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Although the sticky capture threads, and associated well-developed aggregate and flagelliform triad, are characteristic of the Araneoidea, the use of the sticky capture threads is frequently lost, and with it the aggregate and flagelliform triad. In most araneoids, adult males adopt a vagrant lifestyle and the triplet is lost [ 28 ] or vestigial [ 29 , 30 ] in the final instar. Thus, it appears that convergent trait regression, with repeated loss of the sticky spiral triad of spinneret spigots, is tied to the adoption of a cursorial lifestyle.
However, it is not clear whether these convergent phenotypic changes are reflected at the molecular level, and hence the relationship between genotype and phenotype remains unknown. In particular, given that the trait is convergent, are the morphological and behavioral similarities the result of similar changes at the molecular level, and are the selective pressures also acting in a similar way?
However, partial loss of the triad has been documented in multiple lineages within the Tetragnathidae. This lineage appears to be monophyletic, with early divergence, ca. The parallel radiation of these two lineages provides an ideal opportunity to compare selective pressures acting on each clade. Finally, we ask 4 whether natural selection has acted convergently in Spiny Leg Tetragnatha and in the clades Mimetidae, Malkaridae, and Arkyidae, where web loss has occurred independently.
We sequenced six new transcriptomes and conducted a transcriptomic analysis between web building and non-web building members of the genus Tetragnatha , then tested for evidence of selection associated with web loss and the associated adoption of a cursorial lifestyle across the Tetragnatha phylogeny. We also tested for convergent selection using available transcriptomes from Mimetidae, Malkaridae, and Arkyidae.
The most remarkable feature of the posterior lateral spinnerets is the very obvious presence of the aggregate and flagelliform spigots in all seven species of web-spinners Fig. However, the four species in the Spiny Leg clade all demonstrate a complete absence of the aggregate and flagelliform spigots.
Dissections were perfomed on three web-building T. Flagelliform glands are much smaller and more difficult to identify [ 24 ]. For this reason, we are not able to say with confidence that flagelliform glands are definitively absent from Spiny Leg spiders; however, aggregate glands have clearly been lost. Scanning Electron Microscopy Images of the posterior lateral spinnerets. Web builders 7 shown on the left: a Tetragnatha acuta , b T. Spiny Leg clade 6 on the right: h T. Yellow arrows: tubuliform spigots; blue arrows: flagelliform spigots; green arrows: aggregate spigots.
Unlabelled spigots are aciniform. Representative photographs of dissected abdomens showing silk glands. Aggregate glands red are large, multilobed, whitish structures that are only visible in web-building species, shown on the left. Major ampullate glands green are whitish but smaller, and have a distinctive duct shape that is easy to recognize. For simplicity, other glands are not labelled or are too small to see. Yellowish lumps are adipose tissue.
Left: Web builder, T. Right: Spiny leg, T. We have assembled the first protein-coding transcriptomes of six species of Hawaiian Tetragnatha spiders. We generated twelve RNA-seq libraries from the dissected abdomens of adult female spiders two individuals per species ; library and assembly statistics are given in Additional file 1. Sequencing depth ranged between Quality filtering removed an average of 6.
After trimming, libraries contained between 19 and 33 million paired-end reads per individual, or between 43 and 62 million reads per species, with fragment lengths between 50 and bp. De novo assemblies made with Trinity contained between , and , transcripts with a minimum contig length of bp. The six assemblies recovered between Full-length spidroins are difficult to assemble due to their unique structure, so we limited our analysis to N- and C-terminal domain sequences.
We searched the predicted peptides for spidroin terminal domains using BLAST and constructed Bayesian consensus trees for both sets of termini Fig. Phylogenetic conflict can occur between spidroin N- and C-termini, and N-termini generally contain more phylogenetic signal [ 21 , 39 ]. Note that with our data, we have no way of knowing which N- and C-terminal sequences belong to the same physical gene. None of the three Spiny Leg transcriptomes contained sequences belonging to the flagelliform or Sp clades.
Hawaiian Tetragnatha appear to possess three aggregate spidroin genes, two of which are expressed in some Spiny Leg species Additional file 2. Bayesian consensus trees of terminal domains. Branches leading to species sequenced in this study are colored red, and Spiny Leg species are labelled with blue text.
Aggregate spidroins are numbered according to the the numbering system of [ 73 ]. Letters are used to distinguish multiple copies of spidroins in Tetragnatha e. MaSp-a, MaSp-b. Where abbreviated, genus names are: A. Trees produced using Mr. Bayes v3. OrthoFinder assigned predicted proteins to 19, orthogroups, and PhyloTreePruner identified single-copy orthologs with genes in all six taxa, which were used for differential expression analysis between web builders and Spiny Legs.
