Biology subjects

Cresko, W. A.

Publications and source records attributed to Cresko, W. A..

At least 19 recordsLinked to original sources

bioRxiv2026

Functionally convergent anti-predator morphologies arise through divergent cellular strategies in Daphnia

Phenotypic plasticity exemplifies how environmental signals can shape organismal development, yet the cellular mechanisms translating ecological cues into adaptive morphologies remain incompletely characterized. Many species of Daphnia (freshwater crustaceans) develop a diverse array of inducible defenses in response to predator chemical cues (kairomones), providing a tractable system for examining how ecological pressures are transduced through developmental mechanisms. Daphnia lumholtzi produce elongated head and tailspines in response to kairomones. How this occurs at the cellular level, through changes in cell size, proliferation, or both, is currently unknown. To address this question, we quantified the temporal dynamics of cell proliferation in D. lumholtzi across 72 hours following kairomone exposure using EdU incorporation (marking proliferating cells) and DAPI staining (to quantify total nuclei). Predator cue exposure induced a three-phase proliferative response: initiation within 24 hours (slightly increased proliferation and total cells), a transitional plateau at 48 hours (minimal effects in both treatments), and commitment by 72 hours (strong increases in both proliferation and cell accumulation). Headspines exhibited higher proliferation than tailspines, suggesting anterior- posterior developmental prioritization. Treated animals maintained smaller average cell sizes throughout the response, consistent with continuous addition of newly divided cells rather than cell enlargement. Unlike the delayed-division strategy in D. longicephala or bilayer formation in D. pulex, D. lumholtzi employs sustained hyperplasia, demonstrating that the same selective pressure produces similar ecological outcomes through mechanistically distinct developmental programs. Our findings bridge ecological signals with cellular responses, exemplifying eco-evo- devo integration whereby environmental pressures (predation) are transduced through developmental processes (cell proliferation dynamics) to generate adaptive and heritable morphological diversity across ecological and evolutionary timescales.

cell biology↗

bioRxiv2026

Lineage-specific change in craniofacial genetic networks of syngnathid fishes revealed by integrating multiomics across fishes

Cranial neural crest (CNC) cells are essential developmental contributors to the remarkable diversity of vertebrate skull shapes, yet how underlying gene regulatory networks (GRNs) evolve to produce highly derived morphologies remains a challenging question. Syngnathid fishes (seahorses, pipefishes, pipehorses, and seadragons) are an opportune family of species in which to address this problem because of their unusual and extensive cranial diversity and their loss of craniofacial patterning genes, fgf3 and fgf4. Here we investigated whether syngnathid craniofacial evolution experienced only a few localized network changes or required global rewiring of CNC GRNs. Using comparative single-cell RNA sequencing, ATAC-seq and whole genome alignments across Gulf pipefish, threespine stickleback, and zebrafish, we found that the core pharyngeal arch CNC gene network is notably conserved in syngnathids despite their derived morphology. However, we identified key local changes including expression of fgf22 in percomorph CNC-derived pharyngeal arch cells that is not shared with more basally diverging zebrafish, as well as syngnathid-specific changes in conserved regulatory elements associated with the genes ece1 and spry2. We propose that, while loss of fgf3 expression causes severe craniofacial defects in zebrafish, pharyngeal CNC expression of fgf22 in the percomorph fish lineage provided functional redundancy and relaxed constraint on fgf3/4, and that altered regulation of Fgf pathway modulators could contribute to craniofacial elaboration. Our findings support a model in which local GRN modifications, rather than widespread network rewiring, underlie the evolution of derived syngnathid craniofacial structures. SignificanceUnderstanding how developmental genetic changes drive the evolution of unique traits remains a long-standing challenge in biology. In the case of syngnathid fishes (pipefishes, seahorses, and seadragons), previous genomic studies identified candidate craniofacial gene losses which are proposed to relate to their elongate and derived heads, but the developmental impact of these losses is unknown. Through gene expression and comparative genomics analyses, we find that these fishes have distinct changes to craniofacial gene regulatory networks including gene content losses and gene expression gains and losses. Our study suggests that morphological adaptations may arise from multiple key changes within largely conserved developmental regulatory networks.

