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Sanyal, A.

Publications and source records attributed to Sanyal, A..

35 records · Page 2Linked to original sources

The LRRK2 kinase substrates Rab8a and Rab10 contribute complementary but distinct disease-relevant phenotypes in human neurons

Mutations in the LRRK2 gene cause familial Parkinsons disease presenting with pleomorphic neuropathology that can involve -synuclein or tau accumulation. LRRK2 mutations are thought to converge toward a pathogenic increase in LRRK2 kinase activity. A subset of small Rab GTPases have been identified as LRRK2 substrates, with LRRK2-dependent phosphorylation resulting in Rab inactivation. We used CRISPR/Cas9 genome editing to generate a novel series of isogenic iPSC lines deficient in the two most well validated LRRK2 substrates, Rab8a and Rab10, from two independent, deeply phenotyped healthy control lines. Thorough characterization of NGN2-induced neurons revealed divergent effects of Rab8a and Rab10 deficiency on lysosomal pH, LAMP1 association with Golgi, -synuclein insolubility and tau phosphorylation, while parallel effects on lysosomal numbers and Golgi clustering were observed. Our data demonstrate largely antagonistic effects of genetic Rab8a or Rab10 inactivation which provide discrete insight into the pathologic features of their biochemical inactivation by pathogenic LRRK2 mutation. HighlightsO_LIRab8a and Rab10 deficiency induce lysosomal and Golgi defects C_LIO_LIRab8a and Rab10 deficiency induce opposing effects on lysosomal pH C_LIO_LIRab8a KO and Rab10 KO neurons show divergent effects on synuclein and tau proteostasis C_LIO_LIInactivation of different Rab GTPases can induce distinct disease-relevant phenotypes C_LI

neuroscience↗

Aberrant phase separation is a common killing strategy of positively charged peptides in biology and human disease

Positively charged repeat peptides are emerging as key players in neurodegenerative diseases. These peptides can perturb diverse cellular pathways but a unifying framework for how such promiscuous toxicity arises has remained elusive. We used mass-spectrometry-based proteomics to define the protein targets of these neurotoxic peptides and found that they all share similar sequence features that drive their aberrant condensation with these positively charged peptides. We trained a machine learning algorithm to detect such sequence features and unexpectedly discovered that this mode of toxicity is not limited to human repeat expansion disorders but has evolved countless times across the tree of life in the form of cationic antimicrobial and venom peptides. We demonstrate that an excess in positive charge is necessary and sufficient for this killer activity, which we name polycation poisoning. These findings reveal an ancient and conserved mechanism and inform ways to leverage its design rules for new generations of bioactive peptides.

cell biology↗

Bacopa monnieri phytochemicals regulate fibroblast cell migration via modulation of focal adhesions

The Bacopa monnieri plant contains a large repertoire of active phytochemicals that have been used extensively in traditional medicine for the treatment of various complex diseases. More recently it has been shown to increase the wound healing rate in rats, though its mechanism of action is largely unknown. Here we investigated the cellular pathways activated by a methanol extract of Bacopa monnieri in human dermal fibroblasts, which play many critical roles in the wound healing program. Gene expression analysis revealed that Bacopa monnieri extract can enhance tissue repair by modulating multiple processes involved in the wound healing program such as migration, proliferation, and angiogenesis. We discovered that Bacopa monnieri extract can increase migration of fibroblasts via modulating the size and number of focal adhesions. Bacopa monnieri-mediated changes in focal adhesions are dependent on 5{beta}1 integrin activation and subsequent phosphorylation of Focal Adhesion Kinase (FAK). Altogether our results suggest that Bacopa monnieri extract could enhance the wound healing rate via modulating fibroblast migration in the wound bed.

cell biology↗

Deep neural network automated segmentation of cellular structures in volume electron microscopy

