In a paper published in the Annual Review of Ecology and Systematics in 1987, John Avise, Jonathan Arnold, Martin Ball, Eldredge Bermingham, Trip Lamb, Joseph Neigel, Carol. A. Reeb and Nancy C. Saunders highlighted the value of mitochondrial DNA in bringing phylogenetic thinking into population genetic studies, and laid the foundation for the birth of phylogeography. Twenty-nine years after the paper was published, I asked John Avise about the making of this paper, the origins of his interest in evolution and genetics, and the progress that phylogeography has made in this period.
Citation: Avise, John C., Jonathan Arnold, R. Martin Ball, Eldredge Bermingham, Trip Lamb, Joseph E. Neigel, Carol A. Reeb, and Nancy C. Saunders. “Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics.” Annual review of Ecology and Systematics 18, no. 1 (1987): 489-522.
Date of interview: Questions sent by email on 11th December 2016; responses received by email on 13th December 2016
Hari Sridhar: I would like to start by asking you what your motivation was to write this paper. When did you start thinking about the need to link population genetics and systematics? Also, how and when did you discover the value of Mitochondrial DNA?
John Avise: The immediate impetus to write this paper came about as follows: for nearly ten years, I had been writing numerous papers about mtDNA genealogies in conspecific populations of various vertebrate species. In paper after paper, I had been forced to use cumbersome phrases to encapsulate our observations. For example, I would write sentences such as “There clearly is a strong geographic orientation to the matrilineal genealogies in this species.” I needed a simpler word or phrase to convey such sentiments. That’s when I thought of the word “phylogeography”. After the word was coined in my 1987 paper, I could thereafter simplify everything by stating that there was a clear phylogeographic pattern in each dataset. Furthermore, just by coining the word, I was motivated to think more clearly about what would henceforth be recognized as phylogeographic principles, patterns, and processes. My initial attempt at this emerging framework was the subject of that 1987 paper.
Throughout my graduate training in the early 1970’s I had been dismayed by the fact that systematists (phylogeneticists) and population geneticists seemed to speak very different languages, and had little meaningful contact or communication. This seemed to me to be highly ironic because microevolution (evolution at the intraspecific level) and macroevolution (evolution above the species level) must, in truth, be relatable segments along a genealogical continuum (because, in any generation, each organism has parents who in turn had parents and so on going back in time). So I had always been primed to want to discover some way to draw meaningful connections between the formerly separate disciplines of population genetics and phylogenetics.
I had begun to discover the value of mtDNA in the late 1970’s, as elaborated in a response to a question below.
HS: Stepping back a bit, could you share with us how you got interested in evolution and genetics?
JA: Since early childhood, I have always had a keen interest in nature and natural history. These interests seemed to come from the heart. By contrast, my interest in genetics was an acquired taste that seems to be harbored in my mind. That interest in genetics stems from my early training in graduate school, which began at the University of Texas in 1970. Throughout my career, a consistent theme has been to try to wed the fields of genetics and natural history.
HS: This paper has eight authors, all of whom share one common affiliation. How this group came together to write this paper and what did each author bring to this work?
JA: With the exception of Jonathan Arnold (who was a collaborating statistician in my department, all of the other authors were my graduate students or lab technicians who at one time or another had worked on various lab projects. I conceived and wrote the paper entirely myself, and then added these other authors essentially as a thank-you or courtesy (and/or to help further their careers).
HS: You acknowledge “Dr. Bob Lansman for introducing [you] to mitochondrial DNA”. Could you tell us who Dr. Lansman was and how you knew him?
JA: Lansman was a faculty member in the Biochemistry Department at the University of Georgia, which was housed in the same building as my Genetics Department. One day in about 1977, I went to Bob to ask whether I might work in his lab for a brief time to learn restriction enzyme digestion techniques. Restriction enzymes had just recently been discovered, and I thought they might offer a means by which to study regulatory genes (perhaps encoded by repetitive DNA) in the nuclear genome. Bob welcomed me into his lab, but emphasized that he had little or no experience with nuclear DNA, but instead was interested in the biochemistry and physiology of mitochondria. Soon we found ourselves doing restriction digests of mtDNA (for example, in mice and gophers that I had been studying). The results were so fascinating that I quickly jettisoned my idea of studying nuclear regulatory genes, and instead switched almost all of my attention to mtDNA.
HS: Would you remember how long it took you to write this paper, and where and when you did most of the writing? How did the other authors get involved in the writing?
JA: It took about one month to write the paper, which I did in my office at UGA.
HS: Did this paper have a relatively smooth ride through peer review? How did you decide to submit this to AROES?
