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Tuesday, October 29, 2024

Zach Hancock's 10 most influential papers on evolution

Zach Hancock is a postdoc in the Dept. of Ecology and Evolutionary Biology at the University of Michigan. He has a popular YouTube channel where he has recently posted a video describing his top ten evolutionary biology papers of all time. I've added links to all of the papers below.

Zach emphasizes that this is a personal list and others might disagree with his choices. He is much more interested than I am in explaining the history of life with an emphasis on animals. I'm much more interested in molecular evolution so I would choose a slightly different list as I explain below. Please add your own choices in the comments.

  1. Force, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y. L., and Postlethwait, J. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics, 151(4), 1531-1545. [doi: 10.1093/genetics/151.4.1531]
  2. Coyne, J. A., and Orr, H. A. (1989) Patterns of speciation in Drosophila. Evolution, 43(2), 362-381. [doi: 10.1111/j.1558-5646.1989.tb04233.x]
  3. Lande, R., and Arnold, S. J. (1983) The measurement of selection on correlated characters. Evolution, 1210-1226. [doi: 10.2307/2408842]
  4. Lederberg, J., and Lederberg, E. M. (1952) Replica plating and indirect selection of bacterial mutants. Journal of bacteriology, 63(3), 399-406. [PDF]
  5. Gould, S.J. and Lewontin, R.C. (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London. Series B. Biological Sciences 205:581-598. [doi: 10.1098/rspb.1979.0086]
  6. Maynard Smith, J. M. (1974) The theory of games and the evolution of animal conflicts. Journal of theoretical biology, 47(1), 209-221. [doi: 10.1016/0022-5193(74)90110-6"]
  7. Fisher, R.A. (1918) The correlation between relatives on the supposition of Mendelian Inheritance. Proceedings of the Royal Society of Edingurgh [PDF]
  8. Hamilton, W. D. (1964) The genetical evolution of social behaviour. II. Journal of theoretical biology, 7(1), 17-52. [doi: 10.1016/0022-5193(64)90039-6]
  9. Kimura, M. (1968) Evolutionary rate at the molecular level. Nature, 217(5129), 624-626. [PDF]
  10. Wright, S. (1931) Evolution in Mendelian populations. Genetics, 16(2), 97. [doi: 10.1093/genetics/16.2.97]

I disagree with Hamilton (1964). I realize that there are many evolutionary biologists who think that kin selection and the evolution of altruistic behavior is extremely important1 but I think it's restricted to a tiny perecentage of characteristics in a tiny percentage of all living things on the planet. I would delete the Hamilton paper and replace it with ...

Margoliash, E. (1963) Primary structure and evolution of cytochrome c. Proceedings of the National Academy of Sciences, 50(4), 672-679. [PDF]

This is the first accessible paper on using the animo acid seqences of proteins to obtain information on evolution. It's the beginning of the field of molecular evolution and the idea of a molecular clock. Surely that deserves to be one of the most important advances in the field of evolution. (Linus Pauling and Emile Zuckerkandl published similar work on globins at about the same time but their original papers were not as accessible as the Margoliash paper. See Emile Zuckerkandl and the 50th anniversary of the birth of molecular evolution.)

I'm not a big fan of John Maynard Smith and game theory. I think it only applies to a small part of the field of evolution. I would delete the Maynard Smith (1974) paper and replace it with ...

Ohta, T. (1973) Slightly deleterious mutant substitutions in evolution. Nature 246:96-98. [doi:10.1038/246096a0]

This is the beginning of the nearly neutral theory. I agree that putting the Kimura paper on the neutral theory at #2 is a good choice but it's the Ohta paper that really drives home the idea that deleterious mutations can also be fixed under some circumstances and made (some) evolutionary biologists understand that natural selection was not the only game in town.

Finally, I'd like to see one of David Raup's papers in the top ten list but I don't know enough about the other papers to pick one to delete. (I'm skeptical of Lande and Arnold (1983) but I know they have fierce defenders.) Here's a candidate Raup paper that includes Sepkoski.

Raup, David M.; Sepkoski, J. John Jr. (1982) Mass extinctions in the marine fossil record. Science. 215 (4539). [doi:10.1126/science.215.4539.1501]

I'm waiting for the list of the top nine books on evolution—we all know what #1 is going to be.


Image credit: The photo is from Zach's personal website.

1. Richard Dawkins thinks Hamilton is "the greatist Darwinina of my lifetime" [quoted in W.D. Hamilton]

25 comments :

Muhammad Abdullah said...

I know what the no.1 book is going to be .... It's Lynch's The Origin of Genome Architecture, isn't it Larry ? :)

matts2 said...

I've read two of these. Including the game theory one that you want to remove. Based on my personal knowledge is clearly belongs on the list.

