Convergent Evolution of Conserved Mitochondrial Pathways Underlies Repeated Adaptation to Extreme Environments

Abstract

22Extreme environments test the limits of life. Still, some organisms thrive in harsh conditions, 23 begging the question whether the repeated colonization of extreme environments is facilitated by 24 predictable and repeatable evolutionary innovations. We identified the mechanistic basis underlying 25 convergent evolution of tolerance to hydrogen sulfide (H2S)-a potent toxicant that impairs 26 mitochondrial function-across evolutionarily independent lineages of a fish (Poecilia mexicana, 27 Poeciliidae) from H2S-rich freshwater springs. We found that mitochondrial function is maintained 28 in the presence of H2S in sulfide spring P. mexicana, but not ancestral lineages in adjacent nonsulfidic 29 habitats, due to convergent adaptations in both the primary toxicity target and a major detoxification 30 enzyme. Additionally, we show that H2S tolerance in 10 independent lineages of sulfide spring fishes 31 across multiple genera of Poeciliidae is mediated by convergent modification and expression changes 32 of genes associated with H2S toxicity and detoxification. Our results demonstrate that the repeated 33 modification of highly conserved physiological pathways associated with essential mitochondrial 34 processes enabled the colonization of novel environments. 35 36 3 Stephen J. Gould was a fierce proponent of the importance of contingency in evolution, famously 37 quipping that replaying the "tape of life" would lead to different outcomes every time (1). 38Mitochondrial genomes were historically thought to be a prime example of such contingency 39 evolution, because alternative genetic variants were assumed to be selectively neutral (2). This 40 paradigm has been shifting, with mounting evidence that mitochondria-and genes encoded in the 41 mitochondrial genome-play an important role in adaptation, especially in the context of 42 physiochemical stress (3). However, it often remains unclear how genetic variation in mitochondrial 43 genomes and nuclear genes that contribute to mitochondrial function translates to variation in 44 physiological and organismal function. Furthermore, it is not known whether exposure to similar 45 selective regimes may cause convergent modifications of mitochondrial genomes and emergent 46 biochemical and physiological functions in evolutionarily independent lineages. Extreme 47 environments that represent novel ecological niches are natural experiments to address questions 48 about mechanisms underlying mitochondrial adaptations and illuminate the predictability of adaptive 49 evolution of mitochondria. Among the most extreme freshwater ecosystems are springs with high 50 levels of hydrogen sulfide (H2S), a potent respiratory toxicant lethal to metazoans due to its 51 inhibition of mitochondrial ATP production (4). Multiple lineages of livebearing fishes (Poeciliidae) 52 have colonized H2S-rich springs throughout the Americas and independently evolved tolerance to 53 sustained H2S concentrations orders of magnitudes higher than those encountered by ancestral 54 lineages in nonsulfid...

Ecology drives the degree of convergence in the gene expression of extremophile fishes

“…To test whether population pairs in more ecologically similar habitats exhibit higher degrees of convergence, we measured aspects of water quality in situ (temperature, pH, specific conductivity, dissolved oxygen, and H2S concentration) and downloaded 19 geospatial variables that describe climatic variation for each sulfide spring (28). Principal component (PC) analysis indicated that different springs primarily segregated along the first PC axis (Figure 2C), which was correlated with temperature, pH, and H2S concentration, as well as bioclimatic variables 1,4,6,7,9,11,12,13,14,16,17,18, and 19 (correlations: |0.20| < r < |0.28|; Table S1). In general, sulfide springs in Mexico (negative scores along PC axis 1) exhibited higher temperatures and H2S concentrations, lower pH, less seasonality, and more precipitation compared to the springs in Florida and the Dominican Republic (positive scores along PC axis 1).…”

“…We analyzed 118 gill transcriptomes from ten lineages of sulfide spring poeciliids and ten closely related lineages from adjacent nonsulfidic habitats (17). To quantify variation in the degree of convergence in gene expression between pairs of sulfide spring populations, we selected the 5,000 top expressed genes across all lineages as dependent variables in expression variance and evolution (EVE) models (24, 25), which allow for the identification of convergent expression shifts while accounting for the evolutionary relationship among lineages [see Figure 1A; (26)].…”

“…Sulfide spring lineages span over 40 million years of evolutionary divergence, facilitating comparisons between populations of the same species and between species within and among genera (Figure 1A). Previous research has documented that sulfide spring lineages show clear signatures of convergent evolution of mitochondrial genomes, the regulation of genes associated with H 2 S toxicity and detoxification, and aspects of physiological function, morphology, reproductive life history, and behavior (17–21). Despite the evidence for convergence across levels of organismal organization and across a wide gradient of phylogenetic relationships, past studies have also found evidence of lineage-specific evolutionary change, giving rise to substantial variation in the degree of convergent evolution between specific pairs of sulfide spring lineages (22).…”

Genomic signature of shifts in selection and alkaline adaptation in highland fish

“…In general, metabolism processes were involved in fish response to varies environmental stresses (including alkaline stress) by a huge amount of researches (Wood 1991). A most recent study highlights the genes involved in conserved mitochondrial pathways under selection in adaptation to extreme environment (Greenway et al 2020). In addition to our previous studies in highland alkaline tolerant fish, we found a number of genes associated with energy metabolism processes under selection as well, such as mitochondrial function and protein metabolism (Tong, Fei, et al 2017).…”

Ecology and genomic background shape the probability of parallel adaptation to climate

“…Likewise, the Agouti and Mc1R genes control coloration in diverse organisms (Kingsley et al 2009;Manceau et al 2010;Linnen et al 2013). Beyond case studies, meta-analyses have shown that parallel phenotypic evolution often involves the same genomic region (Elmer and Meyer 2011;Stern 2013;Greenway et al 2020). In contrast to these studies of major genes, parallelism is less understood when evolution involves many genes of smaller effect, although studies of genome-wide variation are beginning to fill this gap (Barrett and Schluter 2008;Yeaman 2015;Yeaman et al 2016;Papadopulos et al 2021).…”