Extreme environments and the origins of biodiversity: Adaptation and speciation in sulphide spring fishes

Abstract

Organisms adapted to physiochemical stressors provide ideal systems to study evolutionary mechanisms that drive adaptation and speciation. This review study focuses on livebearing fishes of the Poecilia mexicana species complex (Poeciliidae), members of which have repeatedly colonized hydrogen sulphide (H₂ S)-rich springs. H₂ S is a potent respiratory toxicant that creates extreme environmental conditions in aquatic ecosystems. There is also a rich history of research on H₂ S in toxicology and biomedicine, which has facilitated the generation of a priori hypotheses about the proximate mechanisms of adaptation. Testing these hypotheses through the application of high-throughput genomic and transcriptomic analyses has led to the identification of the physiological underpinnings mediating adaptation to H₂ S-rich environments. In addition, systematic natural history studies have provided a nuanced understanding of how the presence of a physiochemical stressor interacts with other sources of selection to drive evolutionary change in a variety of organismal traits, including physiology, morphology, behaviour and life history. Adaptation to extreme environments in P. mexicana also coincides with ecological speciation, and evolutionarily independent lineages span almost the full range of the speciation continuum from panmixia to complete reproductive isolation. Multiple mechanisms of reproductive isolation are involved in reducing gene flow between adjacent populations that are adapted to contrasting environmental conditions. Comparative studies among evolutionarily independent lineages within the P. mexicana species complex and, more recently, other members of the family Poeciliidae that have colonized H₂ S-rich environments will provide insights into the factors facilitating or impeding convergent evolution, providing tangible links between micro-evolutionary processes and macro-evolutionary patterns.

Keywords: Poeciliidae; ecological genomics; extremophile fishes; hydrogen sulphide; local adaptation; speciation.