Biology subjects

Goodheart, J. A.

Publications and source records attributed to Goodheart, J. A..

9 recordsLinked to original sources

bioRxiv2025

A subset of conserved phagocytic genes are likely used for the intracellular theft of cnidarian stinging organelles in nudibranch gastropods

BackgroundPhagocytosis is a universal physiological process in eukaryotes with many important biological functions. In nudibranch gastropods, a novel form of phagocytosis called nematocyst sequestration is specialized for the uptake of venomous stinging organelles stolen from their cnidarian prey. This process is highly selective. Here we use the emerging model nudibranch species Berghia stephanieae and Hermissenda opalescens to identify genes enriched within the body regions where nematocyst sequestration occurs, and investigate how the expression profile of phagocytosis, immune, and digestive genes differs between nematocyst sequestering regions relative to those where other phagocytic functions occur. ResultsWe identified 166 genes with significantly higher expression in sequestering regions in B. stephanieae, including genes associated with development, membrane transport, and metabolism. Of these, 41 overlap with transcripts upregulated in H. opalescens sequestering tissues. Using Hybridization Chain Reaction in situs, we show that at least two of these genes were localized to sequestering cells in B. stephanieae, including a putative C-type lectin receptor and a collagen. Genes annotated with phagocytosis, digestion, or immunity GO terms were often expressed in both sequestering and non-sequestering tissues, suggesting that they may also play a role in sequestration processes. ConclusionOur results suggest that phagocytosis genes likely play a role in the sequestration phenotype, and that a small subset of genes (e.g., collagen) may play unique functions yet to be uncovered. However, we also show that genes categorized in GO terms related to endocytosis, immunity, and digestion show a clear decrease in overall expression in sequestering tissues. This study lays the foundation for further inquiry into mechanisms of organelle sequestration in nudibranchs and other organisms.

evolutionary biology↗

bioRxiv2023

A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes

How novel phenotypes originate from conserved genes, processes, and tissues remains a major question in biology. Research that sets out to answer this question often focuses on the conserved genes and processes involved, an approach that explicitly excludes the impact of genetic elements that may be classified as clade-specific, even though many of these genes are known to be important for many novel, or clade-restricted, phenotypes. This is especially true for understudied phyla such as mollusks, where limited genomic and functional biology resources for members of this phylum has long hindered assessments of genetic homology and function. To address this gap, we constructed a chromosome-level genome for the gastropod Berghia stephanieae (Valdes, 2005) to investigate the expression of clade-specific genes across both novel and conserved tissue types in this species. The final assembled and filtered Berghia genome is comparable to other high quality mollusk genomes in terms of size (1.05 Gb) and number of predicted genes (24,960 genes), and is highly contiguous. The proportion of upregulated, clade-specific genes varied across tissues, but with no clear trend between the proportion of clade-specific genes and the novelty of the tissue. However, more complex tissue like the brain had the highest total number of upregulated, clade-specific genes, though the ratio of upregulated clade-specific genes to the total number of upregulated genes was low. Our results, when combined with previous research on the impact of novel genes on phenotypic evolution, highlight the fact that the complexity of the novel tissue or behavior, the type of novelty, and the developmental timing of evolutionary modifications will all influence how novel and conserved genes interact to generate diversity.

genomics↗

bioRxiv2023

Predictable genetic recruitment for luciferin sulfation in the convergent evolution of bioluminescence

Genes from ancient families are sometimes involved in the convergent evolutionary origins of similar traits, even across vast phylogenetic distances. Sulfotransferases are an ancient family of enzymes that transfer sulfate from a donor to a wide variety of substrates, including probable roles in some bioluminescence systems. Here we demonstrate multiple sulfotransferases, highly expressed in light organs of the bioluminescent ostracod Vargula tsujii, transfer sulfate in vivo to the luciferin substrate, vargulin. We find luciferin sulfotransferases of ostracods are not orthologous to known luciferin sulfotransferases of fireflies or sea pansies; animals with distinct and convergently evolved bioluminescence systems compared to ostracods. Therefore, distantly related sulfotransferases were independently recruited at least three times, leading to parallel evolution of luciferin metabolism in three highly diverged organisms. Re-use of homologous genes is surprising in these bioluminescence systems because the other components, including luciferins and luciferases, are completely distinct. Whether convergently evolved traits incorporate ancient genes with similar functions or instead use distinct, often newer, genes may be constrained by how many genetic solutions exist for a particular function. When fewer solutions exist, as in genetic sulfation of small molecules, evolution may be more constrained to use the same genes time and again.

evolutionary biology↗

bioRxiv2023

Spatial-temporal expression analysis of lineage-restricted shell matrix proteins reveals shell field regionalization and distinct cell populations in the slipper snail Crepidula atrasolea

