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 (H S)-rich springs. H S is a potent respiratory toxicant that creates extreme environmental conditions in aquatic ecosystems. There is also a rich history of research on H 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 H 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 H 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.

A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems

“…The expectation that the independent evolution of similar phenotypes in similar environments corresponds to the response of similar genomic regions (Gagnaire et al ., ; Perrier et al ., ) and the expression of the same genes (Hanson et al ., ) within them is not always upheld. For instance, in some cases the same signalling pathway, rather than the same loci, may be involved in parallel evolution as observed in the adaptation of poecilid fishes to hydrogen sulphide springs (Tobler et al ., ). In addition, most genomic studies have only been able to explain a small proportion of phenotypic variance.…”

Functional consequences of phenotypic variation between locally adapted populations: Swimming performance and ventilation in extremophile fish

“…In addition, this species has independently colonized multiple toxic, hydrogen‐sulphide (H 2 S)‐rich springs in southern Mexico (Tobler et al, ). Populations in adjacent nonsulphidic and sulphidic habitats face strong and multifarious divergent selection that includes variation in abiotic and biotic environmental conditions (Tobler, Kelley, Plath, & Riesch, ). Fish inhabiting sulphide springs are exposed to high levels of toxicity associated with H 2 S, hypoxia, high densities of intraspecific competitors and reduced species‐richness with few aquatic predators and inter‐specific competitors (Culumber et al, ; Greenway, Arias‐Rodriguez, Diaz, & Tobler, ; Plath et al, ; Riesch, Schlupp, Tobler, & Plath, ).…”

Correlated divergence of female and male genitalia in replicated lineages with ongoing ecological speciation

“…data), vary in the degree of total reproductive isolation, and differ in the relative importance of different reproductive isolating barriers (Tobler et al. ). The consistent divergence of genitalia in all population pairs suggests that these traits evolve rapidly and potentially cause mechanical isolation even at early stages of speciation.…”

“…Sulfide spring fishes are locally adapted and differ from ancestral populations in adjacent nonsulfidic habitats in physiological, morphological, behavioral, and life‐history traits (Tobler et al. ). Trait divergence includes changes in sexual behaviors (less coercive mating attempts in sulfidic populations; Plath et al.…”