Integrative analyses of convergent adaptation in sympatric extremophile fishes

Abstract

Divergent selection along ecological gradients can lead to speciation, and replicated speciation events occur when populations of multiple lineages undergo divergence following colonization of similar environments. In such instances, it remains unclear to what extent reproductive isolation evolves via convergent mechanisms at the genomic level due to biases in the types of systems typically used to study convergent evolution. We used a unique system in which three species of poeciliid fishes occur in sympatry in an extremely toxic, hydrogen sulfide (H2S)-rich spring and an adjacent nonsulfidic stream to examine shared patterns of adaptive divergence across multiple levels of biological organization. Despite extremely small spatial scales, we found strong genetic differentiation between populations in sulfidic and nonsulfidic habitats mediated by strong selection against migrants between habitat types. High levels of reproductive isolation were accompanied by convergent patterns of adaptation in morphological and physiological traits, as well as genome-wide patterns of gene expression across all three species. Furthermore, the mitochondrial genomes of each species exhibit shared signatures of selection on key genes involved in H2S toxicity. However, contrary to predictions of speciation theory, analyses of divergence across the nuclear genome neither revealed evidence for clear genomic islands of speciation nor substantial congruence of outlier regions across population pairs. Instead, heterogenous regions of divergence spread across the genome suggest that selection for polygenic physiological adaptations likely facilitated the rapid evolution of high levels of reproductive isolation. Overall, we demonstrate that substantial convergence across multiple levels of biological organization can be mediated by non-convergent modifications at the genomic level. By disentangling environmental variation in natural selection from lineage-specific evolution in this system of highly divergent, yet sympatric lineages, our results emphasize the outsized role of the genomic substrate upon which selection acts in driving convergent evolution at the phenotypic level.

Nascent transcription reveals regulatory changes in extremophile fishes inhabiting hydrogen sulfide-rich environments

“…H 2 S also reacts with dissolved oxygen in aquatic environments, creating additionally stressful hypoxic conditions [25,26]. The ability to modulate gene expression plays a major role in survival in these H 2 S-rich environments, with sulfidic populations showing convergent shifts in the expression of key genes involved in H 2 S detoxification and sulfur metabolism [21,22,27,28]. Many of these changes involve genes in the sulfide : quinone oxidoreductase (SQR) pathway, which endogenously detoxifies H 2 S [29], This pathway is present in all metazoans and likely a bacterial relic from the Proterozoic aeon [30].…”

“…Sulfide spring populations (i.e. sulfidic ecotypes) are locally adapted and are phenotypically and genetically distinct from adjacent populations in non-sulfidic habitats [20][21][22]. H 2 S is toxic to most animals, inhibiting enzymes in the electron transport chain and lethally interfering with aerobic ATP production via oxidative phosphorylation [23,24].…”

“…Many of these changes involve genes in the sulfide : quinone oxidoreductase (SQR) pathway, which endogenously detoxifies H 2 S [29], This pathway is present in all metazoans and likely a bacterial relic from the Proterozoic aeon [30]. The expression of genes involved in the SQR pathway is consistently upregulated in sulfidic populations, as are sulfur transporter genes, and genes encoding subunits of cytochrome c oxidase (COX, the main toxicity target of H 2 S) [21,22,27,28]. Some of these genes show evolved, constitutive expression differences in sulfidic populations compared with non-sulfidic populations, whereas other genes show evolved plasticity in sulfidic populations in response to H 2 S [31].…”

“…Capturing this positional information and identifying shared changes in regulatory RNA transcription across independently adapted populations will reveal how regulatory mechanisms alter gene expression to enable survival of P. mexicana in sulfidic environments. Given that sulfidic lineages are often genetically distinct from adjacent non-sulfidic populations [20][21][22], shared differences across independent lineages may be indicative of adaptation [41]. More broadly, this approach will provide valuable new insight into the mechanisms by which gene expression regulation may evolve in response selection.…”

Selection on standing genetic variation mediates convergent evolution in extremophile fish

“…The sulfide spring populations from the Puyacatengo and Tacotalpa drainages show evidence for recent divergence between ecotypes, estimated at ~10,000 years ago in Tacotalpa and ~300 years ago in Puyacatengo (Brown et al, 2018). In contrast, sulfide spring populations in the Pichucalco and Ixtapangajoya drainages are hypothesized to have diverged earlier, with estimates from the Pichucalco drainage suggesting a timing of divergence of ~19,000 years ago (Greenway et al, 2021). Sulfide spring populations are locally adapted and exhibit convergent phenotypes related to morphology (Greenway et al, 2019; Riesch et al, 2016; Tobler & Hastings, 2011), life history traits (Riesch et al, 2010, 2014) and physiology (Greenway et al, 2020; Pfenninger et al, 2014; Plath et al, 2013; Tobler et al, 2011, 2016).…”