Biology subjects

Woodruff, G. C.

Publications and source records attributed to Woodruff, G. C..

11 recordsLinked to original sources

bioRxiv2026

Recombination and repetitive genomic landscapes are decoupled in a close relative of Caenorhabditis elegans

Genomes exhibit chromosomal heterogeneity. Distributions of genes, repetitive elements, and polymorphisms are not uniform along chromosomes in multiple species. One explanation for these patterns is recombination rate variation. As recombination interacts with selection to shape the evolutionary fates of alleles, recombination rate variation could promote differences in the chromosomal distribution of genomic features. Thus, clarifying the relationship between recombination rates and genomic organization is a major goal of genetics. In the nematode Caenorhabditis elegans, recombination rate correlates with multiple genomic features that are non-uniformly distributed along chromosomes; recombination rates and repeats are higher on chromosome ends compared to chromosome centers. Its closest known relative, C. inopinata, harbors a radically altered genome with nearly uniform chromosomal distributions of repetitive elements. Is this dramatic change in genomic organization connected to the evolution of recombination rates? Here, we describe a genetic map of C. inopinata constructed via whole-genome sequencing of 180 individual F2 recombinants. This reveals four chromosomes have a conserved recombination rate domain structure whereas two other chromosomes harbor divergent, more uniform recombination rate distributions. Comparisons of these intrachromosomal recombination rates with genomic features reveal little covariation between recombination rate, diversity, gene density, and repeat content in C. inopinata (in stark contrast to most Caenorhabditis species). This suggests that the evolution of recombination may not be entirely responsible for the atypical uniform distribution of repetitive elements across C. inopinata chromosomes. Taken together, these observations reveal that recombination rates can be decoupled from the genomic organization of repetitive elements.

genomics↗

bioRxiv2025

A novel, fig-associated microbe promotes reproductive success via variable life history mechanisms in C. elegans and C. inopinata

Variation in life history strategies is among the most striking features of animal diversity. Simultaneously, the microbes an animal interacts with are a critical and dynamic aspect of the host environment that can have profound impacts on their life history traits. As microbial environments diverge across animal lineages, life histories and their responses to such microbial contexts are expected to evolve as a consequence. Caenorhabditis nematodes are bacterivores that exhibit a diversity of life history strategies and fill diverse ecological niches. C. elegans thrives on rotting plants and grows rapidly with high fecundity; C. inopinata thrives in fresh figs and grows more slowly with lower fecundity. To understand how hosts with divergent life histories and ecologies respond to the microbes they interact with, we isolated over forty bacterial species from the natural fig environment of C. inopinata. This microbial survey revealed an isolate, Klebsiella sp. WOUb2, that doubles the population growth rate of C. inopinata. While this isolate also increases the population growth rate of C. elegans, Klebsiella sp. WOUb2 increases individual fecundity and developmental rate in C. elegans, whereas it only increases developmental rate of C. inopinata. Thus, fitness is modulated by variable life history mechanisms in the two species. Comparisons with nucleotide databases reveal Klebsiella sp. WOUb2 is closely related to other Klebsiella isolates known to influence Caenorhabditis nematode fitness. Additionally, the similarity of Klebsiella sp. WOUb2 to microbes associated with fig wasps and figs suggests C. inopinata frequently encounters this microbe in its natural context. Taken together, this shows that different physiological responses can underlie conserved, beneficial interspecific interactions.