Recent advances in automated segmentation using deep neural network models allow identification of intracellular structures. This study describes a new pipeline to train a convolutional neural network for rapid and efficient detection of structures of wide range in size and complexity. AbstractThree-dimensional electron microscopy is an important imaging modality in contemporary cell biology. Identification of intracellular structures is laborious and time-consuming, however, and impairs effective use of a potentially powerful tool. Resolving this bottleneck is therefore a critical next step in frontier biomedical imaging. We describe Automated Segmentation of intracellular substructures in Electron Microscopy (ASEM), a new pipeline to train a convolutional neural network to detect structures of wide range in size and complexity. We obtain for each structure a dedicated model based on a small number of sparsely annotated ground truth annotations from only one or two cells. To improve model generalization to different imaging conditions, we developed a rapid, computationally effective strategy to refine an already trained model by including a few additional annotations. We show the successful automated identification of mitochondria, Golgi apparatus, endoplasmic reticulum, nuclear pore complexes, caveolae, clathrin coated pits and coated vesicles in cells imaged by focused ion beam scanning electron microscopy with quasi-isotropic resolution. ASEM enabled us to uncover a wide range of membrane-nuclear pore diameters within a single cell and to derive morphological metrics from clathrin coated pits and vesicles at all stages of maturation consistent with the classical constant-growth assembly model.

cell biology↗

A metagenomic view on fungal diversity in freshwater lakes

Fungi are essential components in a wide range of ecosystems and while major efforts have been spent on disentangling the diversity and functional roles of fungi in terrestrial environments, our knowledge about aquatic fungi is lagging. To address this knowledge gap, we explored metagenomes from 25 lakes from the arctic and boreal zone and one tropical reservoir with the aim of describing the community structure of fungi and fungi-like organisms (Oomycota). A second objective was to identify possible environmental factors influencing the composition of the fungal communities. Our results show that the main fungal phyla and orders are the same across all the lakes despite the differences in geographic location and prevailing climate. Still, there was differential distribution of more highly resolved taxa across the lakes that accordingly featured distinct communities, possibly caused by differential availability of carbon substrates in the lakes. A more detailed classification of sequences related to the pathogenic Oomycota genus Phytophthora clearly demonstrated that while technologies now exist for sequencing entire microbial communities in great detail, we are still severely limited by insufficient coverage of eukaryotic sequences and genomes in public databases.

ecology↗

Tracking infectious entry routes of SARS-CoV-2

SARS-CoV-2 cell entry starts with membrane attachment and ends with spike-protein (S) catalyzed membrane fusion depending on two cleavage steps, one usually by furin in producing cells and the second by TMPRSS2 on target cells. Endosomal cathepsins can carry out both. Using real-time 3D single virion tracking, we show fusion and genome penetration requires virion exposure to an acidic milieu of pH 6.2-6.8, even when furin and TMPRSS2 cleavages have occurred. We detect the sequential steps of S1-fragment dissociation, fusion, and content release from the cell surface in TMPRRS2 overexpressing cells only when exposed to acidic pH. We define a key role of an acidic environment for successful infection, found in endosomal compartments and at the surface of TMPRSS2 expressing cells in the acidic milieu of the nasal cavity. Significance StatementInfection by SARS-CoV-2 depends upon the S large spike protein decorating the virions and is responsible for receptor engagement and subsequent fusion of viral and cellular membranes allowing release of virion contents into the cell. Using new single particle imaging tools, to visualize and track the successive steps from virion attachment to fusion, combined with chemical and genetic perturbations of the cells, we provide the first direct evidence for the cellular uptake routes of productive infection in multiple cell types and their dependence on proteolysis of S by cell surface or endosomal proteases. We show that fusion and content release always require the acidic environment from endosomes, preceded by liberation of the S1 fragment which depends on ACE2 receptor engagement. One sentence summaryDetailed molecular snapshots of the productive infectious entry pathway of SARS-CoV-2 into cells

microbiology↗

DiSCs: Domains involving SETDB1 and Cohesin are critical regulators of genome topology and stem cell fate

SETDB1 is a key regulator of lineage-specific genes and endogenous retroviral elements (ERVs) through its deposition of repressive H3K9me3 mark. Apart from its H3K9me3 regulatory role, SETDB1 has seldom been studied in terms of its other potential regulatory roles. To investigate this, a genomic survey of SETDB1 binding in mouse embryonic stem cells across multiple libraries was conducted, leading to the unexpected discovery of regions bereft of common repressive histone marks (H3K9me3, H3K27me3). These regions were enriched with the CTCF motif that is often associated with the topological regulator Cohesin. Further profiling of these non-H3K9me3 regions led to the discovery of a cluster of non-repeat loci that were co-bound by SETDB1 and Cohesin. These regions, which we named DiSCs (Domains involving SETDB1 and Cohesin) were seen to be proximal to the gene promoters involved in embryonic stem cell pluripotency and lineage development. Importantly, it was found that SETDB1-Cohesin co-regulate target gene expression and genome topology at these DiSCs. Depletion of SETDB1 led to localized dysregulation of Cohesin binding thereby locally disrupting topological structures. Dysregulated gene expression trends revealed the importance of this cluster in ES cell maintenance as well as at gene islands that drive differentiation to other lineages. The unearthing of the DiSCs thus unravels a unique topological and transcriptional axis of control regulated chiefly by SETDB1.

