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Firefly genomes illuminate parallel origins of bioluminescence in beetles

Timothy R Fallon, Sarah E Lower, Ching-Ho Chang and 19 more

eLife · 2018 · CC BY

doi:10.1101/237586

Abstract

Fireflies and their luminous courtships have inspired centuries of scientific study. Today firefly luciferase is widely used in biotechnology, but the evolutionary origin of bioluminescence within beetles remains unclear. To shed light on this long-standing question, we sequenced the genomes of two firefly species that diverged over 100 million-years-ago: the North American Photinus pyralis and Japanese Aquatica lateralis. To compare bioluminescent origins, we also sequenced the genome of a related click beetle, the Caribbean Ignelater luminosus , with bioluminescent biochemistry near-identical to fireflies, but anatomically unique light organs, suggesting the intriguing hypothesis of parallel gains of bioluminescence. Our analyses support independent gains of bioluminescence in fireflies and click beetles, and provide new insights into the genes, chemical defenses, and symbionts that evolved alongside their luminous lifestyle.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 26, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

Fireflies (Coleoptera: Lampyridae) represent the best-studied case of bioluminescence. The coded language of their luminous courtship displays (Figure 1A; Video 1) has been long studied for its role in mate recognition, while non-adult bioluminescence is likely a warning signal of their unpalatable chemical defenses, such as the cardiotoxic lucibufagins of Photinus fireflies. The biochemical understanding of firefly luminescence: an ATP, Mg2+, and O2-dependent luciferase-mediated oxidation of the substrate luciferin, along with the cloning of the luciferase gene, led to the widespread use of luciferase as a reporter with unique applications in biomedical research and industry. With >2000 species globally, fireflies are undoubtedly the most culturally appreciated bioluminescent group, yet there are at least three other beetle families with bioluminescent species: click beetles (Elateridae), American railroad worms (Phengodidae) and Asian starworms (Rhagophthalmidae). These four closely related families (superfamily Elateroidea) have homologous luciferases and structurally identical luciferins, implying a single origin of beetle bioluminescence. However, as Darwin recognized in his ‘Difficulties on Theory’, the light organs amongst the luminous beetle families are clearly distinct (Figure 1B), implying independent origins. Thus, whether beetle bioluminescence is derived from a single or multiple origin(s) remains unresolved.

To address this long-standing question, we sequenced and analyzed the genomes of three bioluminescent beetle species. To represent the fireflies, we sequenced the widespread North American ‘Big Dipper Firefly’, P. pyralis (Figure 1A,C) and the Japanese ‘Heike-botaru’ firefly Aquatica lateralis (Figure 1B). P. pyralis was used in classic studies of firefly bioluminescent biochemistry and the cloning of luciferase, while A. lateralis, a species with specialized aquatic larvae, is one of the few fireflies that can be reliably cultured in the laboratory. These two fireflies represent the two major firefly subfamilies, Lampyrinae and Luciolinae, which diverged from a common ancestor over 100 Mya (Figure 1B). To facilitate evolutionary comparisons, we also sequenced the ‘Cucubano’, Ignelater luminosus (Figure 1B), a Caribbean bioluminescent click beetle, and member of the ‘Pyrophorus’ used by Raphaël Dubois (1849-1929) to first establish the enzymatic basis of bioluminescence in the late 1800s. Comparative analyses of the genomes of these three species allowed us to reconstruct the origin(s) and evolution of beetle bioluminescence.

Sequencing and assembly of firefly and click-beetle genomes

Photinus pyralis adult males were collected from the Great Smoky Mountains National Park, USA (GSMNP) and Mercer Meadows New Jersey, USA (MMNJ) (Figure 1C), and sequenced using short-insert, mate-pair, Hi-C, and long-read Pacific Biosciences (PacBio) approaches (Appendix 4—table 1). These datasets were combined in a MaSuRCA hybrid genome assembly (Appendix 1.5). The Aquatica lateralis genome was derived from an ALL-PATHs assembly of short insert and mate-pair reads from a single adult female from a laboratory-reared population, whose lineage, dubbed ‘Ikeya-Y90’, was first collected 25 years ago from a now extinct population in Yokohama, Japan (Appendix 2.5). A single Ignelater luminosus adult male, collected in Mayagüez Puerto Rico, USA, was used to produce a high-coverage Supernova linked-read draft genome (Appendix 3.5), which was further manually scaffolded using low-coverage long-read Oxford Nanopore MinION sequencing (Appendix 3.5.4).

The gene completeness and contiguity statistics of our P. pyralis (Ppyr1.3) and A. lateralis (Alat1.3) genome assemblies are comparable to the genome of the model beetle Tribolium castaneum (Figure 2F; Appendix 4.1). The I. luminosus genome assembly (Ilumi1.2) is less complete, but is comparable to other published insect genomes (Figure 2F; Appendix 4.1). Protein-coding genesets for our study species were produced via an EvidenceModeler-mediated combination of homology alignments, ab initio predictions, and de novo and reference-guided RNA-seq assemblies followed by manual gene curation for gene families of interest (Appendix 1.10; 2.8; 3.8). These coding gene annotation sets for P. pyralis, A. lateralis, and I. luminosus are comprised of 15,773, 14,285, and 27,557 genes containing 94.2%, 90.0%, and 91.8% of the Endopterygota Benchmarking Universal Single-Copy Orthologs (BUSCOs), respectively. Protein clustering via predicted orthology indicated 77% of genes were found in orthogroups with at least one other species (Figure 2E; Appendix 4—figure 1). We found the greatest orthogroup overlap between the P. pyralis and A. lateralis genesets, as expected given the more recent phylogenetic divergence of these species. Remaining redundancy in the P. pyralis assembly and annotation, as indicated by duplicates of the BUSCOs and the assembly size (Figure 2F; Appendix 4—table 2) is likely due to the heterozygosity of the outbred input libraries (Appendix 1). The higher BUSCO completeness of the assemblies as compared to the genesets (Appendix 4—table 3), suggests that future manual curation efforts will lead to improved annotation completeness.

To enable the characterization of long-range genetic structure, we super-scaffolded the P. pyralis genome assembly into 11 pseudo-chromosomal linkage groups using a Hi-C proximity-ligation linkage approach (Figure 2A; Appendix 1.5.3). These linkage groups contain 95% of the assembly (448.8 Mbp). Linkage group LG3a corresponds to the X-chromosome based on expected adult XO male read coverage and gene content (Appendix 1.6.4.1) and its size (22.2 Mbp) is comparable to the expected X-chromosome size based on sex-specific genome size estimates using flow cytometry (~26 Mbp). Homologs to T. castaneum X-chromosome genes were enriched on LG3a over every other linkage group, suggesting that the X-chromosomes of these distantly related beetles are homologous, and that their content has been reasonably conserved for >200 MY (Appendix 1.6.4.1). We hypothesized that the P. pyralis orthologs of known bioluminescence genes, including the canonical luciferase Luc1 and the specialized luciferin sulfotransferase LST, would be located on the same linkage group to facilitate chromosomal looping and enhancer assisted co-expression within the light organ. We, however, found these genes on separate linkage groups (Figure 2A).

In addition to nuclear genome assembly and coding gene annotation, we also assembled the complete mitochondrial genomes (mtDNA) of P. pyralis (Figure 2C; Appendix 1.8) and I. luminosus (Appendix 3.10), while the mtDNA sequence of A. lateralis was recently published. These mtDNA assemblies show high conservation of gene content and synteny, with the exception of the variable ~1 Kbp tandem repeat unit (TRU) found in the firefly mtDNAs.

As repetitive elements are common participants and drivers of genome evolution, we next sought to characterize the repeat content of our genome assemblies. Overall, 42.6%, 19.8%, and 34.1% of the P. pyralis, A. lateralis, and I. luminosus assemblies were found to be repetitive, respectively (Appendix 1.11; 2.9; 3.9). Of these repeats 66.7%, 39.4%, and 55% could not be classified as any known repetitive sequence, respectively. Helitrons, DNA transposons that transpose through rolling circle replication, are among the most abundant individual repeat elements in the P. pyralis assembly. Via in situ hybridization, we identified that P. pyralis chromosomes have canonical telomeres with telomeric repeats (TTAGG) (Figure 2B; Appendix 1.13).

DNA methylation is common in eukaryotes, but varies in degree across insects, especially within Coleoptera. Furthermore, the functions of DNA methylation across insects remain obscure. To examine firefly cytosine methylation, we characterized the methylation status of P. pyralis DNA with whole genome bisulfite sequencing (WGBS). Methylation at CpGs (mCG) was unambiguously detected at ~20% within the genic regions of P. pyralis and its methylation levels were at least twice those reported from other holometabolous insects (Figure 2D; Appendix 1.12). Molecular evolution analyses of the DNA methyltransferases (DNMTs) show that direct orthologs of both DNMT1 and DNMT3 were conserved in P. pyralis, A. lateralis, and I. luminosus (Appendix 4—figure 2; Appendix 4.2.3), implying that our three study species, and inferentially likely most firefly lineages, possess mCG. Corroborating this claim, CpG[O/E] analysis of methylation indicated our three study species had DNA methylation (Appendix 4—figure 3).

The genomic context of firefly luciferase evolution

Two luciferase paralogs have been previously described in fireflies. P. pyralis Luc1 was the first firefly luciferase cloned, and its direct orthologs have been widely identified from other fireflies. The luciferase paralog Luc2 was previously known only from a handful of Asian taxa, including A. lateralis. Previous investigations of these Asian taxa have shown that Luc1 is responsible for light production from the lanterns of adults, larvae, prepupae and pupae, whereas Luc2 is responsible for the dim glow of eggs, ovaries, prepupae and the whole pupal body. From our curated genesets (Appendix 1.10; 2.8), we unequivocally identified two firefly luciferases, Luc1 and Luc2, in both the P. pyralis and A. lateralis genomes. Our RNA-Seq data further show that in both P. pyralis and A. lateralis, Luc1 and Luc2 display expression patterns consistent with previous reports. While Luc1 is the sole luciferase expressed in the lanterns of both larvae and adults, regardless of sex, Luc2 is expressed in other tissues and stages, such as eggs (Figure 3C). Notably, Luc2 expression is detected in RNA libraries derived from adult female bodies (without head or lantern), suggesting detection of ovary expression as described in previous studies. Together, these results support that since their divergence via gene duplication prior to the divergence of Lampyrinae and Luciolinae, Luc1 and Luc2 have established different, but conserved roles in bioluminescence throughout the firefly life cycle.