evolutionary biology↗

bioRxiv2024

The Bacteria of a Fig Microcommunity

Understanding the biotic drivers of diversity is a major goal of microbial ecology. One approach towards tackling this issue is to interrogate relatively simple communities that are easy to observe and perturb. Figs (syconia) of the genus Ficus represent such a system. Here, we describe the microbial communities of Ficus septica figs, which are associated with the nematode Caenorhabditis inopinata (the sister species of the C. elegans genetic model system). In 2019, 38 Ficus septica figs (across 12 plants in Taiwan) were dissected, and metadata such as foundress wasp number and nematode occupancy were collected for each fig. Suspensions derived from interior fig material and fig surface washes were prepared for 16S microbial metabarcoding. Over 3,000 OTUs were detected, and microbial communities were dominated by members of Proteobacteria, Bacteroidota, and Actinobacteriota. Although microbial communities of fig exteriors and interiors can be distinguished, levels of microbial alpha diversity were comparable across these areas of the fig. Nematodes likewise had no detectable impact on microbial alpha diversity, although nematodes were associated with a modest change in microbial community composition. A handful of OTUs (associated with the genera Kosokonia, Ochobactrum, and Stenotrophomonas) revealed potential differential abundance among figs varying in nematode occupancy. Additionally, foundress wasp number was negatively correlated with microbial alpha diversity. These findings set the stage for future studies that directly test the role of nematode and wasp occupancy on microbial communities, as well as investigations that probe nematode-microbe interactions through laboratory experiments. Taken together, these results constitute a fundamental step in characterizing the natural microbial communities of figs and Caenorhabditis nematodes. ImportanceUnraveling why different species live in different places is a longstanding open question in ecology, and it is clear that interspecific interactions among species are a major contributor to species distributions. Ficus figs are a useful system for ecological studies because they are relatively simple microcosms where characterizing animal community composition of multiple samples is straightforward. Additionally, Caenorhabditis inopinata, a close relative of the C. elegans genetic model system, thrives in Ficus septica figs. Here, we tie 16S microbial metabarcoding to nematode and wasp occupancy data to understand the causes of bacterial community composition in F. septica figs. We found that microbial composition, but not total diversity, varies among fig surface and interiors. Likewise, we found that nematode occupancy impacts microbial composition but not alpha diversity. Moreover, we show that as the number of foundress wasps increases, the microbial alpha diversity decreases. Finally, we identified OTUs that are potentially associated with nematode occupancy. Taken together, these results represent a key step in describing a microcommunity wherein ecological genetic hypotheses can be tested, as well as one that can potentially reveal the roles of uncharacterized genes in established model systems.

ecology↗

bioRxiv2024

Computer prediction and genetic analysis identifies retinoic acid modulation as a driver of conserved longevity pathways in genetically-diverse Caenorhabditis nematodes

Aging is a pan-metazoan process with significant consequences for human health and society--discovery of new compounds that ameliorate the negative health impacts of aging promise to be of tremendous benefit across a number of age-based comorbidities. One method to prioritize a testable subset of the nearly infinite universe of potential compounds is to use computational prediction of their likely anti-aging capacity. Here we present a survey of longevity effects for 16 compounds suggested by a previously published computational prediction set, capitalizing upon the comprehensive, multi-species approach utilized by the Caenorhabditis Intervention Testing Program (CITP). While eleven compounds (aldosterone, arecoline, bortezomib, dasatinib, decitabine, dexamethasone, erlotinib, everolimus, gefitinib, temsirolimus, and thalidomide) either had no effect on median lifespan or were toxic, five compounds (all-trans retinoic acid, berberine, fisetin, propranolol, and ritonavir) extended lifespan in Caenorhabditis elegans. These computer predictions yield a remarkable positive hit rate of 30%. Deeper genetic characterization of the longevity effects of one of the most efficacious compounds, the endogenous signaling ligand all-trans retinoic acid (atRA, designated tretinoin in medical products), which is widely prescribed for treatment of acne, skin photoaging and acute promyelocytic leukemia, demonstrated a requirement for the regulatory kinases AKT-1 and AKT-2. While the canonical Akt-target FOXO/DAF-16 was largely dispensable, other conserved Akt-targets (Nrf2/SKN-1 and HSF1/HSF-1), as well as the conserved catalytic subunit of AMPK AAK-2, were all necessary for longevity extension by atRA. Evolutionary conservation of retinoic acid as a signaling ligand and the structure of the downstream effector network of retinoic acid combine to suggest that the all-trans retinoic acid pathway is an ancient metabolic regulatory system that can modulate lifespan. Our results highlight the potential of combining computational prediction of longevity interventions with the power of nematode functional genetics and underscore that the manipulation of a conserved metabolic regulatory circuit by co-opting endogenous signaling molecules is a powerful approach for discovering aging interventions.