genomics↗

Poly(A)-binding protein is an ataxin-2 chaperone that emulsifies biomolecular condensates.

Biomolecular condensation underlies the biogenesis of an expanding array of membraneless assemblies, including stress granules (SGs) which form under a variety of cellular stresses. Advances have been made in understanding the molecular grammar that dictates the behavior of a few key scaffold proteins that make up these phases but how the partitioning of hundreds of other SG proteins is regulated remains largely unresolved. While investigating the rules that govern the condensation of ataxin-2, a SG protein implicated in neurodegenerative disease, we unexpectedly identified a short 14aa sequence that acts as an ataxin-2 condensation switch and is conserved across the eukaryote lineage. We identify poly(A)-binding proteins as unconventional RNA-dependent chaperones that control this regulatory switch. Our results uncover a hierarchy of cis and trans interactions that fine-tune ataxin-2 condensation and reveal a new molecular function for ancient poly(A)-binding proteins as emulsifiers of biomolecular condensate proteins. These findings may inspire novel approaches to therapeutically target aberrant phases in disease.

cell biology↗

Synergistic inhibition of two host factors that facilitate entry of Severe Acute Respiratory Syndrome Coronavirus 2

Repurposing FDA-approved inhibitors able to prevent infection by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) could provide a rapid path to establish new therapeutic options to mitigate the effects of coronavirus disease 2019 (COVID-19). Proteolytic cleavages of the spike S protein of SARS-CoV-2, mediated by the host cell proteases cathepsin and TMPRSS2, alone or in combination, are key early activation steps required for efficient infection. The PIKfyve kinase inhibitor apilimod interferes with late endosomal viral traffic, and through an ill-defined mechanism prevents in vitro infection through late endosomes mediated by cathepsin. Similarly, inhibition of TMPRSS2 protease activity by camostat mesylate or nafamostat mesylate prevents infection mediated by the TMPRSS2-dependent and cathepsin-independent pathway. Here, we combined the use of apilimod with camostat mesylate or nafamostat mesylate and found an unexpected ~5-10-fold increase in their effectiveness to prevent SARS-CoV-2 infection in different cell types. Comparable synergism was observed using both, a chimeric vesicular stomatitis virus (VSV) containing S of SARS-CoV-2 (VSV-SARS-CoV-2) and SARS-CoV-2 virus. The substantial ~5-fold or more decrease of half maximal effective concentrations (EC50 values) suggests a plausible treatment strategy based on the combined use of these inhibitors. IMPORTANCEInfection by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is causing the coronavirus disease 2019 (COVID-2019) global pandemic. There are ongoing efforts to uncover effective antiviral agents that could mitigate the severity of the disease by controlling the ensuing viral replication. Promising candidates include small molecules that inhibit the enzymatic activities of host proteins, thus preventing SARS-CoV-2 entry and infection. They include Apilimod, an inhibitor of PIKfyve kinase and camostat mesylate and nafamostat mesylate, inhibitors of TMPRSS2 protease. Our research is significant for having uncovered an unexpected synergism in the effective inhibitory activity of apilimod used together with camostat mesylate or with nafamostat mesylate.

microbiology↗

Spatial proximity of homologous centromere DNA sequences facilitated karyotype diversity and seeding of evolutionary new centromeres

