Rapid evolution of phenotypic divergence in fish populations

Iceland represents a natural laboratory for studying the colonization of freshwater habitats by fish since rivers and lakes all date from the end of the last Ice-Age less than 10,000 years ago. The North Atlantic provided a refuge for species such as arctic charr (Salvelinus alpinus) which invaded freshwater once the ice retreated. New habitats and the lack of competing species led to the appearance of different forms of Artic charr, called morphs. In particular, 27 discrete populations of dwarf charr have been identified with specialised feeding morphology that enables them to exploit the small larval fissures on the bottom of streams and lakes. Our Icelandic and Canadian partners have collected an enormous amount of data on each of the dwarf populations including, habitat characteristics (temperature and bottom type), diet, maximum body size, size and age at sexual maturity and cranial morphology. Other studies in progress on rapidly evolving DNA sequences we will enable us to determine the relationships between each population and estimate which ones arose independently allowing us to study the repeatability of evolution for populations living in similar habitats. Studies involving such diverse organisms as worms, flies and vertebrates suggest that poor nutrition alone is sufficient to produce dwarfism via effects on the signaling pathways controlled by the hormone Insulin-like growth factor-I (IGF-I): indicating a universal and conserved biological mechanism. Intriguingly, in the zebrafish, which is often used for studies of development, so-called 'knock-outs' of an IGF-binding-protein gene also caused alterations to the shape of the head which are reminiscent of those found in dwarf charr. We will therefore experimentally test the hypothesis that interactions between the environment and the IGF-hormone system during development can produce the specialised jaw and cranial morphology characteristic of the dwarf phenotype. Since early development in fish is entirely dependent on genetic messages passed through the egg yolk we will conduct experiments to determine whether it is the environment of the mother, the embryo or both that are important for producing fish with dwarf characteristics. Thingvallavatn, the largest and oldest lake in Iceland, contains four Arctic charr morphs, including a dwarf form, which are specialised to exploit different habitats. Laboratory breeding experiments have shown that the large differences in body size, morphology and life history such as the size at sexual maturity are heritable. This suggests that intense competition between morphs and reproductive isolation has resulted in natural selection and specialization for characters helping each morph to survive in their chosen environment. Previously we showed that dwarfism in the Thingvallavatn charr has resulted in a reduction in the number of muscle fibres in the trunk, which is thought to lower costs of maintenance relative to the ancestral charr. By studying a large number of Arctic charr populations (15 dwarfs and 5 generalists) we will test the generality of the hypothesis that the relative importance of developmental plasticity versus selection for setting muscle fibre number is related to the age and stability of the habitat and is different depending on whether there is competition with other morphs. The research is important because it addresses the fundamental question of how natural selection and plasticity operate to produce different forms of the same species at the level of physiological systems. The evolution of different morphs of the same species is relatively common and is found, for example, in sticklebacks and African cichclids. The practical application of this research is in understanding how the biodiversity of fish populations arises and how it may be conserved for future generations.