Molluscs are one of the most morphologically diverse clades of metazoans, exhibiting an immense diversification of calcium carbonate structures, such as the shell. Biomineralization of the calcified shell is dependent on shell matrix proteins (SMPs). While SMP diversity is hypothesized to drive molluscan shell diversity, we are just starting to unravel SMP evolutionary history and biology. Here we leveraged two complementary model mollusc systems, Crepidula fornicata and Crepidula atrasolea, to determine the lineage-specificity of 185 Crepidula SMPs. We found that 95% of the adult C. fornicata shell proteome belongs to conserved metazoan and molluscan orthogroups, with molluscan-restricted orthogroups containing half of all SMPs in the shell proteome. The low number of C. fornicata-restricted SMPs contradicts the generally-held notion that an animals biomineralization toolkit is dominated by mostly novel genes. Next, we selected a subset of lineage-restricted SMPs for spatial-temporal analysis using in situ hybridization chain reaction (HCR) during larval stages in C. atrasolea. We found that 12 out of 18 SMPs analyzed are expressed in the shell field. Notably, these genes are present in 5 expression patterns, which define at least three distinct cell populations within the shell field. These results represent the most comprehensive analysis of gastropod SMP evolutionary age and shell field expression patterns to date. Collectively, these data lay the foundation for future work to interrogate the molecular mechanisms and cell fate decisions underlying molluscan mantle specification and diversification.

evolutionary biology↗

bioRxiv2022

Phylogenomics suggests that larvae are ancestral in polyclads, but not homologous to the trochophore

Platyhelminthes (flatworms) are a diverse invertebrate phylum that are useful for exploring life history evolution. Within Platyhelminthes, only two clades develop through a larval stage: free-living polyclads and parasitic neodermatans. Neodermatan larvae are considered evolutionarily derived, whereas polyclad larvae are hypothesized to be retained from the last common ancestor of Platyhelminthes - and Spiralia - due to ciliary band similarities among polyclad and other spiralian larvae. However, larval evolution has been challenging to investigate within polyclads due to low support for deeper phylogenetic relationships. To investigate polyclad life history evolution, we generated transcriptomic data for 21 species of polyclads to build a well-supported phylogeny for the group. We then used ancestral state reconstruction to investigate ancestral modes of development (direct vs indirect) within Polycladida, and flatworms in general. The resulting tree provides strong support for deeper nodes and we recover a new monophyletic clade of early branching cotyleans. Early branching clades of acotyleans and cotyleans possess diverse modes of development, suggesting a complex history of larval evolution in polyclads that likely includes multiple losses and/or multiple gains. Our ancestral state reconstructions in a previous platyhelminth phylogeny also suggests that similarities in larval morphology between flatworms and other phyla may have re-emerged secondarily or are convergently evolved.

evolutionary biology↗

bioRxiv2022

Precocious sperm exchange in the simultaneously hermaphroditic nudibranch, Berghia stephanieae

Sexual systems vary greatly across molluscs. This diversity includes simultaneous hermaphroditism, with both sexes functional at the same time. Most nudibranch molluscs are thought to be simultaneous hermaphrodites, but detailed studies of reproductive development and timing remain rare as most species cannot be cultured in the lab. The aeolid nudibranch, Berghia stephanieae, is one such species that can be cultured through multiple generations on the benchtop. We studied B. stephanieae reproductive timing to establish when animals first exchange sperm and how long sperm can be stored. We isolated age- and size-matched individuals at sequential timepoints to learn how early individuals exchange sperm. Individuals isolated at 13 weeks post laying (wpl) can produce fertilized eggs. This is 6 weeks before animals first lay egg masses, indicating that sperm exchange occurs well before individuals are capable of laying eggs. Our results indicate that male gonads become functional for animals between 6 mm (~9 wpl) and 9 mm (~15 wpl) in length. That is much smaller (and sooner) than the size (and age) of individuals at first laying (12-19 mm; ~19 wpl), indicating that male and female functions do not develop simultaneously. We also tracked the number of fertilized eggs in each egg mass, which remained steady for the first 10-15 egg masses, followed by a decline to near-to-no fertilization. This large, novel dataset provides insights into precise timing of the onset of functionality of the male and female reproductive systems in B. stephanieae. These data contribute to a broader understanding of reproductive development and the potential for understanding evolution of diverse sexual systems in molluscs.

zoology↗

bioRxiv2021

Transcriptome phylogenies support ancient evolutionary transitions in bioluminescence traits of cypridinid ostracods

Although the the diversity, beauty, and intricacy of sexually selected courtship displays command the attention of evolutionists, the longevity of these traits in deep time is poorly understood. Population-based theory suggests sexual selection could either lower or raise extinction risk, resulting in high or low persistence of lineages with sexually selected traits. Furthermore, empirical studies that directly estimate longevity of sexually selected traits are uncommon. Sexually selected signals - including bioluminescent courtship - originated multiple times during evolution, allowing empirical study of their longevity after careful phylogenetic and divergence time analyses. Here, we estimate the first transcriptome-based molecular phylogeny and divergence times of Cypridinidae. We report extreme longevity of bioluminescent courtship, a trait important in mate choice and probably under sexual selection. Our relaxed-clock estimates of divergence times coupled with stochastic character mapping show luminous courtship evolved only once in Cypridinidae in a Sub-Tribe we name Luxorina at least 151 Million Years Ago (Ma) from cypridinid ancestors that used bioluminescence only in anti-predator displays, defining a Tribe we name Luminini. This time-calibrated molecular phylogeny of cypridinids will serve as a foundation for integrative and comparative studies on the biochemistry, molecular evolution, courtship, diversification, and ecology of cypridinid bioluminescence. The persistence of luminous courtship for hundreds of millions of years indicates that rates of speciation within the group exceeded extinction risk, allowing for the persistence of a diverse clade of signalling species and that sexual selection did not cause rapid loss of associated traits.

evolutionary biology↗

bioRxiv2020

Transcriptomics provides a robust framework for the relationships of the major clades of cladobranch sea slugs (Mollusca, Gastropoda, Heterobranchia), but fails to resolve the position of the enigmatic genus Embletonia

BackgroundCladobranch sea slugs represent roughly half of the biodiversity of soft-bodied, marine gastropod molluscs (Nudibranchia) on the planet. Despite their global distribution from shallow waters to the deep sea, from tropical into polar seas, and their important role in marine ecosystems and for humans (as bioindicators and providers of medical drug leads), the evolutionary history of cladobranch sea slugs is not yet fully understood. Here, we amplify the current knowledge on the phylogenetic relationships by extending the cladobranch and outgroup taxon sampling using transcriptome data. ResultsWe generated new transcriptome data for 19 species of cladobranch sea slugs and two additional outgroup taxa. We complemented our taxon sampling with previously published transcriptome data, resulting in a final supermatrix covering 56 species from all but one accepted cladobranch superfamilies. Transcriptome assembly using six different assemblers, selection of those assemblies providing the largest amount of potentially phylogenetically informative sites, and quality-driven compilation of data sets resulted in three different supermatrices: one with a full coverage of genes per species (446 single-copy protein-coding genes) and two with a less stringent coverage (667 genes with 98.9% partition coverage and 1,767 genes with 86% partition coverage, respectively). We used these supermatrices to infer statistically robust maximum-likelihood trees. All analyses, irrespective of the data set, indicate maximum statistical support for all major splits and phylogenetic relationships on family level. The only discordance between the inferred trees is the position of Embletonia pulchra. Extensive testing using Four-cluster Likelihood Mapping, Approximately Unbiased tests, and Quartet Scores revealed that its position is not due to any informative phylogenetic signal, but caused by confounding signal. ConclusionsOur data matrices and the inferred trees inferred can serve as a solid foundation for future work on the taxonomy and evolutionary history of Cladobranchia. The correct placement of E. pulchra, however, proves challenging, even with large data sets. Moreover, quartet mapping shows that confounding signal present in the data is sufficient to explain the inferred position of E. pulchra, again leaving its phylogenetic position as an enigma.

evolutionary biology↗

bioRxiv2019

Laboratory culture of the California Sea Firefly Vargula tsujii (Ostracoda: Cypridinidae): Developing a model system for the evolution of marine bioluminescence

Bioluminescence, or the production of light by living organisms via chemical reaction, is widespread across Metazoa. Culture of bioluminescent organisms from diverse taxonomic groups is important for determining the biosynthetic pathways of bioluminescent substrates, which may lead to new tools for biotechnology and biomedicine. Some bioluminescent groups may be cultured, including some cnidarians, ctenophores, and brittle stars, but those use luminescent substrates (luciferins) obtained from their diets, and therefore are not informative for determination of the biosynthethic pathways of the luciferins. Other groups, including terrestrial fireflies, do synthesize their own luciferin, but culturing them is difficult, and the biosynthetic pathway for firefly luciferin remains unclear. An additional independent origin of endogenous bioluminescence is found within ostracods from the family Cypridinidae, which use their luminescence for defense and, in Caribbean species, for courtship displays. Here, we report the first complete life cycle of a luminous ostracod (Vargula tsujii Kornicker & Baker, 1977, the California Sea Firefly) in the laboratory. We also describe the late-stage embryogenesis of Vargula tsujii and discuss the size classes of instar development. We find embryogenesis in V. tsujii ranges from 25-38 days, and this species appears to have five instar stages, consistent with ontogeny in other cypridinid lineages. We estimate a complete life cycle at 3-4 months. We also present the first complete mitochondrial genome for Vargula tsujii. Bringing a luminous ostracod into laboratory culture sets the stage for many potential avenues of study, including learning the biosynthetic pathway of cypridinid luciferin and genomic manipulation of an autogenic bioluminescent system.

developmental biology↗