The threespine stickleback fish (Gasterosteus aculeatus) has emerged as a powerful model system for studying the genetic basis of organismal diversity. Threespine sticklebacks have undergone one of the most recent and remarkable adaptive radiations on earth. Ancestral ocean-dwelling sticklebacks repeatedly colonized and rapidly adapted to thousands of freshwater lakes and streams that formed by melting of glacial ice within the past 15,000 years. Ancestral and derived forms can be crossed in the lab, enabling forward genetic analyses to map genes responsible for evolved differences.

Molecular genetic analysis of head skeletal evolution

Major changes to the head skeleton, particularly in bones and teeth of the branchial skeleton, have occurred as sticklebacks adapt to new diets in freshwater environments. One of the best ecologically-characterized head skeletal adaptations in freshwater fish is a reduction in the number of gill rakers, a set of segmentally-reiterated bones in the branchial skeleton that helps determine what fish can eat. We have also identified two evolutionary "gain" traits: derived freshwater fish have evolved more pharyngeal teeth and bigger branchial bones. Our genetic studies have identified a handful of chromosome regions that control each of these traits. Studying the sequence, expression patterns, and functions of candidate genes within these chromosome regions, combined with ongoing fine mapping, will ultimately reveal the specific genes and mutations underlying the evolved differences. Molecular genetics in sticklebacks is now greatly facilitated by a wealth of new molecular resources, including genome sequences from 21 populations (Jones et al., 2012) and transgenic methods. Our studies will help answer long-standing questions about the molecular genetic basis of evolutionary change in natural populations. In addition, as many mechanisms of craniofacial, tooth, and bone patterning are conserved between fish and mammals, our studies will shed light on human skeletal disorders.

Developmental biology of head skeletal evolution

While striking changes in gill raker, tooth, and branchial bone patterning are seen in different populations of adult fish, we know little about how these differences manifest during embryonic and juvenile development. By comparing skeletal development in different populations with known differences in adult morphology, we will identify when and how the changes arise during development. Knowing the developmental basis of the evolved changes will help evaluate candidate genes and provide crucial insight into how specific genetic changes translate into evolved morphological differences.

Genetics of parallel evolution

Previously, we showed that parallel genetic mechanisms underlie pigmentation evolution in sticklebacks and humans (Miller et al., 2007b). These results demonstrate that studies in sticklebacks can reveal general mechanisms of evolutionary change used in other organisms, including humans. In addition, these results suggest constraints exist on the types of genes used for morphological evolution, and that perhaps some genes have certain features (e.g. a complex, modular, cis-regulatory region) that make them preferred substrates for evolutionary change. The evolved head skeletal traits offer a powerful system to test this prediction, as dozens of independently derived freshwater stickleback populations have evolved similar modifications in head skeletal morphology. For instance, the gill raker reduction trait is found in most freshwater populations, suggesting this trait is under strong selection during freshwater adaptation. Forward genetic analyses of parallel evolution in multiple independently derived populations will reveal whether evolution uses similar genetic mechanisms to confer similar phenotypic changes.