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

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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.