Centromeres of Candida albicans form on unique and different DNA sequences but a closely related species, Candida tropicalis, possesses homogenized inverted repeat (HIR)-associated centromeres. To investigate the mechanism of centromere-type transition, we improved the fragmented genome assembly and constructed a chromosome-level genome assembly of C. tropicalis by employing PacBio sequencing, chromosome conformation capture sequencing (3C-seq), chromoblot, and genetic analysis of engineered aneuploid strains. Further, we analyzed the 3D genome organization using 3C-seq data, which revealed spatial proximity among the centromeres as well as telomeres of seven chromosomes in C. tropicalis. Intriguingly, we observed evidence of inter-centromeric translocations in the common ancestor of C. albicans and C. tropicalis. Identification of putative centromeres in closely related Candida sojae, Candida viswanathii and Candida parapsilosis indicates loss of ancestral HIR-associated centromeres and establishment of evolutionary new centromeres (ENCs) in C. albicans. We propose that spatial proximity of the homologous centromere DNA sequences facilitated karyotype rearrangements and centromere type transitions in human pathogenic yeasts of the CUG-Ser1 clade.

genetics↗

Identification and Utilization of Copy Number Information for Correcting Hi-C Contact Map of Cancer Cell Line

MotivationHi-C and its variant techniques have been developed to capture the spatial organization of chromatin. Normalization of Hi-C contact maps is essential for accurate modeling and interpretation of genome-wide chromatin conformation. Most Hi-C correction methods are originally developed for normal cell lines and mainly target systematic biases. In contrast, cancer genomes carry multi-level copy number variations (CNVs). Copy number influences interaction frequency between genomic loci. Therefore, CNV-driven bias needs to be corrected for generating euploid-equivalent chromatin contact maps.\n\nResultsWe developed HiCNAtra framework that extracts read depth (RD) signal from Hi-C or 3C-seq reads to generate the high-resolution CNV profile and use this information to correct the contact map. We proposed the \"entire restriction fragment\" counting for better estimation of the RD signal and generation of CNV profiles. HiCNAtra integrates CNV information along with other systematic biases for explicitly correcting the interaction matrix using Poisson regression model. We demonstrated that RD estimation of HiCNAtra recapitulates the whole-genome sequencing (WGS)-derived coverage signal of the same cell line. Benchmarking against OneD method (only explicit method to target CNV bias) showed that HiCNAtra fared better in eliminating the impact of CNV on the contact maps.\n\nAvailability and implementationHiCNAtra is an open source software implemented in MATLAB and is available at https://github.com/AISKhalil/HiCNAtra.

bioinformatics↗

Aneuploidy Spectrum Analysis as a Primer for Copy Number Profiling of Cancer Cells

MotivationHyperploidy and segmental aneuploidy are hallmarks of cancer cells due to chromosome segregation errors and genomic instability. In such situations, accurate aneuploidy profiling of cancer data is critical for calibration of copy number (CN)-detection tools. Additionally, cancer cell populations suffer from different levels of clonal heterogeneity and aneuploidy alterations over time. The degree of heterogeneity adversely affects the segregation of the depth of coverage (DOC) signal into integral CN states. This, in turn, strongly influences the reliability of this data for ploidy profiling and copy number variation (CNV) analysis.\n\nResultsWe developed AStra framework for aneuploidy profiling of cancer data and assessing their suitability for copy number analysis without any prior knowledge of the input sequencing data. AStra estimates the best-fit aneuploidy profile as the spectrum with most genomic segments around integral CN states. We employ this spectrum to extract the CN-associated features such as the homogeneity score (HS), whole-genome ploidy level, and CN correction factor. The HS measures the percentage of genomic regions around CN states. It is used as a reliability assessment of sequencing data for downstream aneuploidy profiling and CNV analysis. We evaluated the accuracy of AStra using 31 low-coverage datasets from 20 cancer cell lines. AStra successfully identified the aneuploidy spectrum of complex cell lines with HS greater than 75%. Benchmarking against nQuire tool showed that AStra is superior in detecting the ploidy level using both low- and high-coverage data. Furthermore, AStra accurately estimated the ploidy of 26/27 strains of MCF7 (hyperploid) cell line which exhibit varied levels of aneuploidy spectrum and heterogeneity. Remarkably, we found that HS is strongly correlated with the doubling time of these strains.\n\nAvailability and implementationAStra is an open source software implemented in Python and is available at https://github.com/AISKhalil/AStra

bioinformatics↗

Hierarchical Discovery of Large-scale and Focal Copy Number Alterations in Low-coverage Cancer Genomes

