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Evolutionary innovations in chemical secretion-such as the production of secondary metabolites, pheromones, and toxins-profoundly impact ecological interactions across a broad diversity of life. These secretory innovations may involve a "legacy-plus-innovation" mode of evolution, whereby new biochemical pathways are integrated with conserved secretory processes to create novel products. Among secretory innovations, bioluminescence is important because it evolved convergently many times to influence predator-prey interactions, while often producing courtship signals linked to increased rates of speciation. However, whether or not deeply conserved secretory genes are used in secretory bioluminescence remains unexplored. Here, we show that in the ostracod Vargula tsujii, the evolutionary novel c-luciferase gene is co-expressed with many conserved genes, including those related to toxin production and high-output protein secretion. Our results demonstrate that the legacy-plus-innovation mode of secretory evolution, previously applied to sensory modalities of olfaction, gustation, and nociception, also encompasses light-producing signals generated by bioluminescent secretions. This extension broadens the paradigm of secretory diversification to include not only chemical signals but also bioluminescent light as an important medium of ecological interaction and evolutionary innovation., Competing Interests: Conflict of Interest The authors declare no competing interests., (© The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.)

Sampling groundwater biodiversity is difficult because of limited access and issues with species identification. Environmental DNA (eDNA) provides a viable alternative to traditional sampling approaches, however limited knowledge of the abundance and fate of DNA in groundwater hinders the interpretation of data from these environments. Groundwater environments are dark and have lower oxygen concentrations and microbial activity than surface waters. Consequently, assumptions about DNA fate in surface ecosystems may not apply to groundwaters. Here, we test the longevity and transport of eDNA in groundwater within a static microcosm and a flow-through mesocosm. A variety of invertebrates were placed within a mesocosm and microcosm to enable DNA shedding, and then removed. DNA persisted for up to 5 weeks after their removal in the static experiment and was detected between 9 and 33 days in the flow-through experiment. Sediments and water both proved important for eDNA detection. Crustacean DNA was detected sporadically and unpredictably, whereas non-crustacean DNA was detected more frequently despite their lower densities. We suggest that detecting crustaceans poses a challenge to utilising eDNA approaches for stygofauna monitoring. This is confounded by the scarcity of sequences for stygofauna in reference databases. Further research is needed before eDNA alone can be routinely employed for stygofauna detection., (© 2024. The Author(s).)

Balancing selection is an evolutionary process that maintains genetic polymorphisms at selected loci and strongly reduces the likelihood of allele fixation. When allelic polymorphisms that predate speciation events are maintained independently in the resulting lineages, a pattern of trans-species polymorphisms may occur. Trans-species polymorphisms have been identified for loci related to mating systems and the MHC, but they are generally rare. Trans-species polymorphisms in disease loci are believed to be a consequence of long-term host-parasite coevolution by balancing selection, the so-called Red Queen dynamics. Here we scan the genomes of three crustaceans with a divergence of over 15 million years and identify 11 genes containing identical-by-descent trans-species polymorphisms with the same polymorphisms in all three species. Four of these genes display molecular footprints of balancing selection and have a function related to immunity. Three of them are located in or close to loci involved in resistance to a virulent bacterial pathogen, Pasteuria, with which the Daphnia host is known to coevolve. This provides rare evidence of trans-species polymorphisms for loci known to be functionally relevant in interactions with a widespread and highly specific parasite. These findings support the theory that specific antagonistic coevolution is able to maintain genetic diversity over millions of years., (© 2024. The Author(s).)

Virus infection causes the metabolic disorder of host cells, whereas the metabolic disorder of cells is one of the major causes of tumorigenesis, suggesting that antiviral molecules might possess anti-tumor activities by regulating cell metabolism. As the key regulators of gene expression, long non-coding RNAs (lncRNAs) play vital roles in the regulation of cell metabolism. However, the influence of antiviral lncRNAs on tumorigenesis has not been explored. To address this issue, the antiviral and anti-tumor capacities of shrimp lncRNAs were characterized in this study. The results revealed that shrimp lncRNA06, having antiviral activity in shrimp, could suppress the tumorigenesis of human gastric cancer stem cells (GCSCs) via triggering apoptosis of GCSCs in a cross-species manner. Shrimp lncRNA06 could sponge human miR-17-5p to suppress the stemness of GCSCs via the miR-17-5p-p21 axis. At the same time, shrimp lncRNA06 could bind to ATP synthase subunit beta (ATP5F1B) to enhance the stability of the ATP5F1B protein in GCSCs, thus suppressing the tumorigenesis of GCSCs. The in vivo data demonstrated that shrimp lncRNA06 promoted apoptosis and inhibited the stemness of GCSCs through interactions with ATP5F1B and miR-17-5p, leading to the suppression of the tumorigenesis of GCSCs. Therefore, our findings highlighted that antiviral lncRNAs possessed anti-tumor capacities and that antiviral lncRNAs could be the anti-tumor reservoir for the treatment of human cancers.

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 vitro to the luciferin substrate, vargulin. We find luciferin sulfotransferases (LSTs) of ostracods are not orthologous to known LSTs 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. Reuse 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.

