Evidence for an ancient adaptive episode of convergent molecular evolution

Castoe et al., “Evidence for an ancient adaptive episode of convergent molecular evolution”  PNAS, April 29, 2009, published on line, doi: 10.1073/pnas.0900233106

 

Abstract: …..These results indicate that nonneutral convergent molecular evolution in mitochondria can occur at a scale and intensity far beyond what has been documented previously, and they highlight the vulnerability of standard phylogenetic methods to the presence of nonneutral convergent sequence evolution.

 

I left a comment on the preprint version of this paper at Nature precedings. http://precedings.nature.com/documents/2123/version/1#comments

 

Indeed, convergent evolution is extremely common. The best illustration of this is a phenomenon I termed ‘genetic nonequidistance to a more complex outgroup’. Thus, relative to a complex outgroup such as human, some sister species from a simple clade are not equidistant to human. The more complex sister species is always closer to human than the simpler sister species. In all five cases (except plants) examined where difference in complexity of the sister species can be inferred (octopus vs. cockle, Terebratulina vs. Lingula, bird vs. snake, dragonfly vs. louse, and smut vs. yeast), the more complex species always show greater sequence similarity to humans.

Because these sister species are separated from humans for the same amount of time, their different sequence similarity to humans must be due to convergent evolution. Thus, sequence similarity to complex species or humans cannot be used to infer closer genealogy with humans.

The sister grouping of chimpanzees and humans really has no other non-ambiguous support other than sequence similarity as measured by percent identity. The premise for this approach has now been nullified by the phenomenon of genetic non-equidistance to a more complex outgroup despite equidistance in time or genealogy. The same premise for grouping an ape (chimpanzee) with human to the exclusion of another ape (orangutan) would equally justify the obviously absurd grouping of human with a mollusk (octopus) to the exclusion of another mollusk (cockle), or with a brachiopod (Terebratulina) to the exclusion of another brachiopod (Lingula), or with a reptile (bird) to the exclusion of another reptile (snake).

The molecular clock hypothesis, i.e., vastly different species have very similar mutation rates, is a tautological interpretation of the ‘genetic equidistance’ result. It is falsified by the ‘genetic nonequidistance’ phenomenon as discussed above. I have recently come up with the ‘maximum genetic diversity’ (MGD) hypothesis to explain equally well both the equidistance and the nonequidistance phenomenon. See my paper posted here, “Inverse relationship between genetic diversity and epigenetic complexity”.

Below is a paragraph from one of my recent manuscripts discussing one of the best facts (newly reported in Nature this year) that simply cannot be reconciled in any way with the sister grouping of humans and chimpanzees but fully supports the MGD hypothesis and the sister grouping of humans and pongids.

Consistent with low genetic diversity in humans, human specific segmented duplications show lower copy number polymorphisms in humans than chimpanzee specific segmented duplications do in chimpanzees [54]. Similarly, those duplications shared among human, chimpanzees, and orangutans, or those shared among human, chimpanzees, orangutans, and monkeys are also less polymorphic in humans than in chimpanzees, indicating clearly that duplications that are shared because of common ancestry are less polymorphic in humans than in chimpanzees. In contrast, the duplications shared between human and chimpanzees are equally polymorphic in humans and chimpanzees. This unusual result contradicts the sister grouping of humans and chimpanzees, because both the MGD and the bottleneck hypothesis would predict lower polymorphism in humans if these duplications are shared because of common ancestry. However, it is fully consistent with the interpretation that the shared duplications between humans and chimpanzees are not due to common ancestry but are due to common selection of independent duplications. Common selection leading to shared sequences is well established [55]. The MGD hypothesis interprets many of the shared sequences between human and chimpanzees as a result of common selection rather than common ancestry. The similar selection pressure leads to similar levels of polymorphism. This result is thus one of the best that simply cannot be reconciled in any way with the sister grouping of humans and chimpanzees but fully supports the MGD hypothesis and the sister grouping of humans and pongids.

