PLoS Genetics: The Evolutionary Value of Recombination Is Constrained by Genome Modularity

PLoS Genetics: The Evolutionary Value of Recombination Is Constrained by Genome Modularity: "Genetic recombination may predate the evolution of cellular life [1] and is the basis of ubiquitous biological processes such as DNA repair and sexual reproduction. The combinatorial nature of recombination can provide organisms with vastly more evolutionary options than are available through mutation alone [2–4]. However, kingdom-wide analyses of bacterial recombination [5] and DNA-shuffling studies [6,7] have indicated that the evolutionary value of recombination can vary depending on both the genes and the sub-gene modules transferred. In bacteria, the complexity hypothesis has been proposed to explain an imbalance in detectable informational and operational gene transfers between species [5]. Similarly, the schema hypothesis has been proposed to explain patterns of sequence mosaics observed in DNA-shuffling experiments [7]. Although the complexity hypothesis concerns genes within the context of genomes, the schema hypothesis concerns amino acids within the context of proteins. Both hypotheses are conceptually related and propose that the functionality of sequence fragments in foreign genetic backgrounds is inversely correlated with the complexity of interaction networks within which they must function.

The complexity hypothesis [5] was proposed to explain the disparity in informational (those involved in transcription, translation, and related processes) and operational (those involved in housekeeping) gene transfer rates in bacteria. It states that because informational genes are generally involved in more complex interactions than operational genes, they are less likely to continue functioning well after horizontal transfer. The functional genes produced by shuffling three or more distinct sequences (i.e., 60%–85% identical) are usually derived predominantly from either one sequence or combinations of the most similar sequences [2,6,23,24].

The schema hypothesis proposes that these imbalances are due to the probability of recombinant protein-fold disruption increasing with increasing divergence of parental sequences [6,7]. The probability of the normal network of intragenome interactions being disrupted by recombination increases with increasing divergence of the exchanged fragments The successful inheritance of genomic fragments through recombination is expected to depend on the maintenance of important intragenome interactions. After all, the exchange of a genome fragment could be seen as a simultaneous introduction of multiple mutations. Negative or purifying selection should remove those recombinants that break the epistatic interactions that define the architecture of a particular genome, whereas genetic drift might permit the survival and spread of “neutral” recombinants. Alternatively, positive selection should favour the spread of rare recombinants with improved genomic interactions. The genomic interactions in the (natural) parental viruses used in these experiments have most likely been optimised through selection over long evolutionary periods. None of the recombinants generated from these viruses was more fit than the fitter of its parents, which is expected if negative selection is the dominant force that now maintains the integrity of these genomes.

The relative degree of modularity that we demonstrated experimentally for each genome component appears to be reflected in the recombination events detected within the same regions in natural viruses represented in GenBank. This correlation is surprising because the natural recombinants—unlike the recombinants we constructed in the laboratory—involve exchanges of fragments of genes or intergenic regions. Such exchanges may disrupt intraprotein or intra-intergenic region interactions as well as interaction networks amongst whole genes and intergenic regions. Survival of the natural viruses with detectable recombination events in coding regions presumably depended on their inheritance of sequences that did not overly disrupt either intraprotein or intergene/intergenic region interaction networks; survival of natural intergenic region recombinants and those we generated in the laboratory would have been subject only to the latter constraint. The correlation between our experimental results and the inferred natural recombinants may indicate that maintenance of intergenome component interactions is the principal determinant of recombination tolerance (at least for MSV and closely related viruses). Alternatively, a requirement for the preservation of both intergenome component, and intragene, interaction networks has a net effect that is difficult to distinguish from either constraint operating alone.

We have provided experimental support for the complexity hypothesis by demonstrating a relationship between the relative modularity of defined genomic regions and the complexity of interactions in which they are involved. The striking correlation between our experimental results and the types of recombination observed in nature lends credence to the notion that these detectable modularity differences are evolutionarily relevant. Our results also suggest that the degree of similarity between an inherited sequence and the sequence it replaces is an important additional determinant of recombinant fitness. Whereas recombination can substantially increase the evolutionary options of an organism, the obligatory maintenance of co-evolved interaction networks may severely restrict its evolutionary value."

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Blogger qtr said...

Glossary of terms: classification systems and population mechanisms in speciation:

Allopatric speciation occurs when a geographical barrier sub-divides a parent species, resulting in geographic and reproductive isolation such that the descendent species can no longer interbreed upon removal of the barrier.

Anagenesis differs from cladogenesis in that one species progressively transforms into a replacement species when sufficient gene mutations fix in the descendant population. At this point, the ancestral species has become extinct. This mechanism is distinct from the increase in numbers of species generated by cladogenetic branching events.

Cladogenesis is the mechanism of speciation in which one or more lineages (clades) arise from an ancestral line. Such speciation events increase the variety of plants or animals through branching of the phylogenetic tree. Cladogenesis is differentiated from anagenesis, which is the in toto replacement of one species by an anatomically distinct species.

Monophyletic taxon or clade: an accurate grouping of only (opp. polyphyletic) and all (opp. paraphyletic) descendents of a shared common ancestor. A monopyletic group is genetically homogeneous and reflects evolutionary relationships.

Paraphyletic taxon or clade: a monophyletic group that excludes one or more discrete groups descended from the most recent common ancestral species of the entire group. Other descendent species of the most recent common ancestor have been excluded from the paraphyletic taxon, usually because of morphologic distinctiveness.

Phenetic system: groupings of organisms based on mutual similarity of phenotypic (physical and chemical) characteristics. Phenetic groupings may or may not correlate with evolutionary relationships.

Phylogenetic system: groups organisms based on shared evolutionary heritage. DNA and RNA sequencing techniques are considered to give the most meaningful phylogenies.

Phylogenetic separation into evolutionary relationships (clades), based on comparison of genomes is likely to supplant phenotypical (phenetic) taxonomies of the prokaryotes.

Peripatry (paripatry) is a subset of allopatry in which an isolated group has a smaller population than the parent group. Ernst Mayr introduced the term. Peripatric speciation occurs when the smaller sub-group of a species enters a novel niche within the range of the parent species, becoming geographically and reproductively isolated. Peripatric speciation (paripatric) is distinguished from allopatric speciation by the smaller size of the isolate group, and from sympatric speciation, which involves no barrier to breeding.

Polyphyletic taxon: opposite to monophyletic taxon: A polyphyletic group is mistakenly or improperly erected on the basis of homoplasy — characteristics that have arisen despite not sharing a common ancestor. Homoplasy arises because of convergent evolution, parallelism, evolutionary reversals, horizontal gene transfer, or gene duplications. Polyphyletic taxa are genetically heterogeneous because members do not share a common ancestor.

Neontology is a branch of biology that emphasizes the study of modern biota (living or recent organisms) rather than fossilized organisms (paleontology).

Numerical Taxonomies are a common approach to phenetic taxonomy that employ a number of phenotypic characteristics to generate similarity coefficients that may be mapped in dendrograms. Groupings based on numerical taxonomy may or may not correlate with evolutionary relationships.

Taxonomies aim to group organisms according to shared characteristics against the background of biological diversity.

Sympatry involves no geographical separation of sub-populations of individuals. Sympatric speciation events occur most often in plants by the mechanism of polyploidy in which the number of chromosomes is doubled or tripled. John Maynard Smith proposed a model called disruptive speciation, in which homozygotes might have greater fitness than heterozygotes under some environmental conditions.

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