genetics↗

bioRxiv2021

Alignment of genetic differentiation across trophic levels in a fig community

Ecological interactions can generate close associations among species, which can in turn generate a high degree of overlap in their spatial distributions. Co-occurrence is likely to be particularly intense when species exhibit obligate comigration, in which they not only overlap in spatial distributions but also travel together from patch to patch. In theory, this pattern of ecological co-occurrence should leave a distinct signature in the pattern of genetic differentiation within and among species. Perhaps the most famous mutual co-isolation partners are fig trees and their co-evolved wasp pollinators. Here, we add another tropic level to this system by examining patterns of genomic diversity in the nematode Caenorhabditis inopinata, a close relative of the C. elegans model system that thrives in figs and obligately disperses on fig wasps. We performed RADseq on individual worms isolated from the field across three Okinawan island populations. The male/female C. inopinata is about five times more diverse than the hermaphroditic C. elegans, and polymorphism is enriched on chromosome arms relative to chromosome centers. FST is low among island population pairs, and clear population structure could not be easily detected among figs, trees, and islands, suggesting frequent migration of wasps between islands. Moreover, inbreeding coefficients are elevated in C. inopinata, consistent with field observations suggesting small C. inopinata founding populations in individual figs. These genetic patterns in C. inopinata overlap with those previously reported in its specific fig wasp vector and are consistent with C. inopinata population dynamics being driven by wasp dispersal. Thus, interspecific interactions can align patterns of genetic diversity across species separated by hundreds of millions of years of evolutionary divergence. HighlightsO_LIThe fig-dwelling female/male nematode Caenorhabditis inopinata is five times more diverse than its closest relative, the self-fertilizing nematode C. elegans. C_LIO_LIC. inopinata migrates frequently among three Okinawan islands despite high levels of inbreeding within individual figs. C_LIO_LIC. inopinata has patterns of genetic diversity that mirror its fig wasp vector. C_LIO_LIEcological specialization aligns patterns of genetic differentiation in closely interacting species. C_LI

evolutionary biology↗

bioRxiv2020

Opposing directions of stage-specific body length change in a close relative of C. elegans

BackgroundBody size is a fundamental organismal trait. However, as body size and ecological contexts change across developmental time, evolutionary divergence may cause unexpected patterns of body size diversity among developmental stages. This may be particularly evident in polyphenic developmental stages specialized for dispersal. The dauer larva is such a stage in nematodes, and Caenorhabditis species disperse by traveling on invertebrate carriers. Here, we describe the morphology of the dispersal dauer larva of the nematode Caenorhabditis inopinata, whose adults can grow to be nearly twice as long as its close relative, the model organism C. elegans. ResultsWe find that the C. inopinata dauer larva is shorter and fatter than those of its close relatives C. elegans, C. briggsae, and C. tropicalis, despite its much longer adult stage. Additionally, many C. inopinata dauer larvae were ensheathed, an apparent novelty in this lineage reminiscent of the infective juveniles of parasitic nematodes. We also found abundant variation in dauer formation frequency among twenty-four wild isolates of C. inopinata, with many strains unable to produce dauer larvae under laboratory conditions. ConclusionMost Caenorhabditis species thrive on rotting plants and disperse on snails, slugs, or isopods (among others) whereas C. inopinata is ecologically divergent and thrives in fresh Ficus septica figs and disperses on their pollinating wasps. These wasps are at least an order of magnitude smaller in length than the vectors of other Caenorhabditis species. While there is some unknown factor of the fig environment that promotes elongated body size in C. inopinata adults, the smaller size of its fig wasp carrier may be driving the reduced body length of its dauer larva. Thus ecological divergence across multiple developmental stages can promote unexpected and opposing changes in body size within a single species.

evolutionary biology↗

bioRxiv2019

Degradation of the repetitive genomic landscape in a close relative of C. elegans

