Profile of Nancy A. Moran ‘‘ always liked insects,’’ says Nancy A. bination,’’ she says. ‘‘Why have males Moran, Regent’s Professor of Ecol- and females, and not just reproduce by ogy and Evolutionary Biology at parthenogenesis and have all females?’’ the University of Arizona (Tuc- One of her advisors, William Hamilton, son,I AZ). ‘‘As a little kid, I was known had proposed that sexual reproduction as the girl who collected insects and had was important to create genetic diversity them in jars and things like that.’’ Years to stay one step ahead of coevolving later, this youthful bug collector has be- natural enemies, especially parasites and come a renowned entomologist whose pathogens. ‘‘I became interested in that work crosses over into multiple disci- idea and began looking at it in aphids,’’ plines, including microbiology, ecology, she says, ‘‘which are very useful since and molecular evolution. Moran’s re- they are parthogenetic for part of their search primarily focuses on the ecology life cycle’’ (3). and evolution of aphids and, since 1990, After receiving her Ph.D. in zoology has especially focused on the interaction in 1982, Moran spent the next several and coevolution of these small insects years studying evolutionary ecology in and the symbiotic bacteria that live in- aphids. ‘‘It was less than completely side of them. satisfying in a lot of ways,’’ she admits. ‘‘The whole evolution of insects has ‘‘At that time you were so far from the been in tandem with these bacteria,’’ actual genetic basis of the variation you Moran says. ‘‘We would not see insects were looking at, so you had no handle feeding on plant sap if it weren’t for as to which genes were actually causing symbiosis.’’ Elected to the National Nancy A. Moran the variation. Everything was like a Academy of Sciences in 2004, Moran black box.’’ Moran carried out this chal- lenging research in postdoctoral studies reveals another level in this symbiont– tion for a while,’’ she says. ‘‘I started out at Northern Arizona University (Flag- host relationship in her Inaugural Arti- as an art major, and then I switched staff, AZ), followed by a faculty ap- cle in this issue of PNAS (1). She shows over to a philosophy major.’’ Then, one pointment at the University of Arizona that in Hamiltonella defensa, a bacterium semester, she enrolled in an introduc- in 1986, where she has remained since. that helps protect aphids against para- tory biology course, initially just to com- sitic wasps, the toxin genes that provide plete an elective. ‘‘They used the famous Old Association and a New Collaborator defense are embedded within phage ge- Keeton textbook [Biological Science], Shortly after arriving at Arizona, Moran nomes. Because the phages have vari- which I thought was really good,’’ she began to work on a side project examin- able genomes, the bacteria have evolved recalls. ‘‘Basically just from reading that ing a local aphid species, Melaphis rhois. multiple isolates containing different book as much as anything else—I don’t ‘‘This aphid has a very peculiar life cy- toxins. ‘‘The phages are a very dynamic even really remember the lectures—I cle, just extremely weird,’’ she explains. part of the symbiont genome,’’ she says, became interested in biology and took ‘‘For part of its life cycle it forms this ‘‘and form an integral component of the several more classes.’’ complex gall, or plant tissue deforma- aphid–bacterium mutualism.’’ During her senior year at college, tion, on a species of sumac. Then, in when she undertook an honors project other part of the cycle, it feeds on Movies and Books to complete her Plan II requirements, mosses. So during the course of its life, Despite her early career as a budding Moran decided to try something in biol- it has to migrate from one plant to the entomologist, when she was young, Mo- ogy. ‘‘I happened to take a class on next.’’ Initially, Moran thought this ran never envisioned becoming a scien- animal behavior. The TA was Nancy behavior could be a complex adaptation tist. Born and raised in Dallas, TX, no Burley, who would later become well to changing seasons, but M. rhois was one in her family was an academic, and established in bird behavior, and I did found to have sister aphid species living she encountered no pressures or expec- a project with her on mate choice in in China and Japan. ‘‘The only way you tations to pursue science. In fact, she pigeons’’ (2). The project solidified an could explain this distribution is that it’s did not find her private school biology interest in evolution and behavior for very, very ancient,’’ she says. In fact, the class particularly interesting. Moran Moran and gave her a taste of what in- life cycle dated back at least 50 million actually grew up surrounded more by dependent research could be like. Thus, years, at a time when sumac was dis- science fiction than science fact—her she decided to apply to graduate school. persed across the Bering land bridge father, Robert Moran, ran a local ‘‘It was all sort of last minute, so I and was present in both the Asian and drive-in movie theater, and Moran and wasn’t at all in the know about any- North American continents, making it her seven siblings spent a lot of time thing,’’ she says. ‘‘I asked the people the oldest known continuous association helping out with the family business. around me for advice on where to ap- between an insect and a plant (4). Moran began her undergraduate stud- ply, and they named some places, and I ‘‘Anyway, I didn’t think this paper was ies at the University of Texas (Austin, eventually ended up at the University of a big deal, and I was going to publish it TX) in 1972. She enrolled in an honors Michigan (Ann Arbor, MI).’’ She gradu- in some tiny little journal, if at all,’’ she program known as Plan II, which al- ated from the University of Texas with explains. But one of Moran’s colleagues lowed students to create their own flexi- a bachelor’s degree in biology in 1976. ble academic plan. This option was ideal When Moran arrived at Michigan that

for Moran, who found almost every year for graduate school, her exact re- This is a Profile of a recently elected member of the National study field interesting. ‘‘There were so search goals were up in the air. ‘‘At that Academy of Sciences to accompany the member’s Inaugural many interesting subjects that I didn’t time, a lot of people were interested in Article on page 16919. even settle down in one particular direc- the evolution of sex and genetic recom- © 2005 by The National Academy of Sciences of the USA

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suggested that she send her paper to the journal Science, because the ancient aphid–plant association seemed like an interesting discovery. ‘‘And so I did, and they published it,’’ she says, ‘‘and the good thing about that was that Paul Baumann at [University of California] Davis, a well known molecular geneticist who was interested in bacterial diversity, saw the paper and called me up. He said he would like to work with some- one who knew something about aphids because he was interested in the bacte- ria that live in [them].’’ So, in 1990, Mo- ran and Baumann began what would become a continuous collaboration spanning 15 years and numerous grant proposals, getting to the heart of the mutualistic relationship between aphids and their tiny bacterial guests. Their first collaborative project in- volved reconstructing the evolutionary history of the primary aphid symbiont, Buchnera aphidicola. Moran and Bau- mann compared the 16S rRNA se- Moran collecting psyllid galls, containing bacterial symbionts, on the University of Arizona campus. quences from 11 different aphid species ‘‘back when sequencing one 16S was considered an accomplishment,’’ says derwent accelerated evolution compared cant because Moran and Ochman would Moran, and found an ancestral relation- with related free-living bacteria (8). later marry, this encounter also shifted ship between insect and bacteria (5). Therefore, these symbionts accumulated the course of Moran’s research. ‘‘The associations with these bacteria go mutations that eventually knock certain Moran was curious about the second- all the way back to the origins of those genes out. ‘‘So while part of the reduc- ary, or facultative, bacterial symbionts groups of animals,’’ she says, ‘‘and the tion is due to adaptation, a lot of it just often present in insects. Unlike primary two have coevolved such that basically reflects genetic drift,’’ she explains.‘‘ It’s symbionts, which provide essential nutri- when the insects speciate and diversify, just a consequence of long-term evolu- ents, these secondary symbionts were you get this parallel diversification of tion in a restricted environment with both horizontally and vertically transmit- the bacteria.’’ Moran and Baumann next small population sizes.’’ ted, were not essential for host survival, demonstrated that this symbiotic coevo- and conferred no known benefits. These lution was not limited to aphids but was symbionts could, however, prove to be present among other insect species (6, ‘‘I’ve always had a valuable research models because they 7). ‘‘As we were doing this, I sort of represented a more recent stage of a gradually became interested in bacterial research theme of host–symbiont relationship. ‘‘These sym- genome evolution,’’ she says, ‘‘especially bionts resemble bacterial pathogens in a the back-and-forth between the genome biological complexity lot of ways,’’ says Moran. ‘‘I mean, from evolution of the symbiont and the ecol- the host point of view, the outcome can ogy of the host and how that affects the and how it came to be.’’ be different, but these bacteria have to symbiont. And a lot of interesting pat- invade a host, get into a cell, and then terns show up in these symbionts.’’ influence the host’s biology, even if they One of the most compelling charac- Opportunity to Study Opportunists do it to help the host.’’ Of course, how these facultative teristics of these symbionts is their small Moran’s groundbreaking work on bacteria helped the host was largely genome size. ‘‘Buchnera only have 600 bacterial symbiosis would earn her the genes, compared to about 4,000 or 5,000 unknown, but together with Martha honor of receiving one of the annual for E. coli,’’ says Moran. ‘‘This is a re- Hunter and graduate student Kerry MacArthur ‘‘genius’’ grants in 1997. Al- curring pattern in the genomes of both Oliver, Moran demonstrated that in though the award itself was exciting, the bacterial symbionts and pathogens, but aphids, secondary symbionts helped why do they get so small?’’ Two reasons monetary award that came with it was confer resistance to attacks by parasitic were the loss of genes that were no also a blessing. ‘‘I was able to use that wasps, and that different isolates of bac- longer needed in the host environment to pay some of my salary so I didn’t teria conferred varying degrees of pro- and the lack of opportunity for these have to take on a full teaching load for tection (9, 10). Unfortunately, another symbionts to pick up additional genes a year or two,’’ she says, ‘‘and that gave key difference between primary and sec- through horizontal transfer. By compar- me more free time for my research and ondary symbionts was that secondary ing the Buchnera with some free-living to have more time with my child.’’ That symbionts were not localized within spe- bacteria, Moran identified a third rea- same year, Moran attended the Gordon cialized host organs and were present in son: she observed that Buchnera genes Conference in Microbial Population Bi- very low amounts. Therefore, character- tended to accumulate more nonsynono- ology and met Howard Ochman, a mo- izing the genomic content of these sym- mous mutations and amino acids with lecular geneticist at the University of bionts, as well as the mechanisms of codon families rich in A ϩ T base pairs, Rochester (Rochester, NY). Although how they confer resistance, was ex- which indicated that the symbionts un- this meeting would prove most signifi- tremely difficult. Ochman, however,

Zagorski PNAS ͉ November 22, 2005 ͉ vol. 102 ͉ no. 47 ͉ 16917 Downloaded by guest on September 26, 2021 happened to be investigating a method Moran hopes to continue conducting Having doubts about the importance for amplifying whole-genome DNA from further research on these opportunistic of natural selection as the sole force low-copy templates and was looking for symbionts in both aphids and other in- important in evolution could be another potential applications. In a previous col- sect species. ‘‘Some insect groups have theme, and, to that end, Moran has laboration with Ochman and Colin Dale very elaborate systems of symbiosis lately been intent on educating biolo- using directed PCR, Moran had shown where they can have up to six different gists on the roles of genetic drift and that a facultative symbiont within grain bacterial symbionts at once in the same historical happenstance in evolution. weevils expressed homologs of the inv͞ insect, and it seems that in these