To evaluate the first stages of adaptation and differentiation following colonization into a vacant and ecologically divergent habitat, 100 melanistic and low-plated adult threespine stickleback (Gasterosteus aculeatus) exhibiting gigantism in body size and robust spines were transferred in 1993 from a large dystrophic lake (Mayer Lake, Haida Gwaii, British Columbia, Canada) with a diverse vertebrate predator regime, into an adjacent fishless eutrophic pond with macroinvertebrate piscivores. Eight generations were examined as a test of multiple functional hypotheses on the morphological traits that differentiate lake and pond stickleback throughout their distribution. Measurements of 20 defence and trophic traits were made on 275 wild-caught fish collected from the source and transplant populations over multiple years. There have been significant reductions (males: females) in plate count (8%: 0.5%), lateral plate 2 frequency (46%: 17%), lateral plate 3 height (17%: 18%), pelvic spine length (12%: 6%), dorsal spine length (21%: 16%), gill raker number (5%: 1%), and gill raker length (37%: 43%), and an increase in gill raker spacing (+5%: 0%), jaw length (+5%: +4%), and eye diameter (+8%: +7%). These changes within eight generations represent one-third of the morphological differences observed between naturally established large lake and pond populations in these archipelago and are all in the direction predicted from the change in habitat. Field samples indicate strong selection in the colonists although lab-reared individuals implicate an additional role of plasticity for dorsal spine and gill raker lengths, which may contribute to the rapid adaptation into novel and highly divergent selective landscapes. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107, 494–509.