The abundance, diversity, and genomic distribution of repetitive elements is highly variable among species. These patterns are thought to be driven in part by reproductive mode and the interaction of selection and recombination, and recombination rates typically vary by chromosomal position. In the nematode C. elegans, repetitive elements are enriched at chromosome arms and depleted on centers, and this mirrors the chromosomal distributions of other genomic features such as recombination rate. How conserved is this genomic landscape of repeats, and what evolutionary forces maintain it? To address this, we compared the genomic organization of repetitive elements across five Caenorhabditis species with chromosome-level assemblies. As previously reported, repeat content is enriched on chromosome arms in most Caenorhabditis species, and no obvious patterns of repeat content associated with reproductive mode were observed. However, the fig-associated Caenorhabditis inopinata has experienced rampant repetitive element expansion and reveals no association of global repeat content with chromosome position. Patterns of transposable element superfamily-specific distributions reveal this global pattern is driven largely by a few transposable element superfamilies that in C. inopinata have expanded in number and have weak associations with chromosome position. Additionally, 15% of predicted protein-coding genes in C. inopinata align to transposon-related proteins. When these are excluded, C. inopinata has no enrichment of genes in chromosome centers, in contrast to its close relatives who all have such clusters. Forward evolutionary simulations reveal that chromosomal heterogeneity in recombination rate is insufficient for generating structured genomic repetitive landscapes. Instead, heterogeneity in the fitness effects of transposable element insertion is needed to promote heterogeneity in repetitive landscapes. Thus, patterns of gene density along chromosomes are likely drivers of global repetitive landscapes in this group, although other historical or genomic factors are needed to explain the idiosyncrasy of genomic organization of various transposable element taxa within C. inopinata. Taken together, these results highlight the power of comparative genomics and evolutionary simulations in testing hypotheses regarding the causes of genome organization.

evolutionary biology↗

bioRxiv2019

Patterns of putative gene loss suggest rampant developmental system drift in nematodes

Gene loss often contributes to the evolution of adaptive traits. Conversely, null mutations frequently reveal no obvious phenotypic consequences. How pervasive is gene loss, what kinds of genes are dispensable, and what are the consequences of gene loss? The nematode Caenorhabditis elegans has long been at the forefront of genetic research, yet only recently have genomic resources become available to situate this species in its comparative phylogenetic and evolutionary context. Here, patterns of gene loss within Caenorhabditis are evaluated using 28 nematode genomes (most of them sequenced only in the past few years). Orthologous genes detected in every species except one were defined as being lost within that species. Putative functional roles of lost genes were determined using phenotypic information from C. elegans WormBase ontology terms as well as using existing C. elegans transcriptomic datasets. All species have lost multiple genes in a species-specific manner, with a genus-wide average of several dozen genes per species. Counterintuitively, nearly all species have lost genes that perform essential functions in C. elegans (an average of one third of the genes lost within a species). Retained genes reveal no differences from lost genes in C. elegans transcriptional abundance across all developmental stages when considering all 28 Caenorhabitis genomes. However, when considering only genomes in the subgeneric Elegans group, lost genes tend to have lower expression than retained genes. Taken together, these results suggest that the genetics of developmental processes are evolving rapidly despite a highly conserved adult morphology and cell lineage in this group, a phenomenon known as developmental system drift. These patterns highlight the importance of the comparative approach in interpreting findings in model systems genetics.