MotivationDetection of copy number alterations (CNA) is critical to understand genetic diversity, genome evolution and pathological conditions such as cancer. Cancer genomes are plagued with widespread multi-level structural aberrations of chromosomes that pose challenges to discover CNAs of different length scales with distinct biological origin and function. Although several tools are available to identify CNAs using read depth (RD) of coverage, they fail to distinguish between large-scale and focal alterations due to inaccurate modeling of the RD signal of cancer genomes. These tools are also affected by RD signal variations, pronounced in low-coverage data, which significantly inflate false detection of change points and inaccurate CNA calling.\n\nResultsWe have developed CNAtra to hierarchically discover and classify large-scale and focal copy number gain/loss from whole-genome sequencing (WGS) data. CNAtra provides an analytical and visualization framework for CNV profiling using single sequencing sample. CNAtra first utilizes multimodal distribution to estimate the copy number (CN) reference from the complex RD profile of the cancer genome. We utilized Savitzy-Golay filter and Modified Varri segmentation to capture the change points. We then developed a CN state-driven merging algorithm to identify the large segments with distinct copy number. Next, focal alterations were identified in each large segment using coverage-based thresholding to mitigate the adverse effects of signal variations. We tested CNAtra calls using experimentally verified segmental aneuploidies and focal alterations which confirmed CNAtras ability to detect and distinguish the two alteration phenomena. We used realistic simulated data for benchmarking the performance of CNAtra against other detection tools where we artificially spiked-in CNAs in the original cancer profiles. We found that CNAtra is superior in terms of precision, recall, and f-measure. CNAtra shows the highest sensitivity of 93% and 97% for detecting focal and large-scale alterations respectively. Visual inspection of CNAs showed that CNAtra is the most robust detection tool for low-coverage cancer data.\n\nAvailability and implementationCNAtra is an open source software implemented in MATLAB, and is available at https://github.com/AISKhalil/CNAtra

bioinformatics↗

Alpha-Synuclein is a Target of Fic-mediated Adenylylation/AMPylation: Implications for Parkinson’s Disease

During disease, cells experience various stresses that manifest as an accumulation of misfolded proteins and eventually lead to cell death. To combat this stress, cells activate a pathway called UPR (Unfolded Protein Response) that functions to maintain ER (endoplasmic reticulum) homeostasis and determines cell fate. We recently reported a hitherto unknown mechanism of regulating ER stress via a novel post-translational modification (PTM) called Fic-mediated Adenylylation/AMPylation. Specifically, we showed that the human Fic (filamentation induced by cAMP) protein, HYPE/FicD, catalyzes the addition of an AMP (adenosine monophosphate) to the ER chaperone, BiP, to alter the cells UPR-mediated response to misfolded proteins. Here, we report that we have now identified a second target for HYPE - alpha-Synuclein (Syn), a presynaptic protein involved in Parkinsons disease (PD). Aggregated Syn has been shown to induce ER stress and elicit neurotoxicity in PD models. We show that HYPE adenylylates Syn and reduces phenotypes associated with Syn aggregation in vitro, suggesting a possible mechanism by which cells cope with Syn toxicity.\n\nHIGHLIGHTSO_LIAggregated forms of the presynaptic protein Syn cause neurotoxicity and induce ER stress in cellular and animal models of Parkinsons disease.\nC_LIO_LIWe have identified Syn as a novel target for the human Fic protein, HYPE, a key regulator of ER homeostasis.\nC_LIO_LIHYPE adenylylates Syn and reduces the aggregation of recombinant Syn\nC_LIO_LIFic-mediated adenylylation/AMPylation is a possible mechanism by which cells cope with Syn toxicity.\nC_LI\n\nGraphic Abstract O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY C_FIG_DISPLAY

biochemistry↗

Kinetic And Structural Parameters Governing Fic-Mediated Adenylylation/AMPylation of the Hsp70 chaperone, BiP/GRP78