Ref:
54. Marques-Bonet T, Kidd JM, Ventura M, Graves TA, Cheng Z, et al. (2009) A burst of segmental duplications in the genome of the African great ape ancestor. Nature 457: 877-881.
http://www.publicacions.ub.es/refs/micoshumans.pdf

55. Bull JJ, Badgett MR, Wichman HA, Huelsenbeck JP, Hillis DM, et al. (1997) Exceptional convergent evolution in a virus. Genetics 147: 1497-1507.

Exceptional convergent evolution in a virus

This paper showed nicely that common selection can lead to extensive identity in DNA sequences. Thus, sequence comparison cannot always be used for inferring time of separation. This is exactly the point made by my MGD hypothesis. When we see a human and chimp identity of ~98%, we must first ask how much of that is due to common selection. The MGD says that there is a lot. The data are completely consistent with a pongid clade with human as the outgroup. Common selection for evolution of high intelligence could lead to more identity between human and chimp than between human and orangutan.

Genetics. 1997 Dec;147(4):1497-507. Links
Exceptional convergent evolution in a virus.

Bull JJ, Badgett MR, Wichman HA, Huelsenbeck JP, Hillis DM, Gulati A, Ho C, Molineux IJ.
Department of Zoology, Institute of Cellular and Molecular Biology, University of Texas, Austin 78712, USA. bull@bull.zo.utexas.edu
Replicate lineages of the bacteriophage phiX 174 adapted to growth at high temperature on either of two hosts exhibited high rates of identical, independent substitutions. Typically, a dozen or more substitutions accumulated in the 5.4-kilobase genome during propagation. Across the entire data set of nine lineages, 119 independent substitutions occurred at 68 nucleotide sites. Over half of these substitutions, accounting for one third of the sites, were identical with substitutions in other lineages. Some convergent substitutions were specific to the host used for phage propagation, but others occurred across both hosts. Continued adaptation of an evolved phage at high temperature, but on the other host, led to additional changes that included reversions of previous substitutions. Phylogenetic reconstruction using the complete genome sequence not only failed to recover the correct evolutionary history because of these convergent changes, but the true history was rejected as being a significantly inferior fit to the data. Replicate lineages subjected to similar environmental challenges showed similar rates of substitution and similar rates of fitness improvement across corresponding times of adaptation. Substitution rates and fitness improvements were higher during the initial period of adaptation than during a later period, except when the host was changed.



Also on the same topic
Genetics, Vol. 181, 225-234, January 2009, Copyright © 2009
doi:10.1534/genetics.107.085225

Parallel Genetic Evolution Within and Between Bacteriophage Species of Varying Degrees of Divergence
Jonathan P. Bollback*,1 and John P. Huelsenbeck

* Department of Biology, Evolutionary Biology, University of Copenhagen, 2100 Copenhagen Ø, Denmark and Department of Integrative Biology, University of California, Berkeley, California 94720

1 Corresponding author: Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, King's Bldgs., W. Mains Rd., Edinburgh, EH9 3JT, United Kingdom.
E-mail: j.p.bollback@ed.ac.uk
Parallel evolution is the acquisition of identical adaptive traits in independently evolving populations. Understanding whether the genetic changes underlying adaptation to a common selective environment are parallel within and between species is interesting because it sheds light on the degree of evolutionary constraints. If parallel evolution is perfect, then the implication is that forces such as functional constraints, epistasis, and pleiotropy play an important role in shaping the outcomes of adaptive evolution. In addition, population genetic theory predicts that the probability of parallel evolution will decline with an increase in the number of adaptive solutions—if a single adaptive solution exists, then parallel evolution will be observed among highly divergent species. For this reason, it is predicted that close relatives—which likely overlap more in the details of their adaptive solutions—will show more parallel evolution. By adapting three related bacteriophage species to a novel environment we find (1) a high rate of parallel genetic evolution at orthologous nucleotide and amino acid residues within species, (2) parallel beneficial mutations do not occur in a common order in which they fix or appear in an evolving population, (3) low rates of parallel evolution and convergent evolution between species, and (4) the probability of parallel and convergent evolution between species is strongly effected by divergence.