Genetics, development and evolution of adaptive pigmentation in vertebrates

SHORT REVIEW Genetics, development and evolution of adaptive pigmentation in vertebrates

The study of pigmentation has played an important role in the intersection of evolution, genetics, and developmental biology. Pigmentation's utility as a visible phenotypic marker has resulted in over one hundred years of intense study of coat color mutations in laboratory mice, thereby creating an impressive list of candidate genes and an understanding of the developmental mechanisms responsible for the phenotypic effects. Variation in color and pigment patterning has also served as the focus of many classic studies of naturally occurring phenotypic variation in a wide variety of vertebrates, providing some of the most compelling cases for parallel and convergent evolution. Thus, the pigmentation model system holds much promise for understanding the nature of adaptation by linking genetic changes to variation in fitness-related traits. Here, I first discuss the historical role of pigmentation in genetics, development and evolutionary

Introduction

Understanding the generation and maintenance of phenotypic diversity requires the integration of genetics, development and evolutionary biology in an ecological context. Historically, biologists have used two parallel approaches to study evolutionary change, one working at the level of genotype and a second working at the level of phenotype. For example, population geneticists have focused on temporal and spatial changes in allele and genotype frequencies, whereas organismal biologists have studied how individuals differ in phenotypic traits across natural environments. However, research linking genotype and phenotype, identifying the molecular changes responsible for phenotypic adaptation and the developmental mechanisms by which genotypes encode phenotypic traits, is necessary to truly understand the processes responsible for generating both genetic and organismal diversity.

The pigmentation system is a particularly promising phenotype in which to explore connections between genotype and phenotype for ecologically important traits. Coat color mutations in laboratory mice have served as a premier model for studying gene action in a biology. I then discuss recent empirically based studies in vertebrates, which rely on these historical foundations to make connections between genotype and phenotype for ecologically important pigmentation traits. These studies provide insight into the evolutionary process by uncovering the genetic basis of adaptive traits and addressing such long-standing questions in evolutionary biology as one, are adaptive changes predominantly caused by mutations in regulatory regions or coding regions? two, is adaptation driven by the fixation of dominant mutations? and three, to what extent are parallel phenotypic changes caused by similar genetic changes? It is clear that coloration has much to teach us about the molecular basis of organismal diversity, adaptation and the evolutionary variety of biological processes, leading to a wealth of information about genes involved in pigmentation and their developmental interactions. Because melanin-based pigmentation biology is highly conserved across vertebrates, a deep understanding of mouse coat color genetics translates easily and directly into testable hypotheses for studying the molecular basis of pigmentation variation in natural vertebrate populations. Most important, color quality and or color patterns frequently exhibit dramatic variation both within and between species in a way that can be quantified and is conspicuously affected by natural selection. In particular, selective forces such as crypsis, aposematism, thermoregulation, and sexual signaling drive variation in both pigmentation and color pattern. Thus, pigmentation phenotypes in natural populations present an ideal opportunity for studying the genetic basis of phenotypic diversity and evolutionary change.

Here, I first discuss how the rich history of pigmentation biology in the fields of genetics, development and evolution provide the essential background information to address fundamental questions in evolutionary developmental biology. Then I provide empirical examples in which the link between genotype and phenotype has been successfully made for adaptive pigmentation in natural populations. Throughout, I focus primarily on studies of mice and melanin-based pigmentation, from which the most data are available, but draw on studies of other vertebrates and pigment types whenever possible. Together, these studies provide exciting insight into how adaptation proceeds at the molecular level and also shed light on the evolutionary process in general.