Firefly luciferase is hypothesized to be derived from an ancestral peroxisomal fatty acyl-CoA synthetase (PACS) (Figure 3A). We found that, in both firefly species, Luc1 is genomically clustered with its closely related homologs, including PACSs and non-peroxisomal acyl-CoA synthetases (ACSs), enzymes which can be distinguished by the presence/absence of a C-terminal peroxisomal-targeting-signal-1 (PTS1). We also found nearby microsomal glutathione S-transferase (MGST) family genes (Figure 3D) that are directly orthologous between both species, Genome-wide phylogenetic analysis of the luciferases, PACSs and ACSs genes indicates that Luc1 and Luc2 form two orthologous groups, and that the neighboring PACS and ACS genes near Luc1 form three major clades (Figure 3C): Clade A, whose common ancestor and most extant members are ACSs, and Clades B and C whose common ancestors and most extant members are PACSs. Luc1 and Luc2 are highly conserved at the level of gene structure—both are composed of seven exons with completely conserved exon/intron boundaries (Appendix 4—figure 4; Appendix 4—figure 5), and most members of Clades A, B, and C also have seven exons. The exact syntenic and orthology relationships of the ACS and PACS genes adjacent to the Luc1 locus remains unclear, likely due to subsequent gene divergence and shuffling (Figure 3C,D).

Luc2 is located on a different linkage-group from Luc1 in P. pyralis and on a different scaffold from Luc1 in A. lateralis, consistent with the interpretation that Luc1 and Luc2 lie on different chromosomes in both firefly species. No PACS or ACS genes were found in the vicinity of Luc2 in either species. These data support that tandem gene duplication in a firefly ancestor gave rise to several ancestral PACS paralogs, one of which neofunctionalized in place to become the ancestral luciferase (AncLuc) (Figure 3B). Prior to the divergence of the firefly subfamilies Lampyrinae and Luciolinae around 100 Mya (Appendix 4.3), this AncLuc duplicated, possibly via a long-range gene duplication event (e.g. transposon mobilization), and then subfunctionalized in its transcript expression pattern to give rise to Luc2, while the original AncLuc subfunctionalized in place to give rise to Luc1 (Figure 3B). From the shared Luc gene clustering in both fireflies, we infer the structure of the pre Luc1/Luc2 duplication AncLuc locus contained one or more ACS genes (Clade A), one or more PACS genes (Clade B/C), and one or more MGST family genes (Figure 3B).

Independent origins of firefly and click beetle luciferase

To resolve the number of origins of luciferase activity, and therefore bioluminescence, between fireflies and click beetles, we first identified the luciferase of I. luminosus luciferase (IlumLuc), and compared its genomic context to the luciferases of P. pyralis and A. lateralis (Figure 3D). Unlike some other described bioluminescent Elateridae, which have separate luciferases expressed in the dorsal prothorax and ventral abdominal lanterns, we identified only a single luciferase in the I. luminosus genome which was highly expressed in both of the lanterns (Figure 3C; Appendix 3.8). The exon number and exon-intron splice junctions of IlumLuc are identical to those of firefly luciferases, but unlike the firefly luciferases which have short introns less than <100 bp long, IlumLuc has two long introns (Appendix 4—figure 4). We found several PACS genes in the I. luminosus genome which were related to IlumLuc and formed a clade (Clade D) specific to the Elateridae (Figure 3C,D). IlumLuc lies on a 366 Kbp scaffold containing 18 other genes, including three related Clade D PACS genes (Scaffold 13255; Figure 3D; Figure 4); however, the Clade D genes that are most closely related to IlumLuc are found on a separate 650 Kbp scaffold (Scaffold 9864; Figure 3D). We infer that the IlumLuc locus is not orthologous to the extant firefly Luc1 locus, as IlumLuc is not physically clustered with Clade A, B or C ACS or PACS genes (Figure 3C,D). We instead identified a different scaffold in I. luminosus that is likely orthologous to the firefly Luc1 locus (Scaffold 9654; Figure 3D). This assessment is based on the presence of adjacent Clade A and B ACS and PACS genes, as well as orthologous exoribonuclease family (PRNT) and inositol monophosphatase family (IMP) genes, both of which were found adjacent to the A. lateralis Luc1 locus, but not the P. pyralis Luc1 locus (Figure 3D). Interestingly, IlumPACS11, the most early-diverging member of Clade D, was also found on Scaffold 9654 (Figure 3D). This finding is consistent with an expansion of Clade D following duplication of the IlumPACS11 syntenic ancestor to a distant site. Overall, these genomic structures are consistent with independent origins of firefly and click beetle luciferases.

We then carried out targeted molecular evolution analyses including the known beetle luciferases and their closely related homologs. Ancestral state reconstruction of luminescent activity on the gene tree using Mesquite recovered two independent gains of luminescence as the most parsimonious and likely scenario: once in click beetles, and once in the common ancestor of firefly, phengodid, and rhagophthalmid beetles (Figure 4A; Appendix 4.3.3). In an independent molecular adaptation analysis utilizing the coding nucleotide sequence of the elaterid luciferases and their close homologs within Elateridae, 35% of the sites of the branch leading to the ancestral click beetle luciferase showed a statistically significant signal of episodic positive selection with dN/dS > 1 (ω or max dN/dS = 3.98) as compared to the evolution of its paralogs using the aBSREL branch-site selection test (Figure 4B; Appendix 4.3.4). This implies that the common ancestor of the click beetle luciferases (EAncLuc) underwent a period of accelerated directional evolution. As the branch under selection in the molecular adaptation analysis (Figure 4B) is the same branch of luciferase activity gain via ancestral reconstruction (Figure 4A), we conclude that the identified selection signal represents the relatively recent neofunctionalization of click beetle luciferase from a non-luminous ancestral Clade D PACS gene, distinct from the more ancient neofunctionalization of firefly luciferase. Based on the constraints from our tree, we determine that this neofunctionalization of EAncLuc occured after the divergence of the elaterid subfamily Agrypninae. In contrast, we cannot determine if the original neofunctionalization of AncLuc occurred in the ancestral firefly, or at some point during the evolution of ‘cantharoid’ beetles, an unofficial group of beetles including the luminous Rhagophthalmidae, Phengodidae and Lampyridae among other non-luminous groups, but not the Elateridae. There is evidence for a subsequent luciferase duplication event in phengodids, but not in rhagophthalmids, that is independent of the duplication event that gave rise to Luc1 and Luc2 in fireflies (Figures 3C and 4). Altogether, our results strongly support the independent neofunctionalization of luciferase activity in click beetles and fireflies, and therefore at least two independent gains of luciferin-utilizing luminescence in beetles.

Metabolic adaptation of the firefly lantern

Beyond luciferase, we sought to characterize other metabolic traits which might have co-evolved in fireflies to support bioluminescence. Of particular importance, the enzymes of the de novo biosynthetic pathway for firefly luciferin remain unknown. We hypothesized that bioluminescent accessory enzymes, either specialized enzymes with unique functions in luciferin metabolism or enzymes with primary metabolic functions relevant to bioluminescence, would be highly expressed (HE: 90th percentile; Appendix 4.2.2) in the adult lantern, and would be differentially expressed (DE; Appendix 4.2.2) between luminescent and non-luminescent tissues. To determine this, we performed RNA-Seq and expression analysis of the dissected P. pyralis and A. lateralis adult male lantern tissue compared with a non-luminescent tissue (Appendix 4.2.2). We identified a set of predicted orthologous enzyme-encoding genes conserved in both P. pyralis and A. lateralis that met our HE and DE criteria (Figure 5). Both luciferase and luciferin sulfotransferase (LST), a specialized enzyme recently implicated in luciferin storage in P. pyralis, were recovered as candidate genes using four criteria (HE, DE, enzymes, direct orthology across species), confirming the validity of our approach. While a direct ortholog of LST is present in A. lateralis, it is absent from I. luminosus, suggesting that LST, and the presumed luciferin storage it mediates, is an exclusive ancestral firefly or cantharoid trait. This finding is consistent with previous hypotheses of the absence of LST in Elateridae, and with the overall hypothesis of independent evolution of bioluminescence between the Lampyridae and Elateridae.

Moreover, we identified several additional enzyme-encoding HE and DE lantern genes that are likely important in firefly lantern physiology (Figure 5). For instance, adenylate kinase likely plays a critical role in efficient recycling of AMP post-luminescence, and cystathionine gamma-lyase supports a key role of cysteine in luciferin biosynthesis and recycling. We also detected a combined adenylyl-sulfate kinase and sulfate adenylyltransferase enzyme (ASKSA) among the lantern-enriched gene list (Appendix 4—figure 8), implicating active biosynthesis of 3'-phosphoadenosine-5'-phosphosulfate (PAPS), the cofactor of LST, in the lantern. This finding highlights the importance of LST-catalyzed luciferin sulfonation for bioluminescence. These firefly orthologs of ASKSA are the only members amongst their paralogs to contain a PTS1 (Appendix 4—figure 8), suggesting specialized localization to the peroxisome, the location of the luminescence reaction. This suggests that the levels of sulfoluciferin and luciferin may be actively regulated within the peroxisome of lantern cells in response to luminescence. Overall, our findings of several directly orthologous enzymes that share expression patterns in the light organs of both P. pyralis and A. lateralis suggests that the enzymatic physiology and/or the gene expression patterns of the photocytes were already fixed in the Luciolinae-Lampyrinae ancestor.

We also performed a similar expression analysis for genes not annotated as enzymes, yielding several genes with predicted lysosomal function (Appendix 4—table 6; Appendix 4.4). This suggests that the abundant but as yet unidentified ‘differentiated zone granule’ organelles of the firefly light organ could be lysosomes. Interestingly, we found a HE (TPM value ~300) and DE opsin, Rh7, in the light organ of A. lateralis, but not P. pyralis (Appendix 4—figure 9; Appendix 4.5), suggesting a potential light perception role for Rh7 in the A. lateralis lantern, akin to the light perception role described for Drosophila Rh7.

