divergence of homo and chimpanzee about 7 myrs. It is up to the debate whether chromosome loss and genetic material might have accelerated human beings evolution.

One comment of the plant geneticists. It is difficult to compare genome evolution between plants and animals since plant tolerate chromosomal changes such as aneuploidy, polyploidy, supernumerary chromosomes far much better than animals where these events are almost lethal.

Ales, could that 6-7% difference not be explained by a myriad of other possible mechanisms or events that may have occurred in the last 6 million years?

Hi Wrosham,

Certainly we can imagine a number of alternative hypothesis that lead to genome and karyotype divegence between humans and chimpanzees: retroelement activity, satellite repeat expansion/contraction, gene conversion, recombination etc.

However, chromosome fusion and subsequent loss of non coding DNA is supported by a simple calculation. For simplicity, let the DNA content is the same for all chromosomes. It follows that loss of one chromosome from 1x = 24 complement equals to 4% reduction of genome size which is the value close to the observed difference in genomie size between two species.

A complete sequence of chimpanzee genome and its pariwise comparison to human reads might perhaps help to clarify the issue althoug the differences are expected in a repeated fraction that is notoroiously difficult to analyze. However, I would not be surprised if few novel functional genes evolved after the speciation event. The CHIMP and HOMO might not be that much similar as previously thought.

Regards,

AK

Evolution has no goal, according to me what happened was chromosomal fusion and genetic rearrangement by chance it was fruitful.

1. I think chromosomal fusion (as well as reciprocal translocations and inversions) does not imply (significant) reduction in genome size (just rearrangement) . The phenomenon is so widespread that it has even a name - Robertsonian - that was very popular in cytogenetic, pre-DNA era.

2. Not all duplications are dooomed to be lost; on the contrary a significant contribution to complixity arises from duplication and subsequent diversification (Ohno's evolution by duplication hypothesis)

3. Rearrangements go on in our species (potentially speciative): see the cases of Down syndrome with only two 21 chromosomes (but with most of a third fused to (I think) chr. 14. In these cases, one of the parents is a carrier of a balanced translocation (just one chr. 21 and a 14+21) and does not show any abnormality.

Reply to Antonio: Chromosome fusion would require inactivation of one of the centromeres since dicentric chromosomes are inherently unstable. Experiments in simple organisms has showed that inactivation of centromeres was connected with loss of centromeric tandem repeats. In addition, there seems to be a higher limit for a chromosomes size that guarantees its safe transmission through the meiosis (Schubert and Out 1997, Cell 88, 515–520). Given that we have smaller genomes than the lovely chimps it is quite high likely that some loss of genetic material occurred after the fusion of chromosomes in a putative human ancestor.

Fully agreed - some degree of deletion occurs but not as much as to 'explain' compression as originally put forward.

The genetic information is presumably very similar among closely related congeneric species, having or not having the same or very different chromosome numbers. See

for example the case of the two Muntiacus deers referred above, which can even

hybridize to give vigorous althought sterile offspring. A reduction of chromosome number does not mean compression of the gene number at all, but that of active centromeres should be obviously decreased. in monocentric species.

The haploid set of human chromosomes has n = 23 chromosomes while the extant species that are most closely related to humans all have n = 24 chromosomes. This difference is due to a fusion of two chromosomes to form a single chromosome (human chromosome 2) that occurred sometime in the human evolutionary lineage following its separation from the ancestor of the other species.

In fishes, we recently presented data that show that there is an obvious trend towards the reduction of the number of chromosomes from values near 2n = 60 with high number of biarmed chromosomes in more primitive species to 2n=48 acrocentric elements in more derived Actinopterygii. Molecular analysis suggests that this reduction is the consequence of loss of repetitive sequences and/or other non-coding DNA sequences, including satellite DNA, ribosomal genes and transposable elements.

Well, I agree with Dr. Frank and understand that it is not about compression of genetic information but about the genetic rearrangements resulted from events like chromosomal fusions and invasion of transposable elements into the genome that might have switched on/ off the various transcriptional pathways.

Chromosomal rearrangements are quite common in eukaryotes. As some people already stated, it does not mean that such event comes with a (significant) loss of genetic material. Maybe the most studied case is the Drosophila genus, in which centromeric fusion between acrocentric chromosomes generated new metacentric chromosomes in different lineages (as happened with human chromosome 2). However, even after such rearrangements, the gene content among homologous chromosomes is highly conserved. As you say, an interesting question is what evolutionary forces drive the fixation of such chromosomal rearrangements. In principle, since this it happens very often, one would not expect chromosomal rearrangements are very deleterious. The cool thing is that you can find in nature species with chromosomal rearrangements that are not fixed yet. These species are good system to study the evolutionary process of chromosomal rearrangements.

Very interesting! I didn't know that within the Drosophila genus some lineages had centromeric fusions. Miguel do you know in which species do this rearrangements occur? Could you tell me some references. Thanks!

Hi Francesc,

Maybe the paper I'd start with is this one:

http://www.genetics.org/content/179/3/1601

In this paper you have a very nice description of the karyotype configurations of the 12 Drosophila species that were sequenced in 2007. In this paper you will find a plethora of interesting references too.

I find particularly interesting Drosophila americana species, since a centromeric fusion between the X chromosome and an autosome was resently originated ant it is not fixed yet. Interesting papers about this species:

http://www.sciencedirect.com/science/article/pii/S1055790304002623

http://onlinelibrary.wiley.com/doi/10.1111/j.1558-5646.2008.00435.x/abstract

For a broader description of the different chromosome rearrangements I'd suggest two of the most important Drosophila books:

1- Michael Ashburner's book:

http://www.amazon.es/Drosophila-Laboratory-Handbook-Michael-Ashburner/dp/1936113694/ref=sr_1_cc_2?s=aps&ie=UTF8&qid=1365749740&sr=1-2-catcorr&keywords=ashburner+drosophila

2- Jeffrey Powell's book:

http://www.amazon.es/Progress-Prospects-Evolutionary-Biology-Drosophila/dp/0195076915/ref=sr_1_2?s=foreign-books&ie=UTF8&qid=1365749824&sr=1-2&keywords=powell+drosophila

“La Autonoma de Barcelona” and “ La Central” have a huge Drosophila study tradition. I am sure you can find these two books (and probably many other important Drosophila books) in there.

Hope this helps. -Best

Thank you very much Miguel!!

Thank you all for the interesting information!

One thing is still not clear to me, though. If we contemplate tracking the chromosome number of, say, Albert Einstein's ancestry tree going backward in time, the forebears would initially all feature 46 chromosomes. By traveling sufficiently far back in time, one must eventually encounter a forebear with 46 chromosomes and at least one parent with a different number. Thus it seems that there must be at least one individual in Einstein's tree, whose parents had different chromosome numbers. Can this fit plausibly into our present understanding of genetics?

I agree with you Kerry, there does seem to be a problem with the chromosome numbers does this mean there were cross species breeding as some suggest? or as others suggest intelligent design was a possiblilty?