Lean on We: How Eco-Evolution Permeates Animal–Microbe Associations

View Large Image | View Hi-Res Image | Download PowerPoint SlideI will come right to the point. I Contain Multitudes is the best general interest book on the science and scientists behind the microbiome revolution. Science writer, blogger, and tweeter Ed Yong composes the story that we, as scientists and students in this area, all want to tell friends, family, and colleagues: macrobiology requires microbiology. To the delight of ecologists and evolutionary biologists, this story is chock-full of community dynamics, population biology, and the seamless integration of these fields. It is also teeming with citations for undergraduate and graduate students to use to write a report, discuss in journal club, or refresh their background knowledge.Cataloging the vast complexity and abundance of the microbiome in animals breathed new energy into ecology and evolution and hit the big time after a 10-year scientific surge and media blitz. Largely facilitated by breakthroughs in technology, the beginning of the microbiome era is not unlike the first decade of genetics or any other discipline. Naturally, basic questions get asked first. Which microbial taxa are there? Why are they there? and What rules or patterns best explain their existence? Indeed, Yong likens today's studies of the microbiome to Darwin and Wallace's studies of the diversity and biogeography of macroscopic life that ultimately preceded their development of a new theory. He also echoes the field's current view that the time for exclusively descriptive studies is over, and the field is now answering the next level of questions: Why are the microbes there? What are they doing? and How do they do it?Earth is first and foremost a microbial planet. All macroscopic life evolved in a soup of microbes that were largely, though not completely, hiding in the blind spots of Darwin and Wallace. Yong's book does not target these environmental microbes per se. Rather it shines the limelight on the microbiome within us and within animals more generally. Botanists will admittedly feel a bit left out in this book, but that leaves room for a good sequel. Yong captures the essence of the microbiome revolution – that all complex hosts must be recast as communities or holobionts – the whole assemblage of a host and its microbes. So what is affected by this community of invisible microbes? Yong notes that the question may be better phrased as what is not? Microbes are traceable to tissue and organ development, smell, behavior, multicellularity, sociality, speciation, etc. In the case of immune systems, animals are not just regulating microbes, but rather immune systems are regulated themselves by microbes. This feedback loop between host and microbial communities challenges the province of biological individuality. As Yong quips, ‘it turns out that the brainless, microscopic, single-celled organisms that live inside us have been pulling on our strings all along’.The newfound appreciation of the diversity and abundance of microbes within animals is what leads Yong to honor Darwin's ‘grandeur in this view of life’ quote in the title of the book. He is right to do so. You cannot overstate the importance of when a scientific idea moves from the edges of biology to the hub. Yong is balanced as he deconstructs the befuddling and humbling complexity of the discipline into a simplistic vision that does not skip key points or nuances. His professorial capacity shines as metaphors illuminate vivid descriptions of the ‘oh wow’ moments of scientific discoveries – that mammals detoxify their toxic plant diets with gut bacteria, that human river blindness is due to Wolbachia endosymbionts in filarial nematodes, or that probiotics are not doing what you think they are doing. He links animal coprophagy of termites and koalas – an ‘ecosystem transplant’ – to the remarkable efficacy of fecal microbiota transplants in treating Clostridium difficile infections in humans. He details the transmission of microbes from mother to babies and describes how vertically inherited microbes face a selection pressure to help their hosts. There is a nuance here that such microbes do not necessarily care about being helpful (e.g., defensive symbiosis) or harmful (e.g., reproductive parasitism) phenotypes per se; rather they care from an evolutionary perspective about simply enhancing their transmission to the next generation. He paints the picture of sharing of microbes upon a kiss or handshake, the ways in which diet can shape our gut microbes and obesity, and what bacteria have to do with heart disease or the metabolism of ingested drugs.Understanding the ecological and evolutionary role of the microbiome within hosts does not end with this book by any stretch of the imagination. In fact, the invigorated frontier has only just been mapped. It will be a century-long period of groundbreaking discoveries. It will demand continued conceptualizations and approaches that integrate community ecology, evolutionary biology, and genomics. What spills out over time will morph the befuddling complexity into a holistic view of eco-evolutionary dynamics in animal–microbe associations that is generally consistent with the reductionist approaches of biology.