Mikkel Rumraket Rasmussen said...

Not sure where they belong in a list of the most important papers, but some honorable mentions in molecular evolution:

Zuckerkandl, E. and Pauling, L. (1965) "Evolutionary Divergence and Convergence in Proteins."

Eck RV, Dayhoff MO. Evolution of the structure of ferredoxin based on living relics of primitive amino Acid sequences. Science. 1966;152(3720):363-366. doi:10.1126/science.152.3720.363

Larry Moran said...

@matts2 Here's the way I look at it. The history of life encompasses more than three billion years of evolution and millions of extinct species. The modern world has about ten million species roughly grouped into five types: bacteria, protozoa, fungi, plants, and animals. Of these, the vast majority are single-cell organisms.

The most important results in evolution are the evolution of cells that contain efficient energy capture structures and complex metabolism. In the case of multicellular organisms, it's accompanied by the evolution of eyes, wings, leaves, and complex developmental processes. All of this can be explained by the fixation of alleles by drift and selection coupled to speciation.

It's not clear to me that game theory makes a significant contribution to our understanding of the history of life. It's only mentioned once in Futuyma's textbook. Why do you think it's so important?

The Rat said...
This comment has been removed by the author.
The Rat said...

Honourable mention to:
Darwin, C.R. (1859) On the Origin of Species, perhaps the most important book in the history of science.
Dave Bailey

Anonymous said...

Larry is perhaps again mislead by thinking that kin selection or game theory only matter when kin recognition or cognitive processes in general are possible. That is not the case at all. At the very least understanding the adaptive aspects of evolution would in many cases be impossible without a good understanding of frequency-dependent selection, which both game theory and kin selection are linked to. But of course if one focuses on the non-adaptive aspects of evolution, then Maynard Smith and Hamilton will both fall off the list almost by definition.

By the way, it should be Maynard Smith, J. M. (1974), not Smith, J. M. (1974).

I also think it's odd to include part 2 of Hamilton's 64 paper instead of part 1. It's certainly not true that part 1 is rarely cited as the video claims. If I am not mistaken, it is part 1 that is the most highly cited paper in Journal of Theoretical Biology.

gert korthof said...

Lynn Margulis ought to be on the list.
Margulis was the primary modern proponent for the significance of symbiosis in evolution. In particular. Lynn Margulis transformed and fundamentally framed current understanding of the evolution of cells with nuclei by proposing it to have been the result of symbiotic mergers of bacteria.
Throughout her career, Margulis' work could arouse intense objections, and her formative paper, "On the Origin of Mitosing Cells", appeared in 1967 after being rejected by about fifteen journals.
The descent of mitochondria from bacteria and of chloroplasts from cyanobacteria was experimentally demonstrated in 1978 by Robert Schwartz and Margaret Dayhoff. (quotes from wikipedia)

Larry Moran said...

@Anonymous No, I'm not "mislead" into thinking that kin selection is absolutely restricted to organisms that can recognize their siblings and cousins. I been discussing this for decades and I'm well aware of the fact that defenders of Hamilton can come up with extensions that cover other species.

I'm also aware of the importance of natural selection in spite of the fact that I'm trying to convince a skeptical public that there's more to evolution than adaptation. I'm also on a mission to convince the public that bacteria. algae, plants, fungi, and protozoa exist and they evolve.

My objection to the Hamilton paper is not that it's wrong or unimportant. It's that its importance to the overall field of evolution has been greatly exaggerated because of the intense narrow focus on adaptation (see #6) the evolution of big animals and their behavior.

Larry Moran said...

@gert korthof I agree that there should be a Margulis paper that deserves at least honorable mention. The problem with Lynn Margulis is that the original idea that chloroplasts and mitochondria originate from bacteria is sound but many of her other ideas were so strange that she's lost a lot of respect.

gert korthof said...

Thanks Larry. "The problem with X is..." (X= any famous scientist). Well, which scientist had produced only good hypotheses? For example James Watson: "Watson has repeatedly asserted that differences in average measured IQ between blacks and whites are due to genetics. ... his view that Africans are less intelligent than Westerners." (wikipedia).

Gerdien de Jong said...

Margulis (1967) gives a list of articles that already had proposed endosymbiosis. Not present is the work of Konstantin Mereschkowski, who seems to be the first one to have thought of it. She mentions Wallin (1927).
What is interesting is why the idea caught on after in 1967, but not earlier.

Anonymous said...

Hi Larry, you may have changed your mind. But you wrote "I'm still not clear on why a concept that mostly applies to animals with substantial brains is so important to all of evolutionary biology".
This is simply false. And kin selection is not about big animals anymore than population genetics is. Nor is there any need to come up with "extensions that cover other species".
I suspect you don't know what you are talking about.