evolutionary biology↗

bioRxiv2026

Genome-wide Analysis Reveals High Genomic Diversity and Panmixia in Bay Pipefish (Syngnathus leptorhynchus) from Coos Bay, Oregon

The over 300 species of fishes in the charismatic family Syngnathidae (seahorses, pipefish, pipehorses, and seadragons) exhibit remarkable morphological and reproductive adaptations. Most syngnathid species inhabit shallow coastal regions where they are vulnerable to human activities, including habitat degradation and collection for use in traditional medicine and the aquarium trade. A gap remains in our understanding of within-species genetic diversity and population structure for most of the species in this family--information that is crucial for establishing baselines to detect future human-driven changes. Here, we investigate fine-scale population structure and genomic diversity in the bay pipefish (Syngnathus leptorhynchus), one of the relatively few temperate lineages within the Syngnathidae. Bay pipefish are habitat specialists that are closely associated with eelgrass (Zostera marina) along the Pacific coast of North America. Due to the patchy and changing nature of eelgrass habitat, bay pipefish provide an instructive case for using population genomics to explore patterns of connectivity in a dynamic coastal environment. We sampled 116 individuals from two locations separated by approximately 17 km in the Coos Bay estuary (Oregon, USA) and used restriction site-associated DNA sequencing (RAD-seq) to discover high and consistent genetic diversity at both sampling locations, with no indication of inbreeding. Genome-wide patterns of genetic variation showed minimal differentiation between the sampling sites, with levels of divergence indistinguishable from those expected under random sampling. Linkage disequilibrium was low and declined rapidly, and estimates of effective population size indicate a large, well-connected population within Coos Bay. These results establish a crucial genomic baseline for understanding how bay pipefish populations may respond to ongoing changes in their eelgrass habitat and offer a genomic framework for conservation and comparative studies across the Syngnathidae.

evolutionary biology↗

bioRxiv2025

Predator induced phenotypes are inherited over four generations in genetically identical Daphnia lumholtzi

Teaser TextCan the ghosts of environments past shape organismal phenotypes of future generations? In an experiment with clonal Daphnia lumholtzi, we reveal that predator-induced changes in body shape in one generation can persist across several unexposed generations, even when the predator signal is long gone. Exposing only the first generation to predator cues, we tracked morphological shifts through five generations of genetically identical individuals. We found that these induced plastic phenotypes persisted to the F4 generation before fading in F5. This discovery supports the importance of non-genetic inheritance and underscores the powerful interplay between ancestral and current environments in shaping organismal form and function. Environmental variation can induce phenotypic changes through adaptation of populations and acclimation of individuals. While genetic adaptation creates persistent change within a population via allele frequency shifts, reversible plastic phenotypes can be inherited through non-genetic mechanisms. However, most transgenerational plasticity studies examine generations where direct embryonic or germline exposure to environmental cues cannot be excluded. Empirical evidence for persistence definitively beyond the critical threshold for distinguishing true transgenerational plasticity from in utero exposure remains scarce, particularly for vertebrate predator-induced defenses. We measured phenotypic effects of vertebrate predator exposure in the clonally reproducing water flea, Daphnia lumholtzi, isolating environmental effects from genetic variation. We exposed the F0 generation to fish conditioned media, then measured morphological defenses in definitively unexposed F3, F4, and F5 generations characterizing the temporal dynamics of non-genetic inheritance. Predator-induced morphologies persisted through F4 before receding in F5, demonstrating that non-genetic effects extend well beyond the embryonically exposed F1 and germ cell exposed F2 generations. This provides rare empirical evidence for transgenerational plasticity lasting through F4, without confounding genetic variation. We also examined ontogenetic patterns of somatic and defensive trait development, revealing trait-specific temporal dynamics in transgenerational effect expression and decay. These results highlight how current and ancestral environments interact to determine phenotypic variation across generations and underscores the ecological significance of non-genetic inheritance in natural populations, particularly for understanding population responses to environmental change and predator reintroduction. Characterizing molecular mechanisms underlying transgenerational phenotypic plasticity remains critical for predicting persistence and ecological consequences of non-genetic inheritance.