Genomic insights into firefly chemical defense

Firefly bioluminescence is postulated to have first evolved as an aposematic warning of larval chemical defenses. Lucibufagins are abundant unpalatable defense steroids described from certain North American firefly species, most notably in the genera Photinus, Lucidota, and Ellychnia, and hence are candidates for ancestral firefly defense compounds. To test whether lucibufagins are widespread among bioluminescent beetles, we assessed the presence of lucibufagins in P. pyralis, A. lateralis, and I. luminosus by liquid-chromatography high-resolution accurate-mass mass-spectrometry (LC-HRAM-MS). While lucibufagins were found in high abundance in P. pyralis adult hemolymph, they were not observed in A. lateralis adult hemolymph, nor in I. luminosus metathorax extract (Figure 6B; Appendix 4.6). Since chemical defense is presumably most critical in the long-lived larval stage, we next tested whether lucibufagins are present in all firefly larvae even if they are not present in the adults of certain species. We found lucibufagins in P. pyralis larval extracts; however, they were not observed in A. lateralis larval extracts (Figure 6B; Appendix 4.6). Together, these results suggest that the lucibufagin biosynthetic pathway is either a derived trait only found in particular firefly taxa (e.g. subfamily: Lampyrinae), or that lucibufagin biosynthesis was an ancestral trait that was lost in A. lateralis. Consistent with the former hypothesis, the presence of lucibufagins in non-North-American Lampyrinae has been previously reported, but to date there are no reports of lucibufagins in the Luciolinae.

The lucibufagin biosynthetic pathway is currently unknown. However, their chemical structure suggests a biosynthetic origin from cholesterol followed by a series of hydroxylations, -OH acetylations, and the side-chain oxidative pyrone formation (Figure 6A). We hypothesized that cytochrome P450s, an enzyme family widely involved in metabolic diversification of organic substrates, could underlie several oxidative reactions in the proposed lucibufagin biosynthetic pathway. We therefore inferred the P450 phylogeny among our three bioluminescent beetle genomes to identify any lineage-specific genes correlated with lucibufagin presence. Our analysis revealed a unique expansion of one P450 family, the CYP303 family, in P. pyralis. While 94/97 of currently sequenced winged-insect genomes on OrthoDB, as well as the A. lateralis and I. luminosus genomes, contain only a single CYP303 family gene, the P. pyralis genome contains 11 CYP303 genes and two pseudogenes (Figure 6C), which expanded via tandem duplication on the same linkage group (Figure 6D). The CYP303 ortholog of D. melanogaster, CYP303A1, has been shown to play a role in mechanosensory bristle development. Although the exact biochemical function and substrate of D. melanogaster CYP303A1 is unknown, its closely related P450 families operate on an insect steroid hormone ecdysone. As ecdysone and lucibufagins are structurally similar, CYP303 may operate on steroid-like compounds. Therefore, the lineage-specific expansion of the CYP303 family in P. pyralis is a compelling candidate in the metabolic evolution of lucibufagins as chemical defenses associated with the aposematic role of bioluminescence. Alternatively, this CYP303 expansion in P. pyralis may be associated with other lineage-specific chemical traits, such as pheromone production.

Symbionts of bioluminescent beetles

Given the increasingly recognized contributions of symbionts to host metabolism, we characterized the hologenome of all three beetles as potential contributors to metabolic processes related to bioluminescence. Whole genome sequencing of our wild-caught and laboratory reared fireflies revealed a rich microbiome. Amongst our firefly genomes, we found various bacterial genomes, viral genomes, and the complete mtDNA for a phorid parasitoid fly, Apocephalus antennatus, the first mtDNA reported for genus Apocephalus. This mtDNA was inadvertently included in the P. pyralis PacBio library via undetected parasitization of the initial specimens, and was assembled via a metagenomic approach (Appendix 5.2). Independent collection of A. antennatus which emerged from field-collected P. pyralis adults and targeted COI sequencing later confirmed the taxonomic origin of this mtDNA (Appendix 5.3). We also sequenced and metagenomically assembled the complete circular genome (1.29 Mbp, GC: 29.7%; ~50x coverage) for a P. pyralis-associated mollicute (Phylum: Tenericutes), Entomoplasma luminosum subsp. pyralis (Appendix 5.1). Entomoplasma spp. were first isolated from the guts of North American fireflies and our assembly provides the first complete genomic assembly of any Entomoplasma species. Broad read coverage for the E. luminosus subsp. pyralis genome was detected in 5/6 of our P. pyralis DNA libraries, suggesting that Entomplasma is a highly prevalent, possibly vertically inherited, P. pyralis symbiont. It has been hypothesized that these Entomoplasma mollicutes could play a role in firefly metabolism, specifically via contributing to cholesterol metabolism and lucibufagin biosynthesis.

Within our unfiltered A. lateralis genomic assembly (Alat1.2), we also found 43 scaffolds (2.3 Mbp; GC:29.8%, ~64x coverage), whose taxonomic annotation corresponded to the Tenericutes (Appendix 2.5.2), suggesting that A. lateralis may also harbor a mollicute symbiont. Alat1.2 also contains 2119 scaffolds (13.0 Mbp, GC:63.7%, ~25x coverage) annotated as of Proteobacterial origin. Limited Proteobacterial symbionts were detected in the I. luminosus assembly (0.4 Mbp; GC:30–65% ~10x coverage) (Appendix 3.5.2), suggesting no stable symbiont is present in adult I. luminosus. Lastly, we detected two species of novel orthomyxoviridae-like ssRNA viruses, which we dub Photinus pyralis orthomyxo-like virus 1 and 2 (PpyrOMLV1/2), that were highly prevalent across our P. pyralis RNA-Seq datasets, and showed multi-generational transovarial transmission in the laboratory (Appendix 5.4). We also found several endogenous viral elements (EVEs) for PpyrOMLV1/2 in P. pyralis (Appendix 5.5). These viruses are the first reported in any firefly species, and represent only the second report of transgenerational transfer of any Orthomyxoviridae virus, and the second report of Orthomyxoviridae derived EVEs. Together, these genomes from the firefly holobiont provide valuable resources for the continued inquiry of the symbiotic associates of fireflies and their biological and ecological significance.

Discussion

Here, we generated genome assembles, diverse tissue and life-stage RNA-Seq data, and LC/MS data for three evolutionarily informative and historically well-studied bioluminescent beetles, and used a series of comparative analyses to illuminate long-standing questions on the origins and evolution of beetle bioluminescence. By analyzing the genomic synteny and molecular evolution of the beetle luciferases and their extant and inferred-ancestral homologs, we found strong support for the independent origins of luciferase, and therefore bioluminescence, between fireflies and click beetles. Our approaches and analyses lend molecular evidence to the previous morphology-phylogeny based hypotheses of parallel gain proposed by Darwin and others. While our elaterid luciferase selection analysis strongly supports an independent gain, we did not perform an analogous selection analysis of luciferase homologs across all bioluminescent beetles, due to the lack of genomic data from key related beetle families. Additional genomic information from early-diverged firefly lineages, other luminous beetle taxa (e.g. Phengodidae and Rhagophthalmidae), and non-luminous elateroid taxa (e.g. Cantharidae and Lycidae), will be useful to further develop and test models of luciferase evolution, including the hypothesis that bioluminescence also originated independently in the Phengodidae and/or Rhagophthalmidae. As some phylogenetic relationships of fireflies and other lineages of superfamily Elateroidea remain uncertain, continued efforts to produce reference phylogeny for these taxa are required. Toward this goal, the recently published Pyrocoelia pectoralis Lampyrinae firefly genome is an important advance which will contribute to future phylogenetic and evolutionary studies.

The independent origins of the firefly and click beetle luciferases provide an exemplary natural model system to understand enzyme evolution through parallel mutational trajectories and the evolution of complex metabolic traits generally. The abundance of gene duplication events of PACSs and ACSs at the ancestral luciferase locus in both fireflies and I. luminosus suggests that ancestral promiscuous enzymatic activities served as raw materials for the selection of new adaptive catalytic functions. But while parallel evolution of luciferase implies evolutionary independence of bioluminescence overall, the reality may be more complex, and the other subtraits of bioluminescence amongst the bioluminescent beetles likely possess different evolutionary histories from luciferase. While subtraits presumably dependent on an efficient luciferase, such as specialized tissues and neural control, almost certainly arose well after luciferase specialization, and thus can be inferred to also have independent origins between fireflies and click beetles, luciferin, which was presumably a prerequisite to luciferase neofunctionalization, may have been present in their common ancestor. Microbial endosymbionts, such as the tenericutes detected in our P. pyralis and A. lateralis datasets, are intriguing candidate contributors to luciferin metabolism and biosynthesis. Alternatively, recent reports have shown that firefly luciferin is readily produced non-enzymatically by mixing benzoquinone and cysteine, and that a compound resulting from the spontaneous coupling of benzoquinone and cysteine acts as a luciferin biosynthetic intermediate in A. lateralis. Benzoquinone is known to be a defense compound of distantly related beetles and other arthropods (e.g. millipedes). Therefore, the evolutionary role of sporadic low-level luciferin synthesis through spontaneous chemical reactions, either in the ancestral bioluminescent taxa themselves, or in non-bioluminescent taxa, and dietary acquisition of luciferin by either the ancestral or modern bioluminescent taxa, should be considered. To decipher between these alternative evolutionary possibilities, the discovery of genes involved in luciferin metabolism in fireflies and other bioluminescent beetles will be essential. Here, as a first step toward that goal, we identified conserved, enriched and highly expressed enzymes of the firefly lantern that are strong candidates in luciferin metabolism and the elusive luciferin de novo biosynthetic pathway. Ultimately focused experimentation will be needed to decipher the biochemical function of these enzymes.

The early evolution of firefly bioluminescence was likely associated with an aposematic role. The adaptive light production of the primordial firefly (or alternatively, a primordial bioluminescent cantharoid beetle) that enabled the selection and neofunctionalization of luciferase was perhaps linked to a response to predators by a primitive whole-body oxygen-gated luminescence, where a startle-response mediated increase in hemolymph oxygenation through spiracle opening and escape locomotion caused a concomitant increase in luminescence. Alternatively, an early role for firefly luminescence in mate attraction has not been ruled out. The presence of particular unpalatable defense compounds in all extant fireflies would be consistent with an ancestral role and the former hypothesis, and the chemical analysis of tissues across species and life stages presented in this work provides new insights into the evolutionary occurrence of lucibufagins, the most well-studied defense compounds associated with fireflies. Our results reject lucibufagins as ancestral defense compounds of fireflies, but rather suggest them as a derived metabolic trait associated with Lampyrinae. Additional chemical analyses across more lineages of fireflies are needed, however, to further support or falsify this hypothesis. Toward this goal, the high sensitivity of our LC-HRAM-MS and MS2 molecular networking-based lucibufagin identification approach is particularly well suited to broadened sampling in the future, including those of rare taxa and possibly museum specimens. Combined with genomic data showing a concomitant expansion of the CYP303 gene family in P. pyralis, we present a promising path toward elucidating the biosynthetic mechanism underlying these potent firefly toxins.

