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Nancy A. Moran ‐ Recipient of the 2017 Molecular Ecology Prize

2018; Wiley; Volume: 27; Issue: 1 Linguagem: Inglês

10.1111/mec.14447

1365-294X

David C. Queller,

Insect-Plant Interactions and Control

Nancy A. Moran has made numerous pioneering contributions to the biology of interspecies interactions, especially the symbioses of homopteran insects and the bacteria that live inside their cells. She has painted a dazzling picture of some of nature's most intimate mutualisms, using a palette of methods from experimental biology, molecular biology, phylogenetics, genomics, molecular evolution and evolutionary theory. Nancy was born 31 December 1954. Her father ran a drive-in movie theatre in Dallas, Texas (adults 44 cents!), supporting a brood that would reach eight in number. She attended the University of Texas at Austin and published her first paper there with Nancy Burley, on pigeon mate preferences (Burley & Moran, 1979). I first met Nancy right at the beginning of our graduate careers at the University of Michigan when we were assigned to the same office. It was immediately obvious that she was sharp, but perhaps less obvious that she would be the very sharpest in our programme's collection of pretty sharp tacks. We were extraordinarily fortunate in our exposure to recent developments in evolutionary biology. Richard Alexander offered a must-take class on social evolution, and in our first 3 years, we had semester-long visits from three giants of the field: John Maynard Smith, William Hamilton and George Williams. All taught a graduate seminar or actually two seminars to meet the demand. Williams had recently written a book on the evolution of sex. Maynard Smith was writing one, and Hamilton was at the career cusp that separated his early work on kin selection from his later focus on sex. Nancy picked up on this theme, at least in the short term. She set out to do a thesis on the topic, supervised by Hamilton (who had returned to Michigan) and Alexander, using aphids and their mix of asexual and sexual cycles. In the end, her thesis ended up largely following other interesting aspects of the biology that her system presented, for example, the relationships between the aphids and their host plants (Moran, 1981). After her PhD and a short stint in Czechoslovakia as an NAS exchange fellow, Nancy settled at the University of Arizona, aided (?) by a glowing letter from Bill Hamilton that, however, described her clumsily as “exceptionally strong on the theoretical and statistical side and with an ability especially remarkable in view of her sex.” There she continued working on aphids and their hosts, including working up new angles on the evolution of alternative phenotypes, both with respect to aphid life cycles (Moran, 1992a) and then in an influential general mathematical model (Moran, 1992b). Nancy's research took a new and important direction when, in collaboration with Paul Baumann, she again began pursuing a fresh angle that her aphid system presented. Aphids feed on phloem, which lacks important nutrients, and they were known to harbour endosymbiotic bacteria, notably Buchnera, that might be helping make up for this lack. Nancy's research on these symbionts, once started, bloomed in multiple directions (Moran, McCutcheon, & Nakabachi, 2008). She showed, using molecular phylogenetics and fossils, that some of these relationships were ancient, going back a hundred million years and more (Moran, Munson, Baumann, & Ishikawa, 1993). Some, like Buchnera, show matching phylogenies and long-term co-speciation with their hosts (Thao et al., 2000). These patterns suggested that these endosymbionts were transmitted vertically like mitochondria and chloroplasts and that, like those organelles, they likely were an important source of evolutionary novelty responsible for host success. Nancy's work also helped reveal how the symbionts contributed to host success. The symbionts often supply amino acids and vitamins to their hosts, sometimes even dividing labour among multiple symbiont species supplying exactly complementary sets of these nutrients (McCutcheon, McDonald, & Moran, 2009). Buchnera genes also affect thermal tolerance of their hosts (Dunbar, Wilson, Ferguson, & Moran, 2007), and genes of the facultative endosymbiont Hamiltonella promote defence against parasitic wasps (Oliver, Russell, Moran, & Hunter, 2003). Even as the Buchnera evolved such intimate relations with their hosts, their evolution has a darker side. Buchnera's genome, and those of other obligate endosymbionts, is greatly reduced in size, is very AT-biased and evolves very rapidly. Many genes are lost, and it was assumed they had become superfluous in their cozy host environment. Nancy proposed an alternative explanation in which coziness is not a good thing; rather than being primarily adaptively streamlined, these genomes are degraded and maladapted (Moran, 1996). This follows from a lifestyle involving small, bottlenecked, clonal populations with ample opportunity for genetic drift and scant opportunity for meaningful recombination. Under these conditions, obligate endosymbionts undergo the process known as Muller's ratchet—the steady fixation of deleterious mutations that cannot generally be restored. This explains not just the loss of genes but also the increase in AT content via mutation bias and rapid rate of evolution (not directional selection but drift!). This explanation, widely supported by later research (e.g., Bennett & Moran, 2015; McCutcheon & Moran, 2012; Moran et al., 2008), brought Nancy's work back full circle to the topic of the evolutionary advantages of sex and recombination. This detailed understanding of host and associated microbe can be contrasted with the current flurry of work on host microbiomes. This connection was not lost on Nancy, and she began a new productive line of microbiome research. But instead of leaping into the formidable complexities of the human gut microbiome, she is working with a much more tractable model system: honey bees. Bees have a smaller, more dedicated microbiome. She found that it is dominated by only nine clusters of species similar in 16S rDNA (Moran, Hansen, Powell, & Sabree, 2012). However, genomic analysis shows that these species can be quite divergent in gene content and it reveals some of the complementary metabolic capabilities (Engel, Martinson, & Moran, 2012; Kwong, Engel, Koch, & Moran, 2014). All of them can be cultured and used to inoculate germ-free bees. Additional work is revealing routes of host colonization, variation with age and caste of host, and disruption of the microbiome by antibiotics (Kwong & Moran, 2016). Work on this and other simple microbiomes has great promise to reveal general principles applicable to more complex systems. The Molecular Ecology Prize we are celebrating here is thoroughly deserved, but a bit late to the game. Nancy has received numerous accolades during her career at Arizona, Yale University, and the University of Texas. She has been awarded a Macarthur Fellowship and the International Prize for Biology and is an elected member or fellow of the National Academy of Sciences, the American Academy of Arts and Science and the American Association for the Advancement of Science. Her contributions to a wide variety of fields are reflected in her being a member of the American Academy of Microbiology, a fellow of the Entomological Society of America and the recipient of two lifetime achievement awards, the James Tiedje Award for microbial ecology, and the Motoo Kimura award molecular evolution. Nancy Moran has shown how much great science can be performed by applying a wide range of methods to focused questions. In this, she was aided by a formidable group of graduate students, postdocs and collaborators. In following her aphid organisms to new questions, she unveiled in endosymbiont genomes what is perhaps the most compelling and comprehensive story of adaptation gone bad. Then by reversing course and following her questions to appropriate new organisms (bees), she is revealing principles underlying the great mysteries of microbiomes.