evolutionary biology↗

bioRxiv2025

Spontaneous mutant in threespine stickleback connects endosome trafficking disorders and inflammatory bowel diseases via changes in the gut microbiome

Endosomes are organelles that sort and traffic materials to different cellular compartments to enable performance of other organelles. One group of organelles supported by endosomes are lysosome related organelles (LROs) - which perform specialized functions using endocytosed or recycled materials from endosomes. LROs include melanosomes, lytic granules, platelet dense granules, lamellar bodies, and more. Individuals with endosome trafficking disorders commonly present with oculocutaneous albinism due to insufficient trafficking to - and maturation of - melanosomes. While the loss of pigment is an easily identifiable phenotype, mutations in endosome trafficking can also cause multi-organ system symptoms due to more broad disruption of LROs. Different endosome trafficking mutations impact LRO maturation at different degrees of severity and can impact a subset or all LROs leading to a wide range of symptomologies. Endosome trafficking disorders can present with oculocutaneous albinism (caused by mutated melanosomes), blood diathesis (caused by mutated platelet dense granules), pulmonary fibrosis (caused by mutated lamellar bodies), or chronic inflammation and inflammatory bowel disease (IBD) (caused by mutated lytic granules), as well as other symptoms. The shared inflammatory patterns of Hermansky-Pudlak Syndrome (HPS) and Inflammatory Bowel Disease (IBD) are well studied. However, impacts of this shared gastrointestinal inflammation on the gut microbiome remain unexplored. Using a spontaneously identified mutant family of threespine stickleback fish, we characterize changes in LROs and symptoms of oculocutaneous albinism. We further demonstrate that the shared gastrointestinal phenotypes of HPS and IBD extend to the gut microbiome showing similar shifts in microbial communities consistent with IBD. We argue endosome trafficking models should be explored as models to study the gut microbiome in addition to inflammatory phenotypes in IBD, and importantly, be used to test microbial/dietary interventions for both IBD and endosome trafficking disorders.

genetics↗

bioRxiv2024

Quantitative Genetics of Microbiome Mediated Traits

Multicellular organisms host a rich assemblage of associated microorganisms, collectively known as their "microbiomes". Microbiomes have the capacity to influence their hosts fitnesses, but the conditions under which such influences contribute to evolution are not clear. This is due in part to a lack of a comprehensive theoretical framework for describing the combined effects of host and associated microbes on phenotypic variation. Here we address this gap by extending the foundations of quantitative genetic theory to include host-associated microbes, as well as alleles of hosts, as factors that explain quantitative host trait variation. We introduce a way to partition host-associated microbiomes into components relevant for predicting a microbiome-mediated response to selection. We then apply our general framework to a simulation model of microbiome inheritance to illustrate principles for predicting host trait dynamics, and to generalize classical narrow and broad sense heritabilities to account for microbial effects. We demonstrate that microbiome-mediated responses to host-level selection can arise from various transmission modes, not solely vertical, but that the contribution of non-vertical modes can depend strongly on host life history. Our work lays a foundation for integrating microbiome-mediated host variation and adaptation into our understanding of natural variation.

evolutionary biology↗

bioRxiv2024

Single Cell RNA Sequencing Provides Clues for the Developmental Genetic Basis of Syngnathidae's Evolutionary Adaptations

Seahorses, pipefishes, and seadragons are fishes from the family Syngnathidae that have evolved extraordinary traits including male pregnancy, elongated snouts, loss of teeth, and dermal bony armor. The developmental genetic and cellular changes that led to the evolution of these traits are largely unknown. Recent syngnathid genome assemblies revealed suggestive gene content differences and provide the opportunity for detailed genetic analyses. We created a single cell RNA sequencing atlas of Gulf pipefish embryos to understand the developmental basis of four traits: derived head shape, toothlessness, dermal armor, and male pregnancy. We completed marker gene analyses, built genetic networks, and examined spatial expression of select genes. We identified osteochondrogenic mesenchymal cells in the elongating face that express regulatory genes bmp4, sfrp1a, and prdm16. We found no evidence for tooth primordia cells, and we observed re-deployment of osteoblast genetic networks in developing dermal armor. Finally, we found that epidermal cells expressed nutrient processing and environmental sensing genes, potentially relevant for the brooding environment. The examined pipefish evolutionary innovations are composed of recognizable cell types, suggesting derived features originate from changes within existing gene networks. Future work addressing syngnathid gene networks across multiple stages and species is essential for understanding how their novelties evolved.