Overall, the resources and analyses generated in this study shed valuable light on the evolutionary questions Darwin first pondered, and will enable future studies of the ecology, behavior, and evolution of bioluminescent beetles. These resources will also accelerate the discovery of new enzymes from bioluminescent beetles that could enhance biotechnological applications of bioluminescence. Finally, we hope that the genomic resources shared here will facilitate the development of effective population genomic tools to monitor and protect wild bioluminescent beetle populations in the face of changing climate and habitats.

Materials and methods

Detailed materials and methods are available in the Appendices. Methods relating to P. pyralis are given in Appendix 1, while methods relating to A. lateralis and I. luminosus are given in Appendix 2 and Appendix 3, respectively. Methods for comparative genomic analyses are given in Appendix 4, while methods for microbiome characterization are given in Appendix 5. References to relevant sections of the Appendices are placed in-line throughout the maintext.

Data and materials availability

Genomic assemblies (Ppyr1.3, Alat1.3, and Ilumi1.2), associated official geneset data, a SequenceServer BLAST server, and a JBrowse genome browser are available at www.fireflybase.org. Raw genomic and RNA-Seq reads for P. pyralis, A. lateralis, and I. luminosus, are available under the NCBI/EBI/DDBJ BioProjects PRJNA378805, PRJDB6460, and PRJNA418169 respectively. Raw WGBS reads can be found on the NCBI Gene Expression Omnibus (GSE107177). Mitochondrial genomes for P. pyralis and I. luminosus and A. antennatus are available on NCBI GenBank with accessions KY778696, MG242621, and MG546669. The complete genome of Entomoplasma luminosum subsp. pyralis is available on NCBI GenBank with accession CP027019. The viral genomes for Photinus pyralis orthomyxo-like virus 1 and 2 are available on NCBI Genbank with accessions MG972985-MG972994. LC-MS data is available on MetaboLights (Accession MTBLS698). Other supporting datasets are available on FigShare (Appendix 6.1).

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    Hackett KJ, Whitcomb RF, Tully JG, Lloyd JE, Anderson JJ, Clark TB, Henegar RB, Roset DL, Clark EA, Vaughn JL. Lampyridae (Coleoptera): A plethora of mollicute associations. Microbial Ecology. 1992;23:181-193.

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    Haig DA, Woodall JP, Danskin D. Thogoto virus: a hitherto underscribed agent isolated from ticks in Kenya. Journal of General Microbiology. 1965;38:389-394.

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    Hall RA, Bielefeldt-Ohmann H, McLean BJ, O'Brien CA, Colmant AMG, Piyasena TBH, Harrison JJ, Newton ND, Barnard RT, Prow NA, Deerain JM, Mah MGKY, Hobson-Peters J. Commensal viruses of mosquitoes: host restriction, transmission, and interaction with arboviral pathogens. Evolutionary Bioinformatics. 2016;12s2:EBO.S40740.

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    Hamberger B, Bak S. Plant P450s as versatile drivers for evolution of species-specific chemical diversity. Philosophical Transactions of the Royal Society B: Biological Sciences. 2013;368:20120426.

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  115. 115.

    Han Y, Wessler SR. MITE-Hunter: a program for discovering miniature inverted-repeat transposable elements from genomic sequences. Nucleic Acids Research. 2010;38:e199.

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    Hara K, Kashiwagi T, Hamada N, Watanabe H. Basic amino acids in the N-terminal half of the PB2 subunit of influenza virus RNA polymerase are involved in both transcription and replication. Journal of General Virology. 2017;98:900-905.

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  117. 117.

    Harvey EN, Stevens KP. The brightness of the light of the west indian elaterid beetle, Pyrophorus. The Journal of General Physiology. 1928;12:269-272.

    Not in our library10.1085/jgp.12.2.269

  118. 118.

    Harvey EN. Bioluminescence. 1952.

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  119. 119.
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    Helvig C, Koener JF, Unnithan GC, Feyereisen R. CYP15A1, the cytochrome P450 that catalyzes epoxidation of methyl farnesoate to juvenile hormone III in cockroach corpora Allata. PNAS. 2004;101:4024-4029.

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  122. 122.

    Hengrung N, El Omari K, Serna Martin I, Vreede FT, Cusack S, Rambo RP, Vonrhein C, Bricogne G, Stuart DI, Grimes JM, Fodor E. Crystal structure of the RNA-dependent RNA polymerase from influenza C virus. Nature. 2015;527:114-117.

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    Herb BR, Wolschin F, Hansen KD, Aryee MJ, Langmead B, Irizarry R, Amdam GV, Feinberg AP. Reversible switching between epigenetic states in honeybee behavioral subcastes. Nature Neuroscience. 2012;15:1371-1373.

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    Hsu MT, Parvin JD, Gupta S, Krystal M, Palese P. Genomic RNAs of influenza viruses are held in a circular conformation in Virions and in infected cells by a terminal panhandle. PNAS. 1987;84:8140-8144.

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    Huson DH, Scornavacca C. Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Systematic Biology. 2012;61:1061-1067.

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    Hyslop JA. The phylogeny of the Elateridae based on larval characters. Annals of the Entomological Society of America. 1917;10:241-263.

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    Ikeya H. Melanic strain of Luciola lateralis. Bull Firefly Mus Toyota Town. 2016;8:175-177.

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  131. 131.

    Imperial Palace Outer Garden Management Office. Efforts to protect heike fireflies living in the moat of the Imperial Palace Gardens. 2017.

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  132. 132.

    iNaturalist. Common eastern firefly (Photinus pyralis). 2017.

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    Inoue M, Yamamoto H. Cytological studies of family Lampyridae I. karyotypes of Luciola lateralis and L. Cruciata. La Kromosomo. 1987;II-45:1440-1443.

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    Johnson PJ, Arnett R. H, Thomas M. C, Skelley P. E, Frank J. H. American Beetles. 2002;2:160-173.

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  135. 135.

    Käll L, Krogh A, Sonnhammer EL. A combined transmembrane topology and signal peptide prediction method. Journal of Molecular Biology. 2004;338:1027-1036.

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    Kanda S. Hotaru. 1935.

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    Kanie S, Nishikawa T, Ojika M, Oba Y. One-pot non-enzymatic formation of firefly luciferin in a neutral buffer from p-benzoquinone and cysteine. Scientific Reports. 2016;6:24794.

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    Kanie S, Nakai R, Ojika M, Oba Y. 2-S-cysteinylhydroquinone is an intermediate for the firefly luciferin biosynthesis that occurs in the pupal stage of the japanese firefly, Luciola lateralis. Bioorganic Chemistry. 2018;80:223-229.

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  139. 139.

    Kapitonov VV, Jurka J. Rolling-circle transposons in eukaryotes. PNAS. 2001;98:8714-8719.

    Not in our library10.1073/pnas.151269298

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    Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution. 2013;30:772-780.

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    Kawashima I, Suzuki H, Sato M. A check-list of Japanese fireflies (Coleoptera, Lampyridae and Rhagophthalmidae). Japanese Society of Systematic Entomology. 2003;9:241-261.

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    Kazantsev SV. Protoluciola albertalleni gen. n., sp. n., a new luciolinae firefly (Insecta: Coleoptera: Lampyridae). Russian Entomological Journal. 2015;24:281-283.

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    Kimble JB. Zoonotic Transmission of Influenza H9 subtype through Reassortment. 2013.

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  148. 148.

    King AMQ, Lefkowitz E, Adams MJ, Carstens EB. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. 2011.

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  149. 149.
  150. 150.

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  151. 151.

    Koutsovoulos G, Kumar S, Laetsch DR, Stevens L, Daub J, Conlon C, Maroon H, Thomas F, Aboobaker AA, Blaxter M. No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini. PNAS. 2016;113:5053-5058.

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  154. 154.

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    Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. Circos: an information aesthetic for comparative genomics. Genome Research. 2009;19:1639-1645.

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  156. 156.

    Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution. 2016;33:1870-1874.

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  157. 157.

    Kundrata R, Bocak L. The phylogeny and limits of Elateridae (Insecta, coleoptera): is there a common tendency of click beetles to soft-bodiedness and neoteny? Zoologica Scripta. 2011;40:364-378.

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  158. 158.

    Kyrpides NC, Woyke T, Eisen JA, Garrity G, Lilburn TG, Beck BJ, Whitman WB, Hugenholtz P, Klenk HP. Genomic encyclopedia of type strains, phase I: the one thousand microbial genomes (KMG-I) project. Standards in Genomic Sciences. 2014;9:1278-1284.

    Not in our library10.4056/sigs.5068949

  159. 159.

    Laetsch DR, Blaxter ML. BlobTools: interrogation of genome assemblies. F1000Research. 2017;6:1287.

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    Langmead B, Salzberg SL. Fast gapped-read alignment with bowtie 2. Nature Methods. 2012;9:357-359.

    Not in our library10.1038/nmeth.1923

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    Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and clustal X version 2.0. Bioinformatics. 2007;23:2947-2948.

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    Larracuente AM, Ferree PM. Simple method for fluorescence DNA in situ hybridization to squashed chromosomes. Journal of Visualized Experiments. 2015;52288.

    Not in our library10.3791/52288

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  165. 165.

    Leahy MB, Dessens JT, Weber F, Kochs G, Nuttall PA. The fourth genus in the Orthomyxoviridae: sequence analyses of two thogoto virus polymerase proteins and comparison with influenza viruses. Virus Research. 1997;50:215-224.

    Not in our library10.1016/s0168-1702(97)00072-5

  166. 166.

    Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Research. 2016;44:W242-W245.

    Not in our library10.1093/nar/gkw290

  167. 167.

    Letunic I, Bork P. 20 years of the SMART protein domain annotation resource. Nucleic Acids Research. 2018;46:D493-D496.

    Not in our library10.1093/nar/gkx922

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    Levy HC, Walker T. J. Book of Insect Records. 1998;72-73.

    Not in our library

  169. 169.

    Lewis SM, Cratsley CK. Flash signal evolution, mate choice, and predation in fireflies. Annual Review of Entomology. 2008;53:293-321.

    Not in our library10.1146/annurev.ento.53.103106.093346

  170. 170.

    Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754-1760.

