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Biology subjects

Tobler, M.

Publications and source records attributed to Tobler, M..

7 recordsLinked to original sources

Gene expression signatures of salinity transitions in Limia perugiae (Poeciliidae), with comparisons to other teleosts

Salinity gradients act as strong environmental barriers that limit the distribution of aquatic organisms. Changes in gene expression associated with transitions between freshwater and saltwater environments can provide insight into organismal responses to variation in salinity. We used RNA-sequencing (RNA-seq) to investigate genome-wide variation in gene expression between a hypersaline population and a freshwater population of the livebearing fish species Limia perugiae (Poeciliidae). Our analyses of gill gene expression revealed potential molecular mechanisms underlying salinity tolerance in this species, including the enrichment of genes involved in ion transport, maintenance of chemical homeostasis, and cell signaling in the hypersaline population. We also found differences in gene expression patterns associated with cell cycle and protein folding processes between the hypersaline and freshwater L. perugiae. Bidirectional freshwater-saltwater transitions have occurred repeatedly during the diversification of fishes, allowing for broad-scale examination of repeatable patterns in evolution. We compared transcriptomic variation in L. perugiae with other teleosts that have made freshwater-saltwater transitions to test for convergence in gene expression. Among the four distantly related population pairs from high- and low-salinity environments that we included in our analysis, we found only ten shared differentially expressed genes, indicating little evidence for convergence. However, we found that differentially expressed genes shared among three or more lineages were functionally enriched for ion transport and immune functioning. Overall, our results--in conjunction with other recent studies-- suggest that different genes are involved in salinity transitions across disparate lineages of teleost fishes.

physiology↗

Recurrent evolution of small body size and loss of the sword ornament in Northern Swordtail fish

Across the tree of life, species have repeatedly evolved similar phenotypes. While well-studied for ecological traits, there is also evidence for convergent evolution of sexually selected traits. Swordtail fish (Xiphophorus) are a classic model system for studying sexual selection, and female Xiphophorus exhibit strong mate preferences for large male body size and a range of sexually dimorphic ornaments. However, sexually selected traits have been lost multiple times in the genus. Phylogenetic relationships between species in this group have historically been controversial, likely as a result of prevalent gene flow, resulting in uncertainty over the number of losses of ornamentation and large body size. Here, we use whole-genome sequencing approaches to re-examine phylogenetic relationships within a Xiphophorus clade that varies in the presence and absence of sexually selected traits. Using wild-caught individuals, we determine the phylogenetic placement of a small, unornamented species, X. continens, confirming an additional loss of ornamentation and large body size in the clade. With these revised phylogenetic relationships, we analyze evidence for coevolution between body size and other sexually selected traits using a phylogenetically independent contrasts approach. These results provide insights into the evolutionary pressures driving the recurrent loss of suites of sexually selected traits.

evolutionary biology↗

Genetics and resource availability shape divergence in life history and behavior between ecotypes of Atlantic mollies (Poecilia mexicana, Poeciliidae)

Phenotypic variation is common along environmental gradients, but it is often unknown to what extent it results from genetic differentiation between populations or phenotypic plasticity. We studied populations of a livebearing fish that have colonized streams rich in toxic hydrogen sulfide (H2S). In nature, there is strong phenotypic differentiation between adjacent sulfidic and nonsulfidic populations. In this study, we varied food availability to pregnant mothers from different populations to induce maternal effects, a form of plasticity, and repeatedly measured life-history and behavioral traits throughout the offsprings ontogeny. Genetic differentiation affected most of the traits we measured, as sulfidic offspring tended to be born larger, mature later, have lower burst swimming performance, be more exploratory, and feed less accurately. In contrast, maternal effects impacted few traits and at a smaller magnitude, even though offspring from poorly provisioned mothers tended to be born larger and be more exploratory. Population differences and maternal effects (when both were present) acted synergistically, and there was no evidence for population differences in plasticity. Overall, our study suggests that phenotypic divergence between these populations in nature is primarily caused by genetic differentiation, and that plasticity mediated by maternal effects accentuates--but does not cause--differences between populations.

evolutionary biology↗

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

Convergent evolution, where independent lineages evolve similar traits when adapting to similar habitats, is a common phenomenon and testament to the repeatability of evolutionary processes. Still, non-convergence is also common, and a major question is whether apparently idiosyncratic, lineage-specific evolutionary changes are reflective of chance events inherent to evolutionary processes, or whether they are also influenced by deterministic genetic or ecological factors. To address this question, we quantified the degree of convergence in genome-wide patterns of gene expression across lineages of livebearing fishes (family Poeciliidae) that span 40 million years of evolution and have colonized extreme environments in the form of toxic, hydrogen-sulfide-rich springs. We specifically asked whether the degree of convergence across lineage pairs was related to their phylogenetic relatedness or the ecological similarity of the habitats they inhabit. Using phylogenetic comparative analyses, we showed that the degree of convergence was highly variable across lineage pairs residing in sulfide springs. While closely related lineages did not exhibit higher degrees of convergence than distantly related ones, we uncovered a strong relationship between degree of convergence and ecological similarity. Our results indicate that variation in the degree of convergence is not merely noise associated with evolutionary contingency. Rather, cryptic environmental variation that is frequently ignored when we employ reductionist approaches can significantly contribute to adaptive evolution. This study highlights the importance of multivariate approaches that capture the complexities of both selective regimes and organismal design when assessing the roles of determinism and contingency in evolution. Significance StatementWhen different species adapt to similar environmental conditions, we frequently observe a mix between shared (convergent) and lineage-specific (nonconvergent) evolutionary changes. Shared changes provide evidence for the repeatability and predictability of evolution. However, it remains unclear whether lineage-specific changes are caused by random forces that limit the predictability of evolution, or whether they reflect deterministic processes shaped by unidentified genetic and environmental factors. By analyzing patterns of gene expression across fishes in extreme environments, we show that the degree of convergence between lineages is related to ecology, indicating that lineage-specific evolutionary changes are not just noise caused by random processes. Thus, acknowledging the complexity of nature in empirical research is critical if we want to predict evolution.