Despite discovery more than 100years ago and documented global occurrence from shallow waters to the deep sea, the life cycle of the enigmatic crustacean y-larvae isincompletely understood and adult forms remain unknown. To date, only 2 of the 17 formally described species, all based on larval stages, have been investigated using an integrative taxonomic approach. This approach provided descriptions of the morphology of the naupliar and cyprid stages, and made use of exuvial voucher material and DNA barcodes. To improve our knowledge about the evolutionary history and ecological importance of y-larvae, we developed a novel protocol that maximises the amount of morpho-ecological and molecular data that can be harvested from single larval specimens. This includes single-specimen DNA barcoding and daily imaging of y-nauplii reared in culture dishes, mounting of the last naupliar exuviae on a slide as a reference voucher, live imaging of the y-cyprid instar that follows, and fixation, DNA extraction, amplification and sequencing of the y-cyprid specimen. Through development and testing of a suite of new primers for both nuclear and mitochondrial protein-coding and ribosomal genes, we showcase how new sequence data can be used to estimate the phylogeny of Facetotecta. We expect that our novel procedure will help to unravel the complex systematics of y-larvae and show how these fascinating larval forms have evolved. Moreover, we posit that our protocols should work on larval specimens from a diverse array of moulting marine invertebrate taxa.

Long noncoding RNA (lncRNA) is a potential regulator of biological processes, including immunity, reproduction, and development. Although several transcriptome studies have focused on responses of viral infections in several organisms, the role of lncRNAs in viral responses in shrimp is still unclear. Therefore, this work aimed to identify putative lncRNAs and study their role in white spot syndrome virus (WSSV) infection in white shrimp. The hepatopancreas transcriptome from WSSV infected shrimp was analyzed in silico to identify putative lncRNAs. Among 221,347 unigenes of the de novo assembled transcriptome, 44,539 putative lncRNAs were identified, 32 of which were differentially expressed between WSSV-infected and control shrimp. Five candidate lncRNAs were validated for their expressions in shrimp tissues and in response to WSSV infection. Lnc164 was chosen for further investigation of its role in WSSV infection. Knockdown of lnc164 prolonged survival of shrimp when challenged with WSSV, suggesting a role in shrimp immunity. In addition, lnc164 was not directly involved in the control of total hemocytes and viral loads in hemolymph of WSSV-infected shrimp. A set of lnc164-regulated genes was obtained by RNA sequencing among which 251 transcripts were differentially expressed between lnc164 knockdown and control shrimp. Six immune-related genes were validated for their expression profiles. Our work sheds light on lncRNA profiles in L. vannamei in response to WSSV infection and paves the way to a functional study of lnc164 in host antiviral response., Competing Interests: Declaration of competing interest None., (Copyright © 2023 Elsevier Ltd. All rights reserved.)

The special rhabdom structure of the mid-band ommatidium in compound eye contributes to the mantis shrimp being the only animal species known to science that can recognize circularly polarized light (CPL). Although the number of mid-band ommatidium of Oratosquilla oratoria is reduced, the mid-band ommatidium still has orthogonal geometric interleaved rhabdom and short oval distal rhabdom, which may mean that the O. oratoria has weakened circular polarized light vision (CPLV). Here we explored the molecular mechanisms of how O. oratoria response to the polarization of light. Based on the specific expression patterns of vision-related functional genes and proteins, we suggest that the order of light response by O. oratoria compound eye was first natural light, then left-circularly polarized light (LCPL), linearly polarized light, right-circularly polarized light (RCPL) and dark. Meanwhile, we found that the expression levels of vision-related functional genes and proteins in O. oratoria compound eye under RCPL were not significantly different from those in DL, which may imply that O. oratoria cannot respond to RCPL. Furthermore, the response of LCPL is likely facilitated by the differential expression of opsin and microvilli - related functional genes and proteins (arrestin and sodium-coupled neutral amino acid transporter). In conclusion, this study systematically illustrated for the first time how O. oratoria compound eye response to the polarization of light at the genetic level, and it can improve the visual ecological theory behind polarized light vision evolution., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2023. Published by Elsevier B.V.)

In the species-rich Phylum Arthropoda, the mitochondrial genome is relatively well conserved both in terms of number and order of genes. However, specific clades have a 'typical' gene order that differs from the putative arthropod ancestral arrangement. The aim of this work was to compare the rate of mitochondrial gene rearrangements at inter- and intra-taxonomic levels in the Arthropoda and to postulate the most parsimonious ancestral orders representing the four major arthropod lineages. For this purpose, we performed a comparative genomic analysis of arthropod mitochondrial genomes available in the NCBI database. Using a combination of bioinformatics methods that examined mitochondrial gene rearrangements in 464 species of arthropods from three subphyla (Chelicerata, Myriapoda, and Crustacea [except Hexapoda, previously analyzed]), we observed differences in the rate of rearrangement within major lineages. A higher rate of mitochondrial genome rearrangement was observed in Crustacea and Chelicerata compared to Myriapoda. Likewise, early branching clades exhibit less variability in mitochondrial genome order than late branching clades, within each subphylum. We identified 'hot regions' in the mitochondrial genome of each studied subphylum, and postulated the most likely ancestral gene order in each subphylum and taxonomic order. Our work provides new evidence on the evolutionary dynamics of mitochondrial genome gene order in arthropods and new mitochondrial genome architectures in different taxonomic divisions within each major lineage of arthropods., Competing Interests: Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2023 The Authors. Published by Elsevier B.V. All rights reserved.)