evolutionary biology↗

bioRxiv2022

Host genomic variation shapes gut microbiome diversity in threespine stickleback fish

Variation among host-associated microbiomes is well documented across species, populations, and individuals. However, the relative importance of host genetic differences for microbiome variation has been difficult to study. While research in humans has shown that genetic variation influences microbiome differences, confounding environmental effects have been very difficult to control. Isogenic laboratory models help isolate host genetic variants to test for influences of the environment or large-effect mutations on the microbiome, but such studies seldom incorporate natural genetic variation. Thus, although many important factors potentially impacting the microbiome have been identified, most studies have failed to test for the direct influence of natural host-genetic variation on microbiome differences within a controlled environment. Understanding the relationship between host-genetic and microbial variation also has biomedical implications, such as understanding why some humans are more susceptible to chronic inflammatory disorders like Crohns Disease and Ulcerative Colitis. To directly assess the relationship between host-genetic variation and microbiome variation, we performed a common garden experiment using laboratory lines of genetically divergent populations of threespine stickleback fish - a species that is an outbred model organism commonly used for determining the genetic basis of complex traits in the context of natural genetic variation. Using germ-free derivation and the powerful common garden design with these divergent lines, as well as hybrids between them, we detected clear associations between stickleback genetic dissimilarity and microbiome dissimilarity. Using genome-wide RAD-seq data we also identified regions of the genome underlying differences in microbiome composition. Importantly, we highlight that heritable morphological traits such as body size that are correlated with microbiome dissimilarity also need consideration in future microbiome studies.

evolutionary biology↗

bioRxiv2022

Candidate Genes Underlying Wolbachia-Associated Plastic Recombination Revealed by Ovarian Transcriptomics of D. melanogaster

Phenotypic plasticity is prevalent in nature and can facilitate the acclimation of organisms to changing environments. Recombination rate is plastic in a diversity of organisms and under a variety of stressful conditions. However, the recent finding that Wolbachia pipientis induces plastic recombination in Drosophila melanogaster was surprising because Wolbachia is not strictly considered a stressor to this host. We investigate the molecular mechanisms of Wolbachia-associated plastic recombination by comparing the ovarian transcriptomes of D. melanogaster infected and uninfected with Wolbachia. Our data suggest that infection explains a small amount of transcriptional variation but specifically affects genes related to cell cycle, translation, and metabolism. We also find enrichment of cell division and recombination processes among genes with infection-associated differential expression. Broadly, the transcriptomic changes identified in this study provide insight for the mechanisms of microbe-mediated plastic recombination, an important but poorly understood facet of host-microbe dynamics. Significance StatementThough it is documented that Wolbachia is associated with increased recombination in D. melanogaster, the underlying mechanisms remain unknown. Here we use ovarian transcriptomics in Wolbachia-infected and uninfected flies to identify candidate genes underlying Wolbachia-associated plastic recombination. We find that infection alters ovarian gene expression in subtle ways, and also identify exciting candidate genes for functional analysis in subsequent work. These candidate genes may be the first step in determining the molecular mechanisms underlying Wolbachia-associated plastic recombination. Moreover, our data contribute to the growing body of knowledge surrounding how Wolbachia affects host gene expression, and highlights how context-dependent these effects are.