    Not in our library10.1093/bioinformatics/btp324

  171. 171.

    Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34:3094-3100.

    Not in our library10.1093/bioinformatics/bty191

  172. 172.

    Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22:1658-1659.

    Not in our library10.1093/bioinformatics/btl158

  173. 173.

    Li X, Ogoh K, Ohba N, Liang X, Ohmiya Y. Mitochondrial genomes of two luminous beetles, Rhagophthalmus lufengensis and R. ohbai (Arthropoda, Insecta, Coleoptera). Gene. 2007;392:196-205.

    Not in our library10.1016/j.gene.2006.12.017

  174. 174.

    Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009;326:289-293.

    Not in our library10.1126/science.1181369

  175. 175.

    Lloyd JE. Studies on the Flash Communication System in Photinus Fireflies. 1966.

    Not in our library

  176. 176.

    Lloyd JE. Firefly parasites and predators. The Coleopterists Bulletin. 1973;27:91-106.

    Not in our library

  177. 177.

    Lloyd J. Where can I find information on raising fireflies? Fireflyer Companion. 1996;I-2:20.

    Not in our library

  178. 178.

    Lloyd JE, Capinera J. L. Encyclopedia of Entomology. 2008;1429-1452.

    Not in our library

  179. 179.

    Lower SS, Johnston JS, Stanger-Hall KF, Hjelmen CE, Hanrahan SJ, Korunes K, Hall D. Genome size in north american fireflies: substantial variation likely driven by neutral processes. Genome Biology and Evolution. 2017;9:1499-1512.

    Not in our library10.1093/gbe/evx097

  180. 180.

    Luk S, Marshall S, Branham M. The fireflies of Ontario (Coleoptera: Lampyridae). Canadian Journal of Arthropod Identification. 2011;16:1-105.

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  181. 181.

    Maddison WP, Maddison DR. 2017.

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  182. 182.

    Maeda J, Kato D-I, Arima K, Ito Y, Toyoda A, Noguchi H. The complete mitochondrial genome sequence and phylogenetic analysis of Luciola lateralis, one of the most famous firefly in Japan (Coleoptera: Lampyridae). Mitochondrial DNA Part B. 2017;2:546-547.

    Not in our library10.1080/23802359.2017.1365640

  183. 183.

    MAKER Tutorial for GMOD Online Training. MAKER tutorial for GMOD online training. 2014.

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  184. 184.

    Mansfield KG. Viral tropism and the pathogenesis of influenza in the mammalian host. The American Journal of Pathology. 2007;171:1089-1092.

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  185. 185.

    Marçais G, Kingsford C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics. 2011;27:764-770.

    Not in our library10.1093/bioinformatics/btr011

  186. 186.

    Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Geer LY, Bryant SH. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Research. 2017;45:D200-D203.

    Not in our library10.1093/nar/gkw1129

  187. 187.

    Marshall SH, Ramírez R, Labra A, Carmona M, Muñoz C. Bona fide evidence for natural vertical transmission of infectious Salmon Anemia virus in freshwater brood stocks of farmed Atlantic Salmon (Salmo salar) in southern chile. Journal of Virology. 2014;88:6012-6018.

    Not in our library10.1128/jvi.03670-13

  188. 188.

    Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal. 2011;17:10-12.

    Not in our library10.14806/ej.17.1.200

  189. 189.

    Martin GJ, Lord NP, Branham MA, Bybee SM. Review of the firefly visual system (Coleoptera: lampyridae) and evolution of the opsin genes underlying color vision. Organisms Diversity & Evolution. 2015;15:513-526.

    Not in our library10.1007/s13127-015-0212-z

  190. 190.

    Martin GJ, Branham MA, Whiting MF, Bybee SM. Total evidence phylogeny and the evolution of adult bioluminescence in fireflies (Coleoptera: Lampyridae). Molecular Phylogenetics and Evolution. 2017;107:564-575.

    Not in our library10.1016/j.ympev.2016.12.017

  191. 191.

    Masuda T, Tatsumi H, Nakano E. Cloning and sequence analysis of cDNA for luciferase of a japanese firefly, Luciola cruciata. Gene. 1989;77:265-270.

    Not in our library10.1016/0378-1119(89)90074-7

  192. 192.

    McKenna DD, Farrell BD. The Timetree of Life. 2009;278:289.

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  193. 193.

    Mckenna DD, Wild AL, Kanda K, Bellamy CL, Beutel RG, Caterino MS, Farnum CW, Hawks DC, Ivie MA, Jameson MLIZ, Leschen RAB, Marvaldi AE, Mchugh JV, Newton AF, Robertson JA, Thayer MK, Whiting MF, Lawrence JF, Ślipiński A, Maddison DR, Farrell BD. The beetle tree of life reveals that coleoptera survived end-Permian mass extinction to diversify during the cretaceous terrestrial revolution. Systematic Entomology. 2015;40:835-880.

    Not in our library10.1111/syen.12132

  194. 194.
  195. 195.

    McLean M, Buck J, Hanson FE. Culture and larval behavior of photurid fireflies. American Midland Naturalist. 1972;87:133-145.

    Not in our library10.2307/2423887

  196. 196.

    Meinwald J, Wiemer DF, Eisner T. Lucibufagins. 2. esters of 12-oxo-2.beta.,5.beta.,11.alpha.-trihydroxybufalin, the Major defensive steroids of the firefly Photinus pyralis (Coleoptera: lampyridae). Journal of the American Chemical Society. 1979;101:3055-3060.

    Not in our library10.1021/ja00505a037

  197. 197.

    Metegnier G, Becking T, Chebbi MA, Giraud I, Moumen B, Schaack S, Cordaux R, Gilbert C. Comparative paleovirological analysis of crustaceans identifies multiple widespread viral groups. Mobile DNA. 2015;6:16.

    Not in our library10.1186/s13100-015-0047-3

  198. 198.
  199. 199.

    Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, Frandsen PB, Ware J, Flouri T, Beutel RG, Niehuis O, Petersen M, Izquierdo-Carrasco F, Wappler T, Rust J, Aberer AJ, Aspöck U, Aspöck H, Bartel D, Blanke A, Berger S, Böhm A, Buckley TR, Calcott B, Chen J, Friedrich F, Fukui M, Fujita M, Greve C, Grobe P, Gu S, Huang Y, Jermiin LS, Kawahara AY, Krogmann L, Kubiak M, Lanfear R, Letsch H, Li Y, Li Z, Li J, Lu H, Machida R, Mashimo Y, Kapli P, McKenna DD, Meng G, Nakagaki Y, Navarrete-Heredia JL, Ott M, Ou Y, Pass G, Podsiadlowski L, Pohl H, von Reumont BM, Schütte K, Sekiya K, Shimizu S, Slipinski A, Stamatakis A, Song W, Su X, Szucsich NU, Tan M, Tan X, Tang M, Tang J, Timelthaler G, Tomizuka S, Trautwein M, Tong X, Uchifune T, Walzl MG, Wiegmann BM, Wilbrandt J, Wipfler B, Wong TK, Wu Q, Wu G, Xie Y, Yang S, Yang Q, Yeates DK, Yoshizawa K, Zhang Q, Zhang R, Zhang W, Zhang Y, Zhao J, Zhou C, Zhou L, Ziesmann T, Zou S, Li Y, Xu X, Zhang Y, Yang H, Wang J, Wang J, Kjer KM, Zhou X. Phylogenomics resolves the timing and pattern of insect evolution. Science. 2014;346:763-767.

    Not in our library10.1126/science.1257570

  200. 200.

    Mjaaland S, Rimstad E, Falk K, Dannevig BH. Genomic characterization of the virus causing infectious salmon anemia in Atlantic salmon (Salmo salar L.): an orthomyxo-like virus in a teleost. Journal of Virology. 1997;71:7681-7686.

    Not in our library10.1128/jvi.71.10.7681-7686.1997

  201. 201.

    Mofford DM, Liebmann KL, Sankaran GS, Reddy G, Reddy GR, Miller SC. Luciferase activity of insect fatty Acyl-CoA synthetases with synthetic luciferins. ACS Chemical Biology. 2017;12:2946-2951.

    Not in our library10.1021/acschembio.7b00813

  202. 202.

    Nathanson JA, Kantham L, Hunnicutt EJ. Isolation and N-terminal amino acid sequence of an octopamine ligand binding protein. FEBS Letters. 1989;259:117-120.

    Not in our library10.1016/0014-5793(89)81508-x

  203. 203.

    Nei M, Kumar S. Molecular Evolution and Phylogenetics. 2000.

    Not in our library

  204. 204.

    Neuberger G, Maurer-Stroh S, Eisenhaber B, Hartig A, Eisenhaber F. Motif refinement of the peroxisomal targeting signal 1 and evaluation of taxon-specific differences. Journal of Molecular Biology. 2003;328:567-579.

    Not in our library10.1016/s0022-2836(03)00318-8

  205. 205.

    Neuberger G, Maurer-Stroh S, Eisenhaber B, Hartig A, Eisenhaber F. 2017.

    Not in our library

  206. 206.

    Newman DJ, Cragg GM. Endophytic and epiphytic microbes as "sources" of bioactive agents. Frontiers in Chemistry. 2015;3:34.

    Not in our library10.3389/fchem.2015.00034

  207. 207.

    Ni JD, Baik LS, Holmes TC, Montell C. A rhodopsin in the brain functions in circadian photoentrainment in Drosophila. Nature. 2017;545:340-344.

    Not in our library10.1038/nature22325

  208. 208.

    Nurk S, Bankevich A, Antipov D, Gurevich A, Korobeynikov A, Lapidus A. Assembling genomes and Mini-metagenomes from highly chimeric reads. Lecture Notes in Computer Science. 2013;158-170.

    Not in our library10.1007/978-3-642-37195-0_13

  209. 209.

    O'Connell J, Schulz-Trieglaff O, Carlson E, Hims MM, Gormley NA, Cox AJ. NxTrim: optimized trimming of illumina mate pair reads. Bioinformatics. 2015;31:2035-2037.

    Not in our library10.1093/bioinformatics/btv057

  210. 210.

    Oba Y, Ojika M, Inouye S. Firefly luciferase is a bifunctional enzyme: atp-dependent monooxygenase and a long chain fatty acyl-CoA synthetase. FEBS Letters. 2003;540:251-254.

    Not in our library10.1016/s0014-5793(03)00272-2

  211. 211.