cases ‘‘It’s always made me kind of uneasy spa genes, components of a secretion the different symbionts are actually de- that you would just start with the as- system used by bacterial pathogens like pendent on each other,’’ she says. ‘‘You sumption that organisms are well Salmonella to invade cells (11). Because have reductions in the metabolic capa- adapted and perfectly suited to their Moran wanted to know what other in- bilities in one symbiont because it be- environment,’’ she says, ‘‘so I always teresting genes might be present within comes dependent on another symbiont, give little sections on genetic drift when symbionts, she and Ochman decided and you can end up having a set of I talk about my work. It’s tempting just that secondary symbionts would make a organisms, all of which have to live to- to skip over it, because outside of popu- good test case for his DNA amplifica- gether. So it adds a layer of complexity lation geneticists, people don’t think tion technique. to this community.’’ about it much and don’t really want to In her PNAS Inaugural Article (1), think about it.’’ Moran utilized Ochman’s method and Importance of Randomness But she thinks an improved understand- ing of genetic drift and random chance found that facultative symbionts of ‘‘I’ve always had a research theme of could help prevent the misunderstandings aphids do indeed have additional genes biological complexity and how it came surrounding evolution. ‘‘I think part of the associated with pathogenesis, including to be,’’ says Moran. Recently, Moran problem in teaching evolution is that peo- toxin genes. ‘‘And when you look at dif- has continued to increase the complex- ple are used to thinking of everything as ferent bacterial isolates,’’ she says, ‘‘they ity of her work by venturing away from adapted while ignoring chance events,’’ have different toxins. Some have ho- insect symbionts and increasing her fo- she says, adding that molecular biology is mologs of the shiga toxin, others have cus on bacterial evolution as a whole, often taught like so-called intelligent de- cytolethal distending factor, and some another influence partially attributed to sign. ‘‘It’s like this binds here, that binds have other unknown genes.’’ Moran Ochman. Along with Vincent Daubin, there, it’s all complicated and yet some- suggests that these toxins are targeted Moran and Ochman recently picked how it all works,’’ she says. ‘‘If more peo- against the eggs laid by parasitic wasps, their way through the morass of lateral ple thought about mutation, genetic drift, and the degree of resistance varies due gene transfers that occur between differ- and population processes as important to the differing toxic mechanisms: ent bacterial species and built a phyloge- aspects of evolution, I think the under- ‘‘Depending on the local ecology, netic tree for bacteria in the Escherichia standing of evolution would be better.’’ selection might favor one type over coli family, a feat many researchers another type.’’ thought unattainable (12). Nick Zagorski, Science Writer

1. Moran, N. A., Degnan, P. H., Santos, S. R., 5. Munson, M. A., Baumann, P., Clark, M. A., Bau- 9. Oliver, K., Russell, J., Moran, N. & Hunter, M. Dunbar, H. E. & Ochman, H. (2005) Proc. Natl. mann, L., Moran, N. A., Voegtlin, D. J. & Camp- (2003) Proc. Natl. Acad. Sci. USA 100, 1803– Acad. Sci. USA 102, 16919–16926. bell, B. C. (1991) J. Bacteriol. 173, 6321–6324. 1807. 2. Burley, N. & Moran, N. (1979) Anim. Behav. 27, 6. Munson, M., Baumann, P. & Moran, N. (1992) 10. Oliver, K., Moran, N. & Hunter, M. (2005) Proc. 686–698. Mol. Phylogenet. Evol. 1, 26–30. Natl. Acad. Sci. USA 102, 12795–12800. 3. Hamilton, W. D., Henderson, P. A. & Moran, N. A. 7. Clark, M. A., Baumann, L., Munson, M. A., Baumann, 11. Dale, C., Plague, G., Wang, B., Ochman, H. & (1980) Natural Selection and Social Behavior: Recent P., Campbell, B. C., Duffus, J. E., Osborne, L. S. & Moran, N. A. (2002) Proc. Natl. Acad. Sci. USA 99, Research and New Theory, eds. Alexander, R. D. & Moran, N. A. (1992) Curr. Microbiol. 25, 119–123. 12397–12402. Tinkle, D. W. (Chiron Press, New York), pp. 363–382. 8. Moran, N. A. (1996) Proc. Natl. Acad. Sci. USA 93, 12. Daubin, V., Moran, N. A. & Ochman, H. (2003) 4. Moran, N. A. (1989) Science 245, 173–175. 2873–2878. Science 301, 829–832.

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