evolutionary biology↗

bioRxiv2021

Single cell Iso-Sequencing enables rapid genome annotation for scRNAseq analysis

Single cell RNA sequencing (scRNAseq) is a powerful technique that continues to expand across various biological applications. However, incomplete 3' UTR annotations in less developed or non-model systems can impede single cell analysis resulting in genes that are partially or completely uncounted. Performing scRNAseq with incomplete 3' UTR annotations can impede the identification of cell identities and gene expression patterns and lead to erroneous biological inferences. We demonstrate that performing single cell isoform sequencing (ScISOr-Seq) in tandem with scRNAseq can rapidly improve 3' UTR annotations. Using threespine stickleback fish (Gasterosteus aculeatus), we show that gene models resulting from a minimal embryonic ScISOr-Seq dataset retained 26.1% greater scRNAseq reads than gene models from Ensembl alone. Furthermore, pooling our ScISOr-Seq isoforms with a previously published adult bulk Iso-Seq dataset from stickleback, and merging the annotation with the Ensembl gene models, resulted in a marginal improvement (+0.8%) over the ScISOr-Seq only dataset. In addition, isoforms identified by ScISOr-Seq included thousands of new splicing variants. The improved gene models obtained using ScISOr-Seq lead to successful identification of cell types and increased the reads identified of many genes in our scRNAseq stickleback dataset. Our work illuminates ScISOr-Seq as a cost-effective and efficient mechanism to rapidly annotate genomes for scRNAseq.

genetics↗

bioRxiv2021

Leafy and Weedy Seadragon Genomes Connect Genic and Repetitive DNA Features to the Extravagant Biology of Syngnathid Fishes

Seadragons are a remarkable lineage of teleost fishes, and they are members of the family Syngnathidae renowned for having evolved male pregnancy. Comprising three known species, seadragons are widely recognized and admired for their fantastical body forms and coloration, and their specific habitat requirements have made them flagship representatives for marine conservation and natural history interests. Until recently, a gap has been the lack of significant genomic resources for seadragons. We have produced gene-annotated, chromosome-scale genome models for the leafy and weedy seadragon to advance investigations into evolutionary innovation and elaboration of morphological traits in seadragons as well as their pipefish and seahorse relatives. We identified several interesting features specific to seadragon genomes, including divergent non-coding regions near a developmental gene important for integumentary outgrowth, a high genome-wide density of repetitive DNA, and recent expansions of transposable elements and a vesicular trafficking gene family. Surprisingly, comparative analyses leveraging the seadragon genomes and additional syngnathid and outgroup genomes revealed striking, syngnathid-specific losses in the family of fibroblast growth factors (FGFs), which likely involve re-organization of highly conserved gene regulatory networks in ways that have not previously been documented in natural populations. The resources presented here serve as important tools for future evolutionary studies of developmental processes in syngnathids and will be a key resource for conservation studies of the extravagant seadragons and their relatives.

genomics↗

bioRxiv2019

QTL mapping of intestinal neutrophil variation and inflammation between threespine stickleback populations reveals links to neurodegenerative disease

Host selection is often required to foster beneficial microbial symbionts and suppress deleterious pathogens. In animals, the host immune system is at the center of this relationship. Failed host immune system-microbial interactions can result in a persistent inflammatory response in which the immune system indiscriminately attacks resident microbes, and at times the host cells themselves, leading to diseases such as Ulcerative Colitis, Crohns Disease, and Psoriasis. Host genetic variation has been linked to both microbiome diversity and to severity of such inflammatory disease states in humans. However, the microbiome and inflammatory states manifest as quantitative traits, which encompass many genes interacting with one another and the environment. The mechanistic relationships among all of these interacting components are still not clear. Developing natural genetic models of host-microbe interactions is therefore fundamental to understanding the complex genetics of these and other diseases. Threespine stickleback (Gasterosteus aculeatus) fish are a tractable model for attacking this problem because of abundant population-level genetic and phenotypic variation in the gut inflammatory response. Previous work in our laboratory identified genetically divergent stickleback populations exhibiting differences in intestinal neutrophil activity. We took advantage of this diversity to genetically map variation in an emblematic element of gut inflammation - intestinal neutrophil recruitment - using an F2-intercross mapping framework. We identified three regions of the genome associated with increased intestinal inflammation containing several promising candidate genes. Within these regions we found candidates in the Coagulation/Complement System, NFkB and MAPK pathways along with several genes associated with neurodegenerative diseases commonly accompanying intestinal inflammation as a secondary symptom. These findings highlight the utility of using naturally genetically diverse evolutionary mutant models such as threespine stickleback to better understand interactions among host genetic diversity and microbiome variation in health and disease states.