    Oba Y, Sato M, Ohta Y, Inouye S. Identification of paralogous genes of firefly luciferase in the japanese firefly, Luciola cruciata. Gene. 2006a;368:53-60.

    Not in our library10.1016/j.gene.2005.10.023

  212. 212.

    Oba Y, Sato M, Inouye S. Cloning and characterization of the homologous genes of firefly luciferase in the mealworm beetle, Tenebrio molitor. Insect Molecular Biology. 2006b;15:293-299.

    Not in our library10.1111/j.1365-2583.2006.00646.x

  213. 213.

    Oba Y, Sagegami-Oba R. Phylogeny of Elateridae inferred from molecular analysis. Nat Insects. 2007;42:30-42.

    Not in our library

  214. 214.

    Oba Y, Meyer-Rochow VB. Bioluminescence in Focus. 2009;277-290.

    Not in our library

  215. 215.

    Oba Y, Kumazaki M, Inouye S. Characterization of luciferases and its paralogue in the panamanian luminous click beetle Pyrophorus angustus: a click beetle luciferase lacks the fatty acyl-CoA synthetic activity. Gene. 2010a;452:1-6.

    Not in our library10.1016/j.gene.2009.12.001

  216. 216.

    Oba Y, Mori N, Yoshida M, Inouye S. Identification and characterization of a luciferase isotype in the japanese firefly, Luciola cruciata, involving in the dim glow of firefly eggs. Biochemistry. 2010b;49:10788-10795.

    Not in our library10.1021/bi1016342

  217. 217.

    Oba Y, Yoshida M, Shintani T, Furuhashi M, Inouye S. Firefly luciferase genes from the subfamilies psilocladinae and ototretinae (Lampyridae, Coleoptera). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology. 2012;161:110-116.

    Not in our library10.1016/j.cbpb.2011.10.001

  218. 218.

    Oba Y, Furuhashi M, Bessho M, Sagawa S, Ikeya H, Inouye S. Bioluminescence of a firefly Pupa: involvement of a luciferase isotype in the dim glow of pupae and eggs in the japanese firefly, Luciola lateralis. Photochemical & Photobiological Sciences. 2013a;12:854-863.

    Not in our library10.1039/c3pp25363e

  219. 219.

    Oba Y, Yoshida N, Kanie S, Ojika M, Inouye S. Biosynthesis of firefly luciferin in adult lantern: decarboxylation of L-cysteine is a key step for benzothiazole ring formation in firefly luciferin synthesis. PLoS ONE. 2013b;8:e84023.

    Not in our library10.1371/journal.pone.0084023

  220. 220.

    Oba Y, Hoffmann K. H. Insect Molecular Biology and Ecology. 2014;94-120.

    Not in our library

  221. 221.

    Ohba N. Studies on the communication system of Japanese fireflies. Sci Rept Yokosuka City Mus. 1983;30:1-62.

    Not in our library

  222. 222.

    Ohba N, Hidaka T. Reflex bleeding of fireflies and prey-predator relationship. Sci Rept Yokosuka City Mus. 2002;49:1-12.

    Not in our library

  223. 223.

    Ohba N. Mystery of Fireflies. 2004.

    Not in our library

  224. 224.

    Ohira H. Morphological and Taxonomic Study on the Larvae of Elateridae in Japan (Coleoptera). 1962.

    Not in our library

  225. 225.

    Ohira H. Illustrated key to click beetles of japan. Jpn Soc Environ Entomol Zool. 2013;227-251.

    Not in our library

  226. 226.

    Ohmiya Y, Sumiya M, Viviani VR, Ohba N. Comparative aspects of a luciferase molecule from the Japanese luminous beetle, Rhagophthalmus ohbai. Sci Rep Yokosuka City Mus. 2000;47:31-38.

    Not in our library

  227. 227.

    Okada K, Iio H, Kubota I, Goto T. Firefly bioluminescence III. Conversion of oxyluciferin to luciferin in firefly. Tetrahedron Letters. 1974;15:2771-2774.

    Not in our library10.1016/s0040-4039(01)91738-1

  228. 228.
  229. 229.

    Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC. Terrestrial ecoregions of the world: a new map of life on earth: a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. BioScience. 2001;51:933-938.

    Not in our library10.1641/0006-3568(2001)051[0933:teotwa]2.0.co;2

  230. 230.

    Olson KE, Bonizzoni M. Nonretroviral integrated RNA viruses in arthropod vectors: an occasional event or something more? Current Opinion in Insect Science. 2017;22:45-53.

    Not in our library10.1016/j.cois.2017.05.010

  231. 231.

    OSG Foundation. 2017.

    Not in our library

  232. 232.

    Ow DW, DE Wet JR, Helinski DR, Howell SH, Wood KV, Deluca M. Transient and stable expression of the firefly luciferase gene in plant cells and transgenic plants. Science. 1986;234:856-859.

    Not in our library10.1126/science.234.4778.856

  233. 233.

    Pacific Biosciences. 2017.

    Not in our library

  234. 234.
  235. 235.

    Pankey MS, Minin VN, Imholte GC, Suchard MA, Oakley TH. Predictable transcriptome evolution in the convergent and complex bioluminescent organs of squid. PNAS. 2014;111:E4736-E4742.

    Not in our library10.1073/pnas.1416574111

  236. 236.
  237. 237.

    Perez-Gelabert DE. Arthropods of Hispaniola (Dominican Republic and Haiti): A Checklist and Bibliography. 2008.

    Not in our library

  238. 238.

    Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology. 2015;33:290-295.

    Not in our library10.1038/nbt.3122

  239. 239.

    Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods. 2011;8:785-786.

    Not in our library10.1038/nmeth.1701

  240. 240.

    Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF chimera--a visualization system for exploratory research and analysis. Journal of Computational Chemistry. 2004;25:1605-1612.

    Not in our library10.1002/jcc.20084

  241. 241.

    Pflug A, Lukarska M, Resa-Infante P, Reich S, Cusack S. Structural insights into RNA synthesis by the influenza virus transcription-replication machine. Virus Research. 2017;234:103-117.

    Not in our library10.1016/j.virusres.2017.01.013

  242. 242.

    Picard Tools. 2017.

    Not in our library

  243. 243.

    Pimentel H, Bray NL, Puente S, Melsted P, Pachter L. Differential analysis of RNA-seq incorporating quantification uncertainty. Nature Methods. 2017;14:687-690.

    Not in our library10.1038/nmeth.4324

  244. 244.
  245. 245.

    Poelchau M, Childers C, Moore G, Tsavatapalli V, Evans J, Lee CY, Lin H, Lin JW, Hackett K. The i5k Workspace@NAL--enabling genomic data access, visualization and curation of arthropod genomes. Nucleic Acids Research. 2015;43:D714-D719.

    Not in our library10.1093/nar/gku983

  246. 246.

    Pond SL, Frost SD, Muse SV. HyPhy: hypothesis testing using phylogenies. Bioinformatics. 2005;21:676-679.

    Not in our library10.1093/bioinformatics/bti079

  247. 247.

    Porter ML, Blasic JR, Bok MJ, Cameron EG, Pringle T, Cronin TW, Robinson PR. Shedding new light on opsin evolution. Proceedings of the Royal Society B: Biological Sciences. 2012;279:3-14.

    Not in our library10.1098/rspb.2011.1819

  248. 248.

    Presti RM, Zhao G, Beatty WL, Mihindukulasuriya KA, da Rosa AP, Popov VL, Tesh RB, Virgin HW, Wang D. Quaranfil, Johnston atoll, and lake chad viruses are novel members of the family Orthomyxoviridae. Journal of Virology. 2009;83:11599-11606.

    Not in our library10.1128/jvi.00677-09

  249. 249.

    Price AL, Jones NC, Pevzner PA. De novo identification of repeat families in large genomes. Bioinformatics. 2005;21 Suppl 1:i351-i358.

    Not in our library10.1093/bioinformatics/bti1018

  250. 250.
  251. 251.
  252. 252.

    Pryszcz LP, Gabaldón T. Redundans: an assembly pipeline for highly heterozygous genomes. Nucleic Acids Research. 2016;44:e113.

    Not in our library10.1093/nar/gkw294

  253. 253.

    R Development Core Team. 2013.

    Not in our library

  254. 254.

    Reich S, Guilligay D, Cusack S. An in vitro fluorescence based study of initiation of RNA synthesis by influenza B polymerase. Nucleic Acids Research. 2017;45:3353-3368.

    Not in our library10.1093/nar/gkx043

  255. 255.

    Rewitz KF, O'Connor MB, Gilbert LI. Molecular evolution of the insect halloween family of cytochrome P450s: phylogeny, gene organization and functional conservation. Insect Biochemistry and Molecular Biology. 2007;37:741-753.

    Not in our library10.1016/j.ibmb.2007.02.012

  256. 256.

    Reyes N, Lee V. Behavioral and Morphological Observations of Ignelater Luminosus in Dominica. 2010.

    Not in our library

  257. 257.

    Rice P, Longden I, Bleasby A. EMBOSS: the european molecular biology open software suite. Trends in Genetics. 2000;16:276-277.

    Not in our library10.1016/s0168-9525(00)02024-2

  258. 258.

    Rooney J, Lewis SM. Fitness advantage from nuptial gifts in female fireflies. Ecological Entomology. 2002;27:373-377.

    Not in our library10.1046/j.1365-2311.2002.00420.x

  259. 259.

    Rosa SP. Análise filogenética e revisão taxonômica da tribo pyrophorini candeze, 1863 (Coleoptera, Elateridae, Agrypninae). 2007.

    Not in our library

  260. 260.

    Rosa SP. New species of Ignelater Costa (Coleoptera, Elateridae, Pyrophorini). Pap Avulsos Zool. Museu De Zoologia Da Universidade De São Paulo. 2010;50:445-449.

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  261. 261.

    Sagegami-Oba R, Oba Y, Ohira H. Phylogenetic relationships of click beetles (Coleoptera: Elateridae) inferred from 28S ribosomal DNA: insights into the evolution of bioluminescence in Elateridae. Molecular Phylogenetics and Evolution. 2007;42:410-421.

    Not in our library10.1016/j.ympev.2006.07.017

  262. 262.
  263. 263.

    Sander SE, Hall DW. Variation in opsin genes correlates with signalling ecology in north american fireflies. Molecular Ecology. 2015;24:4679-4696.

    Not in our library10.1111/mec.13346

  264. 264.

