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Kitchen, S. A.

Publications and source records attributed to Kitchen, S. A..

6 recordsLinked to original sources

Evolutionary assembly of cooperating cell types in an animal chemical defense system

A long-standing challenge in biology is explaining how the functions of multicellular organs emerge from the underlying evolution of cell types. We deconstructed evolution of an organ novelty: a rove beetle gland that secretes a defensive cocktail. We show that gland function was pieced together via assembly of two cell types that manufacture distinct compounds. One cell type forms a chemical reservoir in the beetles abdomen and produces alkane and ester compounds. We demonstrate that this cell type is a hybrid of cuticle cells and ancient pheromone and adipocyte-like cells, and executes its function via a mosaic of enzymes sourced from each parental cell type. The second cell type synthesizes noxious benzoquinones using a chimeric pathway derived from conserved cellular energy and cuticle formation pathways. We present evidence that evolution of each cell type was shaped by coevolution between the two cell types: the benzoquinones produced by the second cell type dissolve in solvents produced by the first, yielding a potent secretion that confers adaptive value onto the gland as a whole. Our findings illustrate how cooperation between cell types can arise, generating new, organ-level behaviors.

evolutionary biology

The coral symbiont Candidatus Aquarickettsia is variably abundant in threatened Caribbean acroporids and transmitted horizontally.

The aquatic symbiont "Candidatus Aquarickettsia rohweri" infects a diversity of non-bilaterian metazoan phyla. In the threatened coral Acropora cervicornis, Aquarickettsia proliferates in response to increased nutrient exposure, resulting in suppressed growth and increased disease susceptibility and mortality. This study evaluated the extent, as well as the ecology and evolution of Aquarickettsia infecting the Caribbean corals: Ac. cervicornis and Ac. palmata and their hybrid ( Ac. prolifera). The bacterial parasite Aquarickettsia was found in all acroporids, with host and sampling location impacting infection magnitude. Phylogenomic and genome-wide single nucleotide variant analysis found Aquarickettsia clustering by region, not by coral taxon. Fixation analysis suggested within coral colonies, Aquarickettsia are genetically isolated to the extent that reinfection is unlikely. Relative to other Rickettsiales, Aquarickettsia is undergoing positive selection, with Florida populations experiencing greater positive selection relative to the other Caribbean locations. This may be due to Aquarickettsia response to increased nutrient stress in Florida, as indicated by greater in situ replication rates in these corals. Aquarickettsia did not significantly codiversify with either coral animal nor algal symbiont, and qPCR analysis of gametes and juveniles from susceptible coral genotypes indicated absence in early life stages. Thus, despite being an obligate parasite, Aquarickettsia must be horizontally transmitted via coral mucocytes, an unidentified secondary host, or a yet unexplored environmentally mediated mechanism. Importantly, the prevalence of Aquarickettsia in Ac. cervicornis and high abundance in Florida populations suggests that disease mitigation efforts in the US and Caribbean should focus on preventing early infection via horizontal transmission.

microbiology

Molecular evolutionary trends and biosynthesis pathways in the Oribatida revealed by the genome of Archegozetes longisetosus

Oribatid mites are a specious order of microarthropods within the subphylum Chelicerata, compromising about 11,000 described species. They are ubiquitously distributed across different microhabitats in all terrestrial ecosystems around the world and were among the first animals colonizing terrestrial habitats as decomposers and scavengers. Despite their species richness and ecological importance genomic resources are lacking for oribatids. Here, we present a 190-Mb genome assembly of the clonal, all-female oribatid mite species Archegozetes longisetosus Aoki, a model species used by numerous laboratories for the past 30 years. Comparative genomic and transcriptional analyses revealed patterns of reduced body segmentation and loss of segmental identity gene abd-A within Acariformes, and unexpected expression of key eye development genes in these eyeless mites across developmental stages. Consistent with their soil dwelling lifestyle, investigation of the sensory genes revealed a species-specific expansion of gustatory receptors, the largest chemoreceptor family in the genome used in olfaction, and evidence of horizontally transferred enzymes used in cell wall degradation of plant and fungal matter, both components of the A. longisetosus diet. Oribatid mites are also noted for their biosynthesis capacities and biochemical diversity. Using biochemical and genomic data, we were able to delineate the backbone biosynthesis of monoterpenes, an important class of compounds found in the major exocrine gland system of Oribatida - the oil glands. Given the mites strength as an experimental model, the new high-quality resources provided here will serve as the foundation for molecular research in Oribatida and will enable a broader understanding of chelicerate evolution.