genetics↗

bioRxiv2019

A few stickleback suffice for the transport of alleles to new lakes

Threespine stickleback populations provide a striking example of local adaptation to divergent habitats in populations that are connected by recurrent gene flow. These small fish occur in marine and freshwater habitats throughout the Northern Hemisphere, and in numerous cases the smaller freshwater populations have been established \"de novo\" from marine colonists. Independently evolved freshwater populations show similar phenotypes that have been shown to derive largely from the same standing genetic variants. Geographic isolation prevents direct migration between the freshwater populations, strongly suggesting that these shared locally adaptive alleles are transported through the marine population. However it is still largely unknown how gene flow, recombination, and selection jointly impact the standing variation that might fuel this adaptation. Here we use individual-based, spatially explicit simulations to determine the levels of gene flow that best match observed patterns of allele sharing among habitats in stickleback. We aim to better understand how gene flow and local adaptation in large metapopulations determine the speed of adaptation and re-use of standing genetic variation. In our simulations we find that repeated adaptation uses a shared set of alleles that are maintained at low frequency by migration-selection balance in oceanic populations. This process occurs over a realistic range of intermediate levels of gene flow that match previous empirical population genomic studies in stickleback. Examining these simulations more deeply reveals how lower levels of gene flow leads to slow, independent adaptation to different habitats, whereas higher levels gene flow leads to significant mutation load - but an increased probability of successful population genomic scans for locally adapted alleles. Surprisingly, we find that the genealogical origins of most freshwater adapted alleles can be traced back to the original generation of marine individuals that colonized the lakes, as opposed to subsequent migrants. These simulations provide deeper context for existing studies of stickleback evolutionary genomics, and guidance for future empirical studies in this model. More broadly, our results support existing theory of local adaptation but extend it by more completely documenting the genealogical history of adaptive alleles in a metapopulation.

evolutionary biology↗

bioRxiv2019

Genetic divergence outpaces phenotypic divergence among threespine stickleback populations in old freshwater habitats

Species such as threespine stickleback fish that are distributed across landscapes with divergent selective environments and that have diversified on different time scales can be valuable for understanding evolutionary processes. Here we synthesize high resolution genotypic and phenotypic data to explore a largely unstudied distribution of threespine stickleback populations living in marine and freshwater habitats along coastal and inland regions of northwestern Oregon. Because many inland aquatic habitats of Oregon were not glaciated during the last ice age, we hypothesized that some extant Oregon lake and river stickleback are descended from freshwater populations that were established long before the well-studied, postglacial freshwater populations of Alaska. Here we characterize the major phenotypic and genetic axes of differentiation in Oregon stickleback, and compare these patterns to their Alaska counterparts currently inhabiting regions that were covered by ice during the last glacial maximum. Phenotypic variation in Oregon stickleback is predictably partitioned between oceanic and freshwater habitats. However, we also found that genetic divergence in Oregon ecotypes is much greater than divergence among studied stickleback populations in Alaska. Additionally, we report a surprising phenotypic and genetic affinity between oceanic stickleback with freshwater populations that live far inland in two Oregon river basins.

evolutionary biology↗

bioRxiv2019

Complex pleiotropic genetic architecture of evolved heat stress and oxidative stress resistance in the nematode Caenorhabditis remanei

The adaptation of complex organisms to changing environments has been a central question in evolutionary quantitative genetics since its inception. The structure of the genotype-phenotype maps is critical because pleiotropic effects can generate widespread correlated responses to selection and potentially restrict the extent of evolutionary change. In this study we use experimental evolution to dissect the genetic architecture of natural variation for acute heat stress and oxidative stress response in the nematode Caenorhabiditis remanei. Previous work in the classic model nematode C. elegans has found that abiotic stress response is controlled by a handful of genes of major effect and that mutations in any one of these genes can have widespread pleiotropic effects on multiple stress response traits. Here, we find that acute heat stress response and acute oxidative response in C. remanei are polygenic, complex traits, with hundreds of genomic regions responding to selection. In contrast to expectation from mutation studies, we find that evolved acute heat stress and acute oxidative stress response for the most part display independent genetic bases. This lack of correlation is reflected at the levels of phenotype, gene expression, and in the genomic response to selection. Thus, while these findings support the general view that rapid adaptation can be generated by changes at hundreds to thousands of sites in the genome, the architecture of segregating variation is likely to be strongly parcellated by the pleiotropic structure of the underlying genetic networks.