    Schnitzler CE, Pang K, Powers ML, Reitzel AM, Ryan JF, Simmons D, Tada T, Park M, Gupta J, Brooks SY, Blakesley RW, Yokoyama S, Haddock SH, Martindale MQ, Baxevanis AD. Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes. BMC Biology. 2012;10:107.

    Not in our library10.1186/1741-7007-10-107

  265. 265.
  266. 266.

    Schultz MD, Schmitz RJ, Ecker JR. 'Leveling' the playing field for analyses of single-base resolution DNA methylomes. Trends in Genetics. 2012;28:583-585.

    Not in our library10.1016/j.tig.2012.10.012

  267. 267.

    Schultz MD, He Y, Whitaker JW, Hariharan M, Mukamel EA, Leung D, Rajagopal N, Nery JR, Urich MA, Chen H, Lin S, Lin Y, Jung I, Schmitt AD, Selvaraj S, Ren B, Sejnowski TJ, Wang W, Ecker JR. Human body epigenome maps reveal noncanonical DNA methylation variation. Nature. 2015;523:212-216.

    Not in our library10.1038/nature14465

  268. 268.

    Sezutsu H, Le Goff G, Feyereisen R. Origins of P450 diversity. Philosophical Transactions of the Royal Society B: Biological Sciences. 2013;368:20120428.

    Not in our library10.1098/rstb.2012.0428

  269. 269.

    Shear WA. The chemical defenses of millipedes (diplopoda): Biochemistry, physiology and ecology. Biochemical Systematics and Ecology. 2015;61:78-117.

    Not in our library10.1016/j.bse.2015.04.033

  270. 270.

    Sheiman IM, Shkutin MF, Terenina NB, Gustafsson MK. A behavioral study of the beetle Tenebrio molitor infected with cysticercoids of the rat tapeworm hymenolepis diminuta. Naturwissenschaften. 2006;93:305-308.

    Not in our library10.1007/s00114-006-0103-4

  271. 271.
  272. 272.

    Shi G, Grimaldi DA, Harlow GE, Wang J, Wang J, Yang M, Lei W, Li Q, Li X. Age constraint on burmese amber based on U–Pb dating of zircons. Cretaceous Research. 2012;37:155-163.

    Not in our library10.1016/j.cretres.2012.03.014

  273. 273.

    Shimomura O. Bioluminescence: Chemical Principles and Methods. 2012.

    Not in our library

  274. 274.

    Sigrist CJ, Cerutti L, Hulo N, Gattiker A, Falquet L, Pagni M, Bairoch A, Bucher P. PROSITE: a documented database using patterns and profiles as motif descriptors. Briefings in Bioinformatics. 2002;3:265-274.

    Not in our library10.1093/bib/3.3.265

  275. 275.

    Sikora D, Rocheleau L, Brown EG, Pelchat M. Influenza A virus cap-snatches host RNAs based on their abundance early after infection. Virology. 2017;509:167-177.

    Not in our library10.1016/j.virol.2017.06.020

  276. 276.

    Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210-3212.

    Not in our library10.1093/bioinformatics/btv351

  277. 277.

    Skinner ME, Uzilov AV, Stein LD, Mungall CJ, Holmes IH. JBrowse: a next-generation genome browser. Genome Research. 2009;19:1630-1638.

    Not in our library10.1101/gr.094607.109

  278. 278.
  279. 279.

    Slipinski SA, Leschen RAB, Lawrence JF, Zhang Z. -Q. Animal Biodiversity: An Outline of Higher-Level Classification and Survey of Taxonomic Richness. 2011;203-208.

    Not in our library

  280. 280.

    Smedley SR, Risteen RG, Tonyai KK, Pitino JC, Hu Y, Ahmed ZB, Christofel BT, Gaber M, Howells NR, Mosey CF, Rahim FU, Deyrup ST. Bufadienolides (lucibufagins) from an ecologically aberrant firefly (Ellychnia corrusca). Chemoecology. 2017;27:141-153.

    Not in our library10.1007/s00049-017-0240-6

  281. 281.

    Smit A, Hubley R, Green P. RepeatMasker. 2015.

    Not in our library

  282. 282.

    Smit A, Hubley R. RepeatModeler. 2017.

    Not in our library

  283. 283.

    Smith MD, Wertheim JO, Weaver S, Murrell B, Scheffler K, Kosakovsky Pond SL. Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection. Molecular Biology and Evolution. 2015;32:1342-1353.

    Not in our library10.1093/molbev/msv022

  284. 284.

    Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688-2690.

    Not in our library10.1093/bioinformatics/btl446

  285. 285.

    Stanger-Hall KF, Lloyd JE. Flash signal evolution in Photinus fireflies: character displacement and signal exploitation in a visual communication system. Evolution. 2015;69:666-682.

    Not in our library10.1111/evo.12606

  286. 286.
  287. 287.

    Steel J, Lowen AC. Influenza A virus reassortment. Current Topics in Microbiology and Immunology. 2014;385:377-401.

    Not in our library10.1007/82_2014_395

  288. 288.

    Stibick JNL. Classification of the Elateridae (Coleoptera). Relationships and Classification of the Subfamilies and Tribes. Pacific Insects. 1979;20:145-186.

    Not in our library

  289. 289.

    Stolz U, Velez S, Wood KV, Wood M, Feder JL. Darwinian natural selection for orange bioluminescent color in a jamaican click beetle. PNAS. 2003;100:14955-14959.

    Not in our library10.1073/pnas.2432563100

  290. 290.

    Suzuki MM, Kerr AR, De Sousa D, Bird A. CpG methylation is targeted to transcription units in an invertebrate genome. Genome Research. 2007;17:625-631.

    Not in our library10.1101/gr.6163007

  291. 291.

    Tanabe AS. Kakusan4 and aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Molecular Ecology Resources. 2011;11:914-921.

    Not in our library10.1111/j.1755-0998.2011.03021.x

  292. 292.
  293. 293.

    Tatsumi H, Kajiyama N, Nakano E. Molecular cloning and expression in Escherichia coli of a cDNA clone encoding luciferase of a firefly, Luciola lateralis. Biochimica Et Biophysica Acta (BBA) - Gene Structure and Expression. 1992;1131:161-165.

    Not in our library10.1016/0167-4781(92)90071-7

  294. 294.

    Te Velthuis AJ, Fodor E. Influenza virus RNA polymerase: insights into the mechanisms of viral RNA synthesis. Nature Reviews Microbiology. 2016;14:479-493.

    Not in our library10.1038/nrmicro.2016.87

  295. 295.

    Temin HM. Reverse transcription in the eukaryotic genome: retroviruses, pararetroviruses, retrotransposons, and retrotranscripts. Molecular Biology and Evolution. 1985;2:455-468.

    Not in our library10.1093/oxfordjournals.molbev.a040365

  296. 296.

    Thompson WW, Weintraub E, Dhankhar P, Cheng PY, Brammer L, Meltzer MI, Bresee JS, Shay DK. Estimates of US influenza-associated deaths made using four different methods. Influenza and Other Respiratory Viruses. 2009;3:37-49.

    Not in our library10.1111/j.1750-2659.2009.00073.x

  297. 297.

    Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Briefings in Bioinformatics. 2013;14:178-192.

    Not in our library10.1093/bib/bbs017

  298. 298.

    Timmermans MJ, Dodsworth S, Culverwell CL, Bocak L, Ahrens D, Littlewood DT, Pons J, Vogler AP. Why barcode? High-throughput multiplex sequencing of mitochondrial genomes for molecular systematics. Nucleic Acids Research. 2010;38:e197.

    Not in our library10.1093/nar/gkq807

  299. 299.

    Timmermans MJ, Vogler AP. Phylogenetically informative rearrangements in mitochondrial genomes of Coleoptera, and monophyly of aquatic elateriform beetles (Dryopoidea). Molecular Phylogenetics and Evolution. 2012;63:299-304.

    Not in our library10.1016/j.ympev.2011.12.021

  300. 300.

    Tong D, Rozas NS, Oakley TH, Mitchell J, Colley NJ, McFall-Ngai MJ. Evidence for light perception in a bioluminescent organ. PNAS. 2009;106:9836-9841.

    Not in our library10.1073/pnas.0904571106

  301. 301.

    Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology. 2010;28:511-515.

    Not in our library10.1038/nbt.1621

  302. 302.

    Tribolium Genome Sequencing Consortium, Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, Beeman RW, Gibbs R, Beeman RW, Brown SJ, Bucher G, Friedrich M, Grimmelikhuijzen CJ, Klingler M, Lorenzen M, Richards S, Roth S, Schröder R, Tautz D, Zdobnov EM, Muzny D, Gibbs RA, Weinstock GM, Attaway T, Bell S, Buhay CJ, Chandrabose MN, Chavez D, Clerk-Blankenburg KP, Cree A, Dao M, Davis C, Chacko J, Dinh H, Dugan-Rocha S, Fowler G, Garner TT, Garnes J, Gnirke A, Hawes A, Hernandez J, Hines S, Holder M, Hume J, Jhangiani SN, Joshi V, Khan ZM, Jackson L, Kovar C, Kowis A, Lee S, Lewis LR, Margolis J, Morgan M, Nazareth LV, Nguyen N, Okwuonu G, Parker D, Richards S, Ruiz SJ, Santibanez J, Savard J, Scherer SE, Schneider B, Sodergren E, Tautz D, Vattahil S, Villasana D, White CS, Wright R, Park Y, Beeman RW, Lord J, Oppert B, Lorenzen M, Brown S, Wang L, Savard J, Tautz D, Richards S, Weinstock G, Gibbs RA, Liu Y, Worley K, Weinstock G, Elsik CG, Reese JT, Elhaik E, Landan G, Graur D, Arensburger P, Atkinson P, Beeman RW, Beidler J, Brown SJ, Demuth JP, Drury DW, Du YZ, Fujiwara H, Lorenzen M, Maselli V, Osanai M, Park Y, Robertson HM, Tu Z, Wang JJ, Wang S, Richards S, Song H, Zhang L, Sodergren E, Werner D, Stanke M, Morgenstern B, Solovyev V, Kosarev P, Brown G, Chen HC, Ermolaeva O, Hlavina W, Kapustin Y, Kiryutin B, Kitts P, Maglott D, Pruitt K, Sapojnikov V, Souvorov A, Mackey AJ, Waterhouse RM, Wyder S, Zdobnov EM, Zdobnov EM, Wyder S, Kriventseva EV, Kadowaki T, Bork P, Aranda M, Bao R, Beermann A, Berns N, Bolognesi R, Bonneton F, Bopp D, Brown SJ, Bucher G, Butts T, Chaumot A, Denell RE, Ferrier DE, Friedrich M, Gordon CM, Jindra M, Klingler M, Lan Q, Lattorff HM, Laudet V, von Levetsow C, Liu Z, Lutz R, Lynch JA, da Fonseca RN, Posnien N, Reuter R, Roth S, Savard J, Schinko JB, Schmitt C, Schoppmeier M, Schröder R, Shippy TD, Simonnet F, Marques-Souza H, Tautz D, Tomoyasu Y, Trauner J, Van der Zee M, Vervoort M, Wittkopp N, Wimmer EA, Yang X, Jones AK, Sattelle DB, Ebert PR, Nelson D, Scott JG, Beeman RW, Muthukrishnan S, Kramer KJ, Arakane Y, Beeman RW, Zhu Q, Hogenkamp D, Dixit R, Oppert B, Jiang H, Zou Z, Marshall J, Elpidina E, Vinokurov K, Oppert C, Zou Z, Evans J, Lu Z, Zhao P, Sumathipala N, Altincicek B, Vilcinskas A, Williams M, Hultmark D, Hetru C, Jiang H, Grimmelikhuijzen CJ, Hauser F, Cazzamali G, Williamson M, Park Y, Li B, Tanaka Y, Predel R, Neupert S, Schachtner J, Verleyen P, Raible F, Bork P, Friedrich M, Walden KK, Robertson HM, Angeli S, Forêt S, Bucher G, Schuetz S, Maleszka R, Wimmer EA, Beeman RW, Lorenzen M, Tomoyasu Y, Miller SC, Grossmann D, Bucher G. The genome of the model beetle and pest tribolium castaneum. Nature. 2008;452:949-955.