zoology

Juvenile corals inherit mutations acquired during the parents lifespan

128 years ago, August Weismann proposed that the only source of inherited genetic variation in animals is the germline1. Julian Huxley reasoned that if this were true, it would falsify Jean-Baptiste Lamarcks theory that acquired characteristics are heritable2. Since then, scientists have discovered that not all animals segregate germline cells from somatic cells permanently and early in development3. In fact, throughout their lives, Cnidaria4-6 and Porifera7 maintain primordial stem cells that continuously give rise to both germline and somatic cells. The fate of mutations generated in this primordial stem cell line during adulthood remains an open question. It was unknown whether post-embryonic mutations could be heritable in animals8-10--until now. Here we use two independent genetic marker analyses to show that post-embryonic mutations are inherited in the coral Acropora palmata (Cnidaria, Anthozoa). This discovery upends the long-held supposition that post-embryonic genetic mutations acquired over an animals lifetime in non-germline tissues are not heritable2. Over the centuries-long lifespan of a coral, the inheritance of post-embryonic mutations may not only change allele frequencies in the local larval pool but may also spread novel alleles across great distances via larval dispersal. Thus, corals may have the potential to adapt to changing environments via heritable somatic mutations10. This mechanism challenges our understanding of animal adaptation and prompts a deeper examination of both the process of germline determination in Cnidaria and the role of post-embryonic genetic mutations in adaptation and epigenetics of modular animals. Understanding the role of post-embryonic mutations in animal adaptation will be crucial as ecological change accelerates in the Anthropocene.

evolutionary biology

Genotypic similarity among algal symbionts corresponds to associations with closely related coral hosts

Mutualisms where hosts are coupled metabolically to their symbionts often exhibit high partner fidelity. Most reef-building corals form obligate symbioses with specific species of photosymbionts, dinoflagellates in the family Symbiodiniaceae, despite needing to acquire symbionts early in their development from environmental sources. Three Caribbean acroporids (Acropora palmata, A. cervicornis, and their hybrid A. prolifera) are geographically sympatric across much of their range in the greater Caribbean, but often occupy different depth and light habitats. Both species and their hybrid associate with Symbiodinium fitti, a genetically diverse species of symbiont that is specific to these hosts. Since the physiology of the dinoflagellate partner is strongly influenced by light (and therefore depth), we investigated whether S. fitti populations from each host source were differentiated genetically. We generated shallow genome sequences of acroporid colonies sampled from across the Caribbean. Single Nucleotide Polymorphisms (SNPs) among S. fitti strains were identified by aligning sequences to a ~600 Mb draft assembly of the S. fitti genome, assembled from an A. cervicornis metagenome. Phylogenomic and multivariate analyses revealed that allelic variation among S. fitti partitioned to each host species, as well as their hybrid, rather than by biogeographic origin. This is particularly noteworthy because the hybrid, A. prolifera, has a sparse fossil record and may be of relatively recent origin. Many of the SNPs putatively under selection were non-synonymous mutations predicted to alter protein efficiency. Differences in allele frequency among S. fitti populations from each host taxon may correspond to distinct phenotypes that thrive in the different cellular environments found in each acroporid. The non-random sorting among genetically diverse strains, or genotypes, to different hosts could be the basis for lineage diversification via disruptive selection, leading to ecological specialization and ultimately speciation.

genomics

STAGdb: a 30K SNP genotyping array and Science Gateway for Acropora corals and their dinoflagellate symbionts

Standardized identification of genotypes is necessary in animals that reproduce asexually and form large clonal populations such as coral. We developed a high-resolution hybridization-based genotype array coupled with an analysis workflow and database for the most speciose genus of coral, Acropora, and their symbionts. We designed the array to co-analyze host and symbionts based on bi-allelic single nucleotide polymorphisms (SNP) markers identified from genomic data of the two Caribbean Acropora species as well as their dominant dinoflagellate symbiont, Symbiodinium fitti. SNPs were selected to resolve multi-locus genotypes of host (called genets) and symbionts (called strains), distinguish host populations and determine ancestry of the coral hybrids in Caribbean acroporids. Pacific acroporids can also be genotyped using a subset of the SNP loci and additional markers enable the detection of symbionts belonging to the genera Breviolum, Cladocopium, and Durusdinium. Analytic tools to produce multi-locus genotypes of hosts based on these SNP markers were combined in a workflow called the Standard Tools for Acroporid Genotyping (STAG). In the workflow the users data is compared to the database of previously genotyped samples and generates a report of genet identification. The STAG workflow and database are contained within a customized Galaxy environment (https://coralsnp.science.psu.edu/galaxy/), which allows for consistent identification of host genet and symbiont strains and serves as a template for the development of arrays for additional coral genera. STAG data can be used to track temporal and spatial changes of sampled genets necessary for restoration planning as well as be applied to downstream genomic analyses.

genetics