Genomic evolution in real time: causes and consequences of an adaptive mutation in the wild

Phenotypic variation is the raw material of evolution and the target of natural and sexual selection. However, evolution can only occur through changes in gene frequencies at the level of DNA. Our proposal capitalizes on a recently discovered adaptive morphological mutation to explicitly link how changes at the genomic level translate into changes at the phenotypic level, which are then subject to rapid and quantifiable evolutionary change in a wild population. We will study a mutation in the Pacific field cricket, Teleogryllus oceanicus, that erases sound-producing structures on male wings. Males ordinarily sing to attract females for mating, but in doing so, they also attract a deadly, acoustically-orienting parasitoid fly. The silencing mutation, flatwing, arose in a wild population in 2003 and rapidly spread to near-fixation over the course of approximately 20 generations because it protects males from attack by the fly. Silent flatwing males appear to act as satellites to the remaining callers in the population by intercepting and mating with responding females. The rapid spread of the flatwing mutation represents one of the fastest rates of evolution ever recorded in the wild. The mutation is a simple Mendelian trait inherited on the sex chromosome. The main goals of our proposal are to (1) identify in what region of the genome the mutation resides, and the underlying genetic changes, and (2) characterize broad-scale differences in gene expression between flatwing and normal-wing male crickets, and between crickets that have experienced different social environments resulting from the presence or absence of silent males. These goals will provide the evolutionary biology community with a better understanding of the type of genomic variation targeted by selection in the wild (e.g. coding genes vs. regulatory genes). Our results will also demonstrate how a major evolutionary event has knock-on effects on the regulation and expression of other genes, thereby exposing new phenotypic traits to selection. The T. oceanicus study system provides an excellent opportunity to demonstrate how evolution works in real time, in the wild, and how change in a single trait initiates a cascade of effects that alter gene expression, phenotypic traits, and selection pressure.

WHO WILL BENEFIT
The main beneficiaries of the research outputs described here are members of the general public. The phenomenon we are studying - a recent, adaptive mutation in a wild population of crickets - has enjoyed a large amount of media attention already. The spread of the mutation represents one of the most rapid examples of evolution ever documented in the wild. We will engage the general public with our research through liaising with the popular press (e.g. Nathan and Marlene recently published a study that was featured on NERC's PlanetEarth Online website) and by developing more direct links with members of the local community through secondary schools and outreach programmes (please see Pathways to Impact statement for more details).

HOW THEY WILL BENEFIT
The primary benefit will be enhanced understanding of the scientific process, channeled via the topical and engaging topic of evolutionary biology. The phenomenon we are studying in crickets is not abstruse. It is a proven winner with the general public: the initial discovery of the mutation was featured on a variety of popular websites, for example Berkeley's "Understanding Evolution" website, which showcases a variety of both Nathan and Marlene's published research results (http://evolution.berkeley.edu/evolibrary/news/061201_quietcrickets).

As is detailed in the Pathways to Impact, the teaching of evolution is being systematically and, in some cases, successfully, undermined by determined groups within the UK and worldwide (e.g. a new Centre for Intelligent Design just opened in Glasgow this autumn). If the UK is to retain its title as a world-leader in scientific research and not suffer the same onslaught from un-scientific quarters that the United States has, then scientists, funding bodies, politicians and educators must actively confront and correct the misinformation that is promulgated by anti-evolution groups. For instance, the UK's most famous example of rapid evolution, the Peppered Moth (Biston betularia), has been attacked by creationists in an effort to undermine confidence in the scientific conclusions from that system. The avidity with which the Peppered Moth story was seized upon by creationists in the UK and US underscores that more examples of "evolution in action" are needed. Our cricket system provides an exemplary one, and understanding the genetics of the system will bolster the evidence for rapid evolution.