evolutionary biology↗

Convergent adaptation and ecological speciation result from unique genomic mechanisms in sympatric extremophile fishes

The evolution of independent lineages along replicated environmental gradients frequently results in convergent adaptation, yet the degree to which convergence is present across multiple levels of biological organization is often unclear. Additionally, inherent biases associated with shared ancestry and variation in selective regimes across geographic replicates often pose challenges for confidently identifying patterns of convergence. We investigated a system in which three species of poeciliid fishes sympatrically occur in a toxic spring rich in hydrogen sulfide (H2S) and an adjacent nonsulfidic stream to examine patterns of adaptive evolution across levels of biological organization. We found convergence in morphological and physiological traits and genome-wide patterns of gene expression among all three species. In addition, there were shared signatures of selection on genes encoding H2S toxicity targets in the mitochondrial genomes of each species. However, analyses of nuclear genomes revealed neither evidence for substantial genomic islands of divergence around genes involved in H2S toxicity and detoxification nor substantial congruence of strongly differentiated regions across population pairs. These non-convergent, heterogenous patterns of genomic divergence may indicate that sulfide tolerance is highly polygenic, with shared allele frequency shifts present at many loci with small effects along the genome. Alternatively, H2S tolerance may involve substantial genetic redundancy, with non-convergent lineage-specific variation at multiple loci along the genome underpinning similar changes in phenotypes and gene expression. Overall, we demonstrate variability in the extent of convergence across organizational levels and highlight the challenges of linking patterns of convergence across scales.

evolutionary biology↗

Convergent evolution of conserved mitochondrial pathways underlies repeated adaptation to extreme environments

Extreme environments test the limits of life; yet, some organisms thrive in harsh conditions. Extremophile lineages inspire questions about how organisms can tolerate physiochemical stressors and whether the repeated colonization of extreme environments is facilitated by predictable and repeatable evolutionary innovations. We identified the mechanistic basis underlying convergent evolution of tolerance to hydrogen sulfide (H2S)--a toxicant that impairs mitochondrial function--across evolutionarily independent lineages of a fish (Poecilia mexicana, Poeciliidae) from H2S-rich springs. Using comparative biochemical and physiological analyses, we found that mitochondrial function is maintained in the presence of H2S in sulfide spring P. mexicana, but not ancestral lineages from nonsulfidic habitats, due to convergent adaptations in the primary toxicity target and a major detoxification enzyme. Genome-wide local ancestry analyses indicated that convergent evolution of increased H2S tolerance in different populations is likely caused by a combination of selection on standing genetic variation and de novo mutations. At a macroevolutionary scale, H2S tolerance in 10 independent lineages of sulfide spring fishes across multiple genera of Poeciliidae is correlated with the convergent modification and expression changes of genes associated with H2S toxicity and detoxification. Our results demonstrate that the modification of highly conserved physiological pathways associated with essential mitochondrial processes mediates tolerance to physiochemical stress. In addition, the same pathways, genes, and--in some instances--codons are implicated in H2S adaptation in lineages that span 40 million years of evolution. Significance StatementSome organisms can tolerate environments lethal for most others, but we often do not know what adaptations allow them to persist and whether the same mechanisms underly adaptation in different lineages exposed to the same stressors. Investigating fish inhabiting springs rich in toxic hydrogen sulfide (H2S), we show that tolerance is mediated by the modification of pathways that are inhibited by H2S and those that can detoxify it. Sulfide spring fishes across multiple genera have evolved similar modifications of toxicity targets and detoxification pathways, despite abundant lineage-specific variation. Our study highlights how constraints associated with the physiological consequences of a stressor limit the number of adaptive solutions and lead to repeatable evolutionary outcomes across organizational and evolutionary scales.

evolutionary biology↗

Parent-offspring conflict, ecology, and life history diversification of livebearing fishes

Shifts in life history evolution can potentiate sexual selection and speciation. However, we rarely understand the causative links between correlated patterns of diversification or the tipping points that initiate changes with cascading effects. We investigated livebearing fishes with repeated transitions from pre- (lecithotrophy) to post-fertilization maternal provisioning (matrotrophy) to identify the potential ecological drivers of evolutionary transitions in life history. Phylogenetic comparative analyses across 94 species revealed that bi-directional evolution along the lecithotrophy-matrotrophy continuum is correlated with ecology, supporting adaptive hypotheses of life history diversification. Consistent with theory, matrotrophy was associated with high resource availability and low competition. Our results suggest that ecological sources of selection contribute to the diversification of female provisioning strategies in livebearing fishes, which have been associated with macroevolutionary patterns of sexual selection and speciation.

evolutionary biology↗