Fic (filamentation induced by cAMP) proteins regulate diverse cell signaling events by post-translationally modifying their protein targets, predominantly by the addition of an AMP (adenosine monophosphate). This modification is called Fic-mediated Adenylylation or AMPylation. We previously reported that the human Fic protein, HYPE/FicD, is a novel regulator of the unfolded protein response (UPR) that maintains homeostasis in the endoplasmic reticulum (ER) in response to stress from misfolded proteins. Specifically, HYPE regulates UPR by adenylylating the ER chaperone, BiP/GRP78, which serves as a sentinel for UPR activation. Maintaining ER homeostasis is critical for determining cell fate, thus highlighting the importance of the HYPE-BiP interaction. Here, we study the kinetic and structural parameters that determine the HYPE-BiP interaction. By measuring the binding and kinetic efficiencies of HYPE in its activated (Adenylylation-competent) and wild type (de-AMPylation-competent) forms for BiP in its wild type and ATP-bound conformations, we determine that HYPE displays a nearly identical preference for the wild type and ATP-bound forms of BiP in vitro and preferentially de-AMPylates the wild type form of adenylylated BiP. We also show that AMPylation at BiPs Thr366 versus Thr518 sites differentially affect its ATPase activity, and that HYPE does not adenylylate UPR accessory proteins like J-protein ERdJ6. Using molecular docking models, we explain how HYPE is able to adenylylate Thr366 and Thr518 sites in vitro. While a physiological role for AMPylation at both the Thr366 and Thr518 sites has been reported, our molecular docking model supports Thr518 as the structurally preferred modification site. This is the first such analysis of the HYPE-BiP interaction and offers critical insights into substrate specificity and target recognition.

biochemistry↗

DNA replication initiator proteins facilitate CENPA loading on early replicating compact chromatin

Spatiotemporal regulation in DNA replication maintains kinetochore stability. The epigenetically regulated centromeres (CENs) in the budding yeast Candida albicans have unique DNA sequences, replicate early and are clustered throughout the cell cycle. In this study, the genome-wide occupancy of replication initiation protein Orc4 reveals its abundance at all CENs in C. albicans. Orc4 associates with four different DNA motifs, one of which coincides with tRNA genes. Hi-C combined with genome-wide replication timing analyses identify enriched interactions among early or late replicating Orc4-bound regions. A simulated polymer model of chromosomes reveals that early replicating and strongly enriched Orc4-bound sites localize towards the kinetochores. Orc4 is constitutively localized to CENs, and both Orc4 and Mcm2 stabilize CENPA. CENPA chaperone Scm3 localizes at the kinetochore during anaphase, coinciding with the loading time of CENPA. We propose that this spatiotemporal nuclear localization of Orc4, with Mcm2 and Scm3, recruits CENPA and stabilizes centromeric chromatin.

molecular biology↗

Holocene DNA sequences -- a dream come true

Microscopic marine planktons have played a major role in the Earths ecosystem and accounts for half the globes primary production. Predicting the fate of marine planktons is imperative to understanding how ocean life will change in future centuries and how organisms have adapted to changes in the past over long timescales (over thousands of years). Studies of revived resting spores of marine diatoms will serve as excellent proxies of environmental change in marine environments. Thus far, only about a century old marine diatom resting spores could be revived. This severely limited the use of diatom resting spores to investigate the effects of environmental perturbations over longer time scales. Here, we, for the first time report revival of thousands of years old resting spores from the deposits of ancient diatoms (Chaetoceros) in sub-seafloor sediments using a revival protocol that involved recreating the ancient environmental conditions (salinity, temperature and light). Our revived diatom resting spores samples range from recent (0-80 years) to [~]7200 years old. Importantly, we also extracted the DNA from the ancient resting spores of Chaetoceros species from the Baltic Sea. Our findings will enable us to compare DNA sequence data obtained from these natural archives of resurrected organisms and provide predictive models to forecast evolutionary responses of natural populations to environmental changes resulting from natural and anthropogenic stressors, including climate change\n\nSignificance StatementOur results address the important topic of adaptive evolution in marine species due to climate and environmental change induced due to anthropogenic perturbations. We present a new model system Chaetoceros muelleri which will help us address important evolutionary and long-term adaptation questions across evolutionary timescales. Our study reports (1) the revival of recent (0-80 years) to ancient (7200 years old) resting spores of Chaetoceros (2) the extraction of DNA and amplification of chloroplast and ribosomal genes from recent and ancient ([~]1300 years old) resting spores of Chaetoceros (3) Radiocarbon dating to determine age of sediments (4) Identification of species by reviving the resting spores (5) Baltic sea an excellent ecosystem to study long-term effects of environment on species adaptation

evolutionary biology↗