PROFILE Profile of Brian Charlesworth Jennifer Viegas my future wife, Deborah Maltby, there. We Science Writer owe a huge amount to each other intellectually, and much of my best work has been done in ” National Academy of Sciences foreign asso- later moved to London, but Charlesworth’s collaboration with her, says Charlesworth. ciate Brian Charlesworth has been at the interest in nature remained. Charlesworth continued his studies at forefront of evolutionary genetics research for At age 11, he entered the private Haber- Cambridge, earning a PhD in genetics in 1969. the last four decades. Using theoretical ideas dashers’ Aske’s Boys’ School, which he at- This was followed by 2 years of postdoctoral to design experiments and experimental data tended on a local government scholarship. work at the University of Chicago, where “ as a stimulant for the development of theory, “It had well-equipped labs and some very Richard Lewontin served as his adviser. He Charlesworth investigates fundamental life good teachers,” Charlesworth says. He read was a wonderful role model, with a penetrat- processes. His work has contributed to im- extensively, visited London museums, and ing intellect and a readiness to argue about ” “ proved understanding of molecular evolution attended public lectures at University Col- almost everything, Charlesworth says. Ihave and variation, the evolution of genetic and lege London. His early role models were probably learnt more about how to do science ” sexual systems, and the evolutionary genetics physics and biology teacher Theodore Sa- from him than anyone else. Population of life history traits. In 2010, Charlesworth vory and biology teacher Barry Goater. He genetics pioneer James Crow was another retired from his faculty position as professor says, “The notion of discovering how the guiding influence. ’ at the University of Edinburgh’s Institute of natural world works, purely from observa- Charlesworth s first teaching position, from Evolutionary Biology but actively continues to tion and reasoning, thrilled me from an 1971 to 1974, was as a lecturer in genetics at inspire students and conduct research. early age and continues to do so.” the University of Liverpool. His research at thetimeprimarilyinvolvedmodelinghow An Early Love of Nature Applying Mathematics to Evolutionary natural selection works in populations with Until age 8, Charlesworth lived near the Genetics age structure (1), in which mating occurs English seaside in Hove, East Sussex. There, In 1966, Charlesworth earned a BA in natural among individuals of different ages. he explored marine life in rockpools, studied sciences with honors at the University of The models provided a foundation for snails collected from a bombsite, admired a Cambridge. During his final year at the uni- evolutionary theories of life history patterns, giant tortoise that lived in a garden behind versity, he studied genetics and soon became especially aging, which he explains is a con- his apartment, and went on walks with his interested in evolution and the application of sequence of the weakened efficiency of se- parents in the Sussex countryside. His family mathematics to evolutionary genetics. “Imet lection on genetic variants whose effects on survival or reproduction are expressed late in life. The work stimulated much empirical research, including the pioneering experi- mentsofhislaterstudentMichaelRoseon selection for extended lifespan in the fruit fly Drosophila. Genetics of Mimicry and the Origin of Two Sexes Leading evolutionary biologists Tony Bradshaw, Philip Sheppard, and Arthur Cain were at the University of Liverpool during Charlesworth’stimethere.“Philip, in par- ticular, encouraged us to work on the theory of mimicry, which stimulated much of our later work on the apparently unrelated topic of the evolution of separate sexes and plant mating systems,” he says. In 1974, evolutionary biologist and geneticist John Maynard Smith recruited Charlesworth for a lecturer position in biology at the University of Sussex. The following year, Charlesworth and his wife authored a seminal This is a Profile of a recently elected member of the National Academy of Sciences to accompany the member’s Inaugural Profile photograph of Brian Charlesworth. Image courtesy of Xulio Maside. Article on page 1662. 