evolutionary biology↗

bioRxiv2018

Highly reproducible 16S sequencing facilitates measurement of host genetic influences on the stickleback gut microbiome

Multicellular organisms interact with resident microbes in important ways, and a better understanding of host-microbe interactions is aided by tools such as high-throughput 16S sequencing. However, rigorous evaluation of the veracity of these tools in a different context from which they were developed has often lagged behind. Our goal was to perform one such critical test by examining how variation in tissue preparation and DNA isolation could affect inferences about gut microbiome variation between two genetically divergent lines of threespine stickleback fish maintained in the same lab environment. Using careful experimental design and intensive sampling of individuals, we addressed technical and biological sources of variation in 16S-based estimates of microbial diversity. After employing a two-tiered bead beating approach consisting of tissue homogenization followed by microbial lysis in subsamples, we found an extremely minor effect of DNA isolation protocol relative to among-host microbial diversity differences. Individual abundance estimates for rare OTUs, however, showed much lower reproducibility. We found that the stickleback gut microbiome was highly variable, even among siblings housed together, but that an effect of host genotype (stickleback lineage) was detectable for some microbial taxa. Our findings demonstrate the importance of appropriately quantifying biological and technical variance components when attempting to understand major influences on high-throughput microbiome data.

microbiology↗

bioRxiv2018

Environmental and evolutionary drivers of the modular gene regulatory network underlying phenotypic plasticity for stress resistance in the nematode Caenorhabditis remanei

In response to changing environmental conditions, organisms can acclimate through phenotypic plasticity or adapt by evolving mechanisms to cope with novel stressors. Changes in gene expression, whether dynamic or evolved, are an important way in which environmental responses are mediated; however, much is still unknown about how the molecular networks underlying plastic phenotypes evolve. Here, we compare transcriptional responses to acute heat stress among four populations of the nematode Caenorhabditis remanei--one selected to withstand heat stress, one selected under oxidative stress, an unselected control, and the ancestral population. We used a weighted gene coexpression network analysis within these lines to identify transcriptional modules, which are sets of genes that respond similarly to stress via plastic responses, evolutionary responses, or both. The transcriptional response to acute heat stress is dominated by a plastic response that is shared in the ancestor and all evolved populations. However, we also identified several modules that respond to artificial selection by (1) changing the baseline level of expression, (2) altering the magnitude of the plastic response, or (3) a combination of the two. Our findings reveal that while it is possible to perturb the nature of the transcriptional response network with short bouts of intense selection, the overall structure of transcriptional plasticity is dominated by inherent, ancestral regulatory systems.

evolutionary biology↗

bioRxiv2017

Sweeping genomic remodeling through repeated selection of alternatively adapted haplotypes occurs in the first decades after marine stickleback colonize new freshwater ponds

Heterogeneous genetic divergence can accumulate across the genome when populations adapt to different habitats while still exchanging alleles. How long does diversification take and how much of the genome is affected? When divergence occurs in parallel from standing genetic variation, how often are the same haplotypes used? We explore these questions using RAD-seq genotyping data, and show that broad-scale genomic re-patterning, fueled by standing variation, can emerge in just dozens of generations in replicate natural populations of threespine stickleback fish (Gasterosteus aculeatus). After the catastrophic 1964 Alaskan earthquake, marine stickleback colonized newly created ponds on seismically uplifted islands. We find that freshwater fish in these young ponds differ from their marine ancestors across the same genomic segments previously shown to have diverged in much older lake populations. Outside of these core divergent regions the genome shows no population structure across the ocean-freshwater divide, consistent with strong local selection acting in alternative environments on stickleback populations still connected by significant gene flow.Reinforcing this inference, a majority of divergent haplotypes that are at high frequency in ponds are shared across independent freshwater populations and are detectable, at low frequency, in the sea even across great geographic distances. Building upon previous work in this model species for population genomics, our data suggest that a long history of divergent selection and gene flow across stickleback in oceanic and freshwater habitats has created balanced polymorphism in large genomic blocks of alternatively adapted DNA sequences, ultimately stoking - and potentially channeling - rapid, parallel evolution.

evolutionary biology↗