evolutionary biology↗

bioRxiv2018

A large close relative of C. elegans is slow-developing but not long-lived

BackgroundVariation in body size is thought to be a major driver of a wide variety of ecological and evolutionary patterns, including changes in development, reproduction, and longevity. Caenorhabditis inopinata is a recently-discovered fig-associated nematode that is unusually large relative to other members of the genus, including the closely related model system C. elegans. Here we test whether the dramatic increase in body size has led to correlated changes in key life history and developmental parameters within this species.\n\nResultsUsing four developmental milestones, C. inopinata was found to have a slower rate of development than C. elegans across a range of temperatures. Despite this, C. inopinata did not reveal any differences in adult lifespan from C. elegans after accounting for differences in developmental timing and reproductive mode. C. inopinata fecundity was generally lower than that of C. elegans, but fitness improved under continuous-mating, consistent with sperm-limitation under gonochoristic (male/female) reproduction. C. inopinata also revealed greater fecundity and viability at higher temperatures.\n\nConclusionConsistent with observations in other ectotherms, slower growth in C. inopinata indicates a potential trade-off between body size and developmental timing, whereas its unchanged lifespan suggests that longevity is largely uncoupled from its increase in body size. Additionally, temperature-dependent patterns of fitness in C. inopinata are consistent with its geographic origins in subtropical Okinawa. Overall, these results underscore the extent to which changes in ecological context and body size can shape life history traits.

evolutionary biology↗

bioRxiv2018

Two levels of host-specificity in a fig-associated Caenorhabditis

BackgroundBiotic interactions are ubiquitous and require information from ecology, evolutionary biology, and functional genetics in order to be completely understood. However, study systems that are amenable to investigations across such disparate fields are rare. Figs and fig wasps are a classic system for ecology and evolutionary biology with poor functional genetics; C. elegans is a classic system for functional genetics with poor ecology. In order to help bridge these disciplines, here we describe the natural history of a close relative of C. elegans, C. sp. 34, that is associated with the fig Ficus septica and its pollinating Ceratosolen wasps.\n\nResultsTo understand the natural context of fig-associated Caenorhabditis, fresh F. septica figs from four Okinawan islands were sampled, dissected, and observed under microscopy. C. sp. 34 was found in all islands where F. septica figs were found. C. sp. 34 was routinely found in the fig interior and almost never observed on the outside surface. Caenorhabditis was only found in pollinated figs, and C. sp. 34 was more likely to be observed in figs with more foundress pollinating wasps. Actively reproducing C. sp. 34 dominated younger figs, whereas older figs with emerging wasp progeny harbored C. sp. 34 dispersal larvae. Additionally, C. sp. 34 was observed dismounting from plated Ceratosolen pollinating wasps. C. sp. 34 was never found on non-pollinating, parasitic Philotrypesis wasps. Finally, C. sp. 34 was only observed in F. septica figs among five Okinawan Ficus species sampled.\n\nConclusionThese observations suggest a natural history where C. sp. 34 proliferates in young F. septica figs and disperses from old figs on Ceratosolen pollinating fig wasps. The fig and wasp host specificity of this Caenorhabditis is highly divergent from its close relatives and frames hypotheses for future investigations. This natural co-occurrence of the fig/fig wasp and Caenorhabditis study systems sets the stage for an integrated research program that can help to explain the evolution of interspecific interactions.

ecology↗

bioRxiv2017

Dramatic evolution of body length due to post-embryonic changes in cell size in a newly discovered close relative of C. elegans

Understanding morphological diversity--and morphological constrainto--has been a central question in evolutionary biology since its inception. Nematodes of the genus Caenorhabditis, which contains the well-studied model system C. elegans, display remarkable morphological consistency in the face of extensive genetic divergence. Here, we provide a description of the broad developmental patterns of a recently discovered species, C. sp. 34, which was isolated from fresh figs in Okinawa and which is among the closest known relatives of C. elegans. C. sp. 34 displays an extremely large body size and can grow to be nearly twice as long as C. elegans and all other known members of the genus. Observations of the timing of developmental milestones reveal that C. sp. 34 develops about twice as slowly as C. elegans. Measurements of embryo and larval size show that the size difference between C. sp. 34 and C. elegans is largely due to post-embryonic events, particularly during the transition from larval to adult stages. This difference in size is not attributable to differences in germ line chromosome number or the number of somatic cells. The overall difference in body size is therefore largely attributable to changes in cell size via increased cytoplasmic volume. Because of its close relationship to C. elegans, the distinctness of C. sp. 34 provides an ideal system for the detailed analysis of evolutionary diversification. The context of over forty years of C. elegans developmental genetics also reveals clues into how natural selection and developmental constraint act jointly to promote patterns of morphological stasis and divergence in this group.

evolutionary biology↗