    Not in our library10.1038/nature06784

  303. 303.

    Tyler J, Mckinnon W, Lord GA, Hilton PJ. A defensive steroidal pyrone in the Glow-worm Lampyris noctiluca L. (Coleoptera: Lampyridae). Physiological Entomology. 2008;33:167-170.

    Not in our library10.1111/j.1365-3032.2007.00610.x

  304. 304.

    United States Census Bureau. Cartographic boundary shapefiles - Counties. 2017.

    Not in our library

  305. 305.

    Urich MA, Nery JR, Lister R, Schmitz RJ, Ecker JR. MethylC-seq library preparation for base-resolution whole-genome bisulfite sequencing. Nature Protocols. 2015;10:475-483.

    Not in our library10.1038/nprot.2014.114

  306. 306.

    van der Reijden ED, Monchamp JD, Lewis SM. The formation, transfer, and fate of spermatophores in Photinus fireflies (Coleoptera: Lampyridae). Canadian Journal of Zoology. 1997;75:1202-1207.

    Not in our library10.1139/z97-143

  307. 307.

    Vélez S, Feder J. L. Biogeographic and Genetic Approaches to the Natural History of the Bioluminescent Jamaican Click Beetle, Pyrophorus Plagiophthalamus (Coleoptera: Elateridae). 2006.

    Not in our library10.1111/j.1365-294x.2005.02793.x

  308. 308.

    Velez S, Feder JL. Integrating biogeographic and genetic approaches to investigate the history of bioluminescent colour alleles in the Jamaican click beetle, Pyrophorus plagiophthalamus. Molecular Ecology. 2006;15:1393-1404.

    Not in our library10.1111/j.1365-294x.2005.02793.x

  309. 309.

    Virkki N, Flores M, Escudero J. Structure, orientation, and segregation of the sex trivalent in Pyrophorus luminosus III. (Coleoptera, Elateridae). Canadian Journal of Genetics and Cytology. 1984;26:326-330.

    Not in our library10.1139/g84-050

  310. 310.

    Viviani VR, Bechara EJ, Ohmiya Y. Cloning, sequence analysis, and expression of active Phrixothrix railroad-worms luciferases: relationship between bioluminescence spectra and primary structures. Biochemistry. 1999a;38:8271-8279.

    Not in our library10.1021/bi9900830

  311. 311.

    Viviani VR, Silva AC, Perez GL, Santelli RV, Bechara EJ, Reinach FC. Cloning and molecular characterization of the cDNA for the brazilian larval click-beetle Pyrearinus termitilluminans luciferase. Photochemistry and Photobiology. 1999b;70:254-260.

    Not in our library10.1111/j.1751-1097.1999.tb07997.x

  312. 312.

    Viviani VR, Amaral D, Prado R, Arnoldi FG. A new blue-shifted luciferase from the brazilian Amydetes fanestratus (Coleoptera: Lampyridae) firefly: molecular evolution and structural/functional properties. Photochem. Photobiol. Sci. 2011;10:1879-1886.

    Not in our library10.1039/c1pp05210a

  313. 313.

    Vurture GW, Sedlazeck FJ, Nattestad M, Underwood CJ, Fang H, Gurtowski J, Schatz MC. GenomeScope: fast reference-free genome profiling from short reads. Bioinformatics. 2017;33:2202-2204.

    Not in our library10.1093/bioinformatics/btx153

  314. 314.
  315. 315.
  316. 316.

    Wasserman M, Ehrman L. Firefly chromosomes, II. (Lampyridae: Coleoptera). The Florida Entomologist. 1986;69:755-757.

    Not in our library10.2307/3495223

  317. 317.
  318. 318.

    Weng JK. The evolutionary paths towards complexity: a metabolic perspective. New Phytologist. 2014;201:1141-1149.

    Not in our library10.1111/nph.12416

  319. 319.

    Wheeler DL, Church DM, Federhen S, Lash AE, Madden TL, Pontius JU, Schuler GD, Schriml LM, Sequeira E, Tatusova TA, Wagner L. Database resources of the national center for biotechnology. Nucleic Acids Research. 2003;31:28-33.

    Not in our library10.1093/nar/gkg033

  320. 320.
  321. 321.

    Wick R. GitHub. 2018.

    Not in our library

  322. 322.

    Williams FX. Notes on the life-history of some North American Lampyridae. Journal of the New York Entomological Society. 1917;25:11-33.

    Not in our library

  323. 323.

    Williamson DL, Tully JG, Rose DL, Hackett KJ, Henegar R, Carle P, Bové JM, Colflesh DE, Whitcomb RF. Mycoplasma somnilux sp. nov., Mycoplasma luminosum sp. nov., and Mycoplasma lucivorax sp. nov., new sterol-requiring mollicutes from firefly beetles (Coleoptera: Lampyridae). International Journal of Systematic Bacteriology. 1990;40:160-164.

    Not in our library10.1099/00207713-40-2-160

  324. 324.

    Willingham AT, Keil T. A tissue specific cytochrome P450 required for the structure and function of Drosophila sensory organs. Mechanisms of Development. 2004;121:1289-1297.

    Not in our library10.1016/j.mod.2004.04.017

  325. 325.

    Wolcott GN. The insects of Puerto Rico: Coleoptera. The Journal of Agriculture of the University of Puerto Rico. 1948;32:225-416.

    Not in our library

  326. 326.

    Wolcott GN. The rise and fall of the white grub in puerto rico. The American Naturalist. 1950;84:183-193.

    Not in our library10.1086/281621

  327. 327.

    Wood KV, de Wet JR, Dewji N, DeLuca M. Synthesis of active firefly luciferase by in vitro translation of RNA obtained from adult lanterns. Biochemical and Biophysical Research Communications. 1984;124:592-596.

    Not in our library10.1016/0006-291x(84)91595-x

  328. 328.

    Wood KV, Lam YA, Seliger HH, McElroy WD. Complementary DNA coding click beetle luciferases can elicit bioluminescence of different colors. Science. 1989;244:700-702.

    Not in our library10.1126/science.2655091

  329. 329.
  330. 330.

    World Wildlife Fund. Terrestrial ecoregions of the world. 2017.

    Not in our library

  331. 331.

    Wu TD, Watanabe CK. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics. 2005;21:1859-1875.

    Not in our library10.1093/bioinformatics/bti310

  332. 332.

    Wulan WN, Heydet D, Walker EJ, Gahan ME, Ghildyal R. Nucleocytoplasmic transport of nucleocapsid proteins of enveloped RNA viruses. Frontiers in Microbiology. 2015;6:553.

    Not in our library10.3389/fmicb.2015.00553

  333. 333.

    Xiang H, Zhu J, Chen Q, Dai F, Li X, Li M, Zhang H, Zhang G, Li D, Dong Y, Zhao L, Lin Y, Cheng D, Yu J, Sun J, Zhou X, Ma K, He Y, Zhao Y, Guo S, Ye M, Guo G, Li Y, Li R, Zhang X, Ma L, Kristiansen K, Guo Q, Jiang J, Beck S, Xia Q, Wang W, Wang J. Single base-resolution methylome of the silkworm reveals a sparse epigenomic map. Nature Biotechnology. 2010;28:516-520.

    Not in our library10.1038/nbt.1626

  334. 334.

    Ye L, Buck LM, Schaeffer HJ, Leach FR. Cloning and sequencing of a cDNA for firefly luciferase from Photuris pennsylvanica. Biochimica Et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology. 1997;1339:39-52.

    Not in our library10.1016/s0167-4838(96)00211-7

  335. 335.
  336. 336.

    Zeng H, Goldsmith CS, Maines TR, Belser JA, Gustin KM, Pekosz A, Zaki SR, Katz JM, Tumpey TM. Tropism and infectivity of influenza virus, including highly pathogenic avian H5N1 virus, in ferret tracheal differentiated primary epithelial cell cultures. Journal of Virology. 2013;87:2597-2607.

    Not in our library10.1128/jvi.02885-12

  337. 337.

    Zimin AV, Marçais G, Puiu D, Roberts M, Salzberg SL, Yorke JA. The MaSuRCA genome assembler. Bioinformatics. 2013;29:2669-2677.

    Not in our library10.1093/bioinformatics/btt476

  338. 338.

    Zimin AV, Puiu D, Luo MC, Zhu T, Koren S, Marçais G, Yorke JA, Dvořák J, Salzberg SL. Hybrid assembly of the large and highly repetitive genome of Aegilops tauschii, a progenitor of bread wheat, with the MaSuRCA mega-reads algorithm. Genome Research. 2017;27:787-792.

    Not in our library10.1101/gr.213405.116

  339. 339.

    Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research. 2003;31:3406-3415.

    Not in our library10.1093/nar/gkg595

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