Identifying the mechanisms and traits that allow organisms to colonize and persist under novel environmental conditions remains a key challenge in biology. There are three theoretical mechanisms that facilitate the ability of species to invade and adapt to the presence of novel stressors: 1) organisms may rapidly evolve post-colonization as a result of natural selection acting on pre-existing genetic variation, 2) a trait evolved for one function in the original environment may be co-opted for a new function under novel conditions (exaptation), and 3) a trait adaptive in the original environmental context facilitates persistence in another without changing function (pre-adaptation). Using a comparative transcriptomics approach, we quantified adaptive and maladaptive plasticity to infer the potential roles of pre-adaptation and post-colonization evolution in facilitating colonization of extreme environments rich in hydrogen sulfide (H2S) by ancestral, sulfide-intolerant species that differ in their colonization success. Expression variation indicated that all species respond plastically respond to H2S exposure, but in largely unique ways. We also found evidence for adaptive plasticity in all species, regardless of colonization success, but only a few of these genes were shared among successful colonizing species. By far, evidence of maladaptive plasticity outnumbered evidence of adaptive plasticity in our dataset. Overall, the findings of this study suggest that pre-adaptation in key pathways may initially facilitate colonization of H2S-rich habitats, but post-colonization evolution, potentially potentiated by maladaptive plasticity, is necessary to persist upon exposure to extreme environmental conditions.