We identified 1. DE genes and their annotations are given in Additional file 3. Many of the remaining DE genes both up- and downregulated belong to groups of genes previously identified as having silk gland-specific expression in [ 18 , 38 , 40 ] , including proteases, transferases, and genes associated with cellular transport and secretion; the expression of some of these genes is shown in Fig.
Genes with higher expression in Spiny Legs include protease inhibitors such as zonadhesins, as well as transferases and transporter proteins. We observed reduced expression in Spiny Legs of some genes with aggregate gland-specific expression in other spiders, including an N-acetylgalactosaminyltransferase pp-GalNAc-T [ 41 ] and a globin protein [ 40 ].
Other genes with lower expression in Spiny Legs include an aminotransferase, a semaphorin membrane protein, and a cathepsin endopeptidase. Genes with higher expression in web builders were not enriched for any GO categories. Relative expression of select genes. Counts have been normalized to average transcript size and library size, and are expressed as transcripts per million TPM on a log scale.
The first approach using the FUSTr [ 42 ] pipeline identified eight gene families corresponding to spidroins: of these, two contained sites showing evidence for pervasive positive selection, an aggregate spidroin and a major ampullate spidroin Table 1. Neither family included sequences from Hawaiian Tetragnatha. Five of the remaining six spidroins included sequences from non-web building taxa and were further analyzed for selection along branches leading to those taxa.
Three genes showed evidence for relaxed selection: an aggregate spidroin exhibited relaxed selection in the Spiny Leg T. Finally, another aggregate sequence showed evidence for episodic positive selection in the Spiny Leg T. These included ribosomal proteins and genes involved in protein ubiquitination and vesicle transport.
For 24 genes, the best model involved selection in all non-web building taxa; these genes included mitochondrial enzymes, ATPases, proteasome components, and additional genes related to protein synthesis and ubiquitination Table 2. None of these 34 genes overlapped with the set of genes that were differentially expressed between Spiny Legs and web builders. Red: Tetragnatha genus.
Green and Blue: Hawaiian Tetragnatha lineage. Blue: Spiny Leg lineage. Branch support values indicate local posterior probabilities. The current study examined secondary loss of web building behavior within a radiation of Hawaiian spiders to determine the associations between behavior, morphology, and gene expression, specifically asking at which level selection appears to operate, and whether there is compensatory selection on other silks in association with the adoption of a cursorial lifestyle.
These behavioral and morphological changes are accompanied by shifts in gene expression and branch-specific selection. Intriguingly, we identify an important role for a novel spidroin in web loss, as this gene shows higher expression and shifts in selection in non-web builders.
We also detect evidence for convergent evolution between Spiny Leg Tetragnatha and other non-web building lineages, not only in morphology loss of aggregate and flagelliform spigots , but at the genomic level, with selection acting on some of the same genes across independent web loss events.
The web building Hawaiian Tetragnatha examined in this study clearly show a well-developed triad of the aggregate and flagelliform spigots. However, these structures appear to be completely absent in the Spiny Leg taxa examined Fig. The absence of these spigots parallels similar losses that have been documented for the Mimetidae, Malkaridae, and Arkyidae s. Similar shifts in morphology have been observed in other spider lineages in which the building of orb webs has been modified or lost.
Notably, in Cyrtophora Araneidae , loss of the triad has been associated with the loss of sticky silk in the production of the mesh of dry silk [ 32 ]; in the species Drapetisca socialis and Neriene peltata Linyphiidae , a similar loss is associated with the ability to catch prey outside the web without using glue in the web [ 33 ]; and in the subfamily Argyrodinae Theridiidae , loss of the triad spigots is linked to abandonment of web building behavior and the adoption of kleptoparasitic or free-living existence [ 34 ].
Reduction in the triad is also known in the families Synaphridae [ 29 ] and Micropholcommatidae [ 44 ], though the predatory behavior in these lineages is not known. Among the Tetragnathidae, the genus Pachygnatha has largely lost the behavior of web building for prey capture and adults have lost the triad [ 26 ], although juvenile Pachygnatha still spin an orb web [ 45 ]. Apart from the Spiny Leg species examined in this study, the loss of the triad has also been documented in other Hawaiian tetragnathids.
The monospecific Doryonychus raptor , which captures its prey without a foraging web, shows no evidence of the triad even during the earliest developmental stages [ 31 ]; prey are captured, either in flight or from the substrate, by impalement with the claws, which occurs through a very rapid movement of one or more of the first two pairs of legs [ 46 ]. The transcriptomes of web-building Tetragnatha contain every major type of spidroin that has been described for the superfamily Araneoidea, while the Spiny Leg transcriptomes contain all major spidