The DNA copying enzymes have a hard time working to the end of a chromosome. For circular chromosomes this is not a problem, since there is not a sharp 'end'. However, for a linear chromosome, without extra mechanisms in place, a bit of DNA is lost off the end of the chromosome after each replication. Because of this, eukaryotes have a telomere to cap off their chromosomes.
In most cells of a mutli-cellular organism, this telomere is slowly worn away after each reproduction leading to apoptosis. Cells that need to reproduce indefinitely such as germ and stem cells have to invest in extra mechanisms to replenish the telomere. For multi-cellular eukaryotes I can see how this might be usefull (for instance as a cancer counter mechanism). However, multi-cellular organisms evolved from single-cell eukaryotes.
I cannot see a reason for wanting apoptosis in a single-cell organism. However, single cell eukaryotes (say yeast) still have linear chromosomes with telomere caps. What advantage did linear chromosomes provide single-cell eukaryotes to offset the extra investment in reparing the telomere?
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I think it is the wrong question. You assume that eukaryotes developed from a single-cell organism with circular DNA. Then, clearly, there must have been an advantage of (newly) developing a linear genome. But eukaryotes could have developed from an organism with linear DNA, too. There are still a few bacterial species with linear chromosomes, so this is not unlikely. We don't know, however.
On the other hand, if linearisation developed independently, you can learn from bacteria why it might have occurred:
J. N. Volff, J. Altenbuchner: A new beginning with new ends: linearisation of circular chromosomes during bacterial evolution. In: FEMS microbiology letters. 186, 2, May 2000, 143–150, PMID 10802162. (Review).
Abstract:
Bacterial circular chromosomes have sporadically become linearised during prokaryote evolution. Unrelated bacteria, including the spirochete Borrelia burgdorferi and the actinomycete Streptomyces, have linear chromosomes. Linear chromosomes may have been formed through integration of linear plasmids. Linear chromosomes use linear plasmid strategies to resolve the 'end-of-replication problem', but they have generally retained from their circular ancestors a central origin of replication. Streptomyces linear chromosomes are very unstable and at high frequency undergo amplifications and large deletions, often removing the telomeres. At least in Streptomyces, chromosome linearity is reversible: circular chromosomes arise spontaneously as products of genetic instability or can be generated artificially by targeted recombination. Streptomyces circularised chromosomes are very unstable as well, indicating that genetic instability is not confined to the linearised chromosomes. Bacterial linear chromosomes may contain telomere-linked regions of enhanced genomic plasticity, which undergo more frequent genetic exchanges and rearrangements and allow differential evolution of genes, depending on their chromosomal location.
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