JA: Yes, this paper breezed through the review process (an extremely rare occurrence in my career-long experience with publishing papers). The journal was called ARES (Annual Review of Ecology and Systematics) at that time and it seemed an obvious choice for such a review paper.
HS: At the time it was published, did this paper attract a lot of attention and discussion?
JA: Yes, definitely.
HS: This paper has been cited over 3000 times. At the time you wrote it, did you anticipate at all that it would have such a huge impact on the field? Do you have a sense of what it mostly gets cited for?
JA: I think the paper is now remembered as representing the formal birth of the field of phylogeography. Of course I couldn’t have fully anticipated this at the time, but I did certainly have a sense that it had the potential to become a landmark treatise.
HS: Did this paper have any kind of direct impact on your career?
JA: Yes, most definitely. For example, within a few years (in 1991), I was elected into the National Academy of Sciences, no doubt in large part because of my decade-long application of mitochondrial DNA (among other molecular markers) to the development of the fields of phylogeography and evolutionary genetics.
HS: In what way did it influence the future course of your research? Does phylogeography continue to be an important area of research in your lab?
JA: In terms of technology, there have been at least three main stages to my career. In the 1970’s and early 1980’s, I had been near the ground floor of the allozyme revolution in population genetics. In the late 1970’s and continuing into the early 1990’s, much more of my attention turned to mtDNA and phylogeography. This probably culminated with my publication in 2000 of my textbook “Phylogeography: the History and Formation of Species” by Harvard University Press. However, by the late 1990’s I had already turned increased attention to animal mating systems as deduced using microsatellite markers. Today, I continue to use mtDNA and microsatellites in conjunction to address phylogeographic and natural history topics in a wide variety of vertebrate and invertebrate animals.
HS: At the end of your paper you say “Study of intraspecific phylogeography should assume a place in evolutionary biology at least commensurate with that of ecogeography, with mutual benefit resulting to both disciplines. Theories of speciation and macroevolution must now recognize and accommodate the reality of phylogeographic differentiation at the intraspecific level.”
Today, almost 30 years later, to what extent has this happened? Are you satisfied with the progress that has been made?
JA: My hopes have been met to a great degree. Indeed, phylogeography today is a household word in genetics, and its concepts and principles have been so thoroughly incorporated into evolutionary biology as to constitute standard accepted wisdom. I sometimes think that students today must think that population genetics and phylogenetics had always been fully integrated. I am pleased and gratified that my efforts have contributed to this outcome.
HS: Could you reflect on the role/importance of Mitochondrial DNA in phylogeography today? Also, what are the developments in techniques, subsequent to this paper, that have surprised you the most?
JA: As I have emphasized throughout my career, matrilineal genealogies as registered by mtDNA constitute only a minuscule fraction of the total hereditary history of any sexual species. Today, in the genomics era, scientists are beginning to mine the wealth of genealogical information that is ensconced within the nuclear genome. Nonetheless, mtDNA is and will continue to be an especially powerful genealogical marker due to its asexual (non-recombining) mode of transmission and its rapid pace of nucleotide sequence evolution.
HS: If you were to rewrite this paper today, would you make any changes to Figure 4 (p. 501)? Any new categories you would include or would you organise this differently?
JA: No, I wouldn’t make any changes. It covers the range of possibilities (but I also don’t think it’s a particularly key feature of the paper).
HS: Towards the end of the paper you identify a set of ‘Phylogeographic Hypotheses’. Could you reflect on the extent to which these have been taken up by the research community for empirical work? Also, today, would you still consider these to be the most important hypotheses to test?
JA: I think these hypotheses have offered a highly useful map and foundation for phylogeographic research. In particular, principles of genealogical concordance have served the field well and been a conceptual beacon for efforts to translate genomic information into robust conclusions in systematics, population genetics, and taxonomy.
HS: In the 30 years since this paper was published, have you ever read it again? If yes, in what context? What strikes you most about it when you read it now?
JA: Yes, I have reread it occasionally, including for this interview. If I may be a bit immodest, I am still amazed by this paper and the impact it has had on evolutionary biology. I am very proud of it.
HS: Would you count this as one of your favourites, among all the papers you have published?
JA: I recognize that it has been among the most conceptually impactful of my papers, but there are many other papers that I am equally or more fond of for a great variety of reasons. Your question is a lot like asking who the favorite among one’s many children is.
HS: What would you say to a student who is about to read this 30-year old paper today? What should he or she take away from it? Would you add any caveats?
JA: I would ask them to think about its importance in an historical context. What they should take from it is that it built long-lasting conceptual and empirical bridges between two formerly disconnected evolutionary arenas.