1652–1653 | PNAS | February 10, 2015 | vol. 112 | no. 6 www.pnas.org/cgi/doi/10.1073/pnas.1423862112 Downloaded by guest on September 23, 2021 PROFILE paper on Batesian mimicry (2), a phenomenon Charlesworth and his team proposed an from studies of DNA sequence variability. in which a harmless species evolves to re- alternative model, background selection, “This class contributes most of the standing semble a dangerous one. The paper describes noting that there is a steady input of harmful variation in fitness within a population,” he a model on how such a system evolves, variants into the population as a result of says. “Variation due to deleterious mutations whereby a new variant that improves mimicry mutation. “These are mostly destined to be explains only some of this standing variation, can only enter the population if it is suffi- removed from the population by selection; so that processes such as balancing selection ciently close in the genome to a variant that when genetic recombination is rare or ab- (when different versions of a gene are actively has already entered the population because it sent, this results in the simultaneous removal maintained in the gene pool) must also confers an imperfect degree of mimicry. The of other variants located in the same ge- contribute.” model explains the origin of the close linkage nome,” he says. “The observed correlation of genes controlling mimicry. between variability and the rate of re- Continuing Goals Four years later, Charlesworth and his wife combination can be explained by background Through his research, faculty positions, lec- formulated a model (3) that elucidates features selection, as well as by the hitchhiking of tures, and books (8–10), Charlesworth inspires of the origin of two sexes from a hermaphro- beneficial mutations.” The findings have numerous students and others to learn more dite ancestor capable of self-fertilization, as is since stimulated substantial research on dis- about evolution and genetics. For these efforts thecaseformanyfloweringplants.Themodel tinguishing hitchhiking from background and his contributions to science, he has re- additionally explains how the specialized selection effects. ceived several awards and honors. He was chromosomes involved in sex determination elected to the Royal Society of London (1991), Y Chromosome Evolution and Variation start to evolve from an ancestral condition in the American Academy of Arts and Sciences in Fitness which they are identical in genetic makeup. (1996), and the Royal Society of Edinburgh Charlesworth returned to the University In 1997, Charlesworth became a Royal Soci- (2000). He was awarded the Darwin Medal of ety Research Professor at the University of of Chicago in 1985. He was a professor of the Royal Society of London in 2000 and the Edinburgh. Five years later, while con- ecology and evolution there for the next 12 Darwin-Wallace Medal of the Linnean Society tinuing to explore the origin of sex chromo- years. In 1987, he and coauthors Jerry Coyne in 2010. somes, Charlesworth and coauthor Doris and Nick Barton investigated how chromo- In his semiretirement, Charlesworth Bachtrog showed that an enormous reduction somal location can affect the fates of new would like to pursue various questions in genetic variability occurred on the mutations (4). Charlesworth explains that, in raised by the patterns he and postdoctoral newly evolved Y chromosome of the fruit many species with genetic sex determination, researcher José Campos have observed in the X chromosome is unusual because its fly species Drosophila miranda compared data compiled on DNA sequences gener- partner in males, the Y chromosome, lacks with the homologous genes on its X chro- ated by the Drosophila Population Genomics genes that are present on the X chromosome. mosome (6). Later work on this system, es- Project. “This would involve extensive com- In contrast, females carry two copies of the pecially by Bachtrog and Carolina Bartolomé, puter simulations of hitchhiking and back- X chromosome. has confirmed and extended the findings. ground selection, tailored to the details of Charlesworth and his colleagues showed The research provides valuable insights into that beneficial mutations often accumulate the early stages of the evolution of the the composition of the chromosome regions Y chromosome. concerned,” he says. along an evolving lineage at a faster rate “ on the X chromosome compared with the Charlesworth’s inaugural article, “The cau- Charlesworth adds, I also plan to work autosomes. This phenomenon was later ses of natural variation in fitness: Evidence on various other theoretical projects in pop- dubbed the “faster-X effect.” He says, “This from studies of Drosophila populations,” ulation genetics and evolution. My general stimulated a large body of research to test applies quantitative genetic studies of the goal is to try and better understand patterns for faster-X effects in a variety of species; fruit fly to resolve the question of why fit- that we can see in the data provided by ge- recent work using whole-genome sequence ness greatly varies (7). The study reveals the netics and genomics, in the light of reason- information suggests that these are