Link to the above quote:
https://sandwalk.blogspot.com/2012/05/squirrels-dawkins-and-evolution.html

Larry Moran said...

@Anonymous If you are going to insult me then I'd rather you had the courage to identify yourself rather than hide behind an anonymous comment.

Larry Moran said...

@Anonymous Kin selection doesn’t come up in any of the aspects of evolution that interest me so it’s possible that I’m completely wrong about its importance. Perhaps you could mention one or two major discoveries that you attribute to kin selection?

Anonymous said...

My sincere apologies for the tone of my comment. My main point is that kin selection isn't about big animals or animals with developed brains and never has been, though many might think so. The same principles apply just as well to plants or microbes or ants. Should it be on the list? There will be some who will say 'of course', some who don't care, and some who think absolutely not. Its influence on evolutionary theory is nevertheless undeniable. Kin selection has also been tightly integrated with fixation probabilities and evolution in finite populations (François Rousset's book Genetic Structure and Selection in Subdivided Populations is an example). It isn't (at least for me) a separate branch of theory, but an integral part of it that builds on the work of Wright, Fisher and Haldane.

gert korthof said...

Larry, I just realized that Watson & Crick "Molecular Structure of Nucleic Acids: A Structure for Deoxyribose Nucleic Acid" Nature, 25 April 1953 is absent!!! It is not even listed on his 'Honorable mentions'.
Has nobody observed this remarkable omission? After Darwin there is no single other contribution that transformed biology and evolution. It made biology into an modern and exact science. Nothing would be the same in biology after 1953. The publication should absolutely be #1 on his list without doubt!

gert korthof said...

Gerdien, why the idea caught on after in 1967? Maybe there must be a number of failed attempts to convince scientists in the field of a new revolutionary idea, each publication with little bits of good evidence mixed with irrelevant and wrong ideas, before somebody makes a synthesis of all the right and relevant ideas into a coherent theory.
Compare: Darwin's idea of evolution. Darwin had his predecessors contributing a mix of immature, wrong and incomplete pieces of the puzzle. Darwin subsequently made the synthesis of the right pieces in to a convincing and coherent theory.

Larry Moran said...

@Anonymous Excuse my ignorance but I'm still having trouble understanding the importance of kin selection. I deal with the effect of drift and selection at the molecular level all the time and I've never had to evoke kin selection to explain the results. Can you give me a more specific example of its use?

Kin selection is barely mentioned in any of the genetics or evolution textbooks on my shelves. Is that because I have an unusual selection of such textbooks or is it because they are wrong?

Anonymous said...

Hi Larry, That's ok. I am not saying it needs to be on your list. But a big brains/big animals/narrow applicability argument is not a good argument because it's not really true. The use of kin selection is purely in understanding adaptation, so it probably isn't on your radar. My point about finite populations/drift/fixation etc is that the seemingly different theoretical fields are not totally disconnected.

Textbooks: no idea. Many mention it, but sounds like many do not. Do you think textbook citations carry more weight than overall citations in research papers? I'm not sure what to think of that myself.

Larry Moran said...

@Anonymous said, "The use of kin selection is purely in understanding adaptation ..."

Can you give me some specific examples of using kin selection to understand adaptation examples in protozoa, fungi, and plants?

Anonymous said...

Here are some examples:
https://www.pnas.org/doi/10.1073/pnas.2119070119
https://pubmed.ncbi.nlm.nih.gov/21682642/
https://pmc.ncbi.nlm.nih.gov/articles/PMC9624078/
https://besjournals.onlinelibrary.wiley.com/doi/pdf/10.1111/1365-2435.12121
https://www.nature.com/articles/s41467-018-04378-3
https://academic.oup.com/jxb/article/61/15/4123/435398
https://pubmed.ncbi.nlm.nih.gov/38577983/
https://www.nature.com/articles/35050087


You might also find this interesting:
https://www.cell.com/current-biology/pdf/S0960-9822(07)01500-X.pdf





Anonymous said...

I checked both on the journal website and on web of science, and "The genetical evolution of social behaviour. I". has thousands more citations than "The genetical evolution of social behaviour. II.". So here the video seems mistaken when it states that part II is much more commonly cited (not that this changes much otherwise). I cannot find a proper record of part I on Google Scholar, perhaps that is a reason for the misunderstanding.

Larry Moran said...

@Anonymous Thank-you for the references. It gives me a much better understanding of how kin selection is being used to support ideas about selection and adaptation in a variety of species.

matts2 said...

I thought I was clear. I know something about game theory. Just like the G&E paper is important because I read it.

Did you think I was making a comment about the work of scientists? I might, but not in this case.

I am a bit surprised that game theory isn't more important. It is a fundamental innovation in how we look at things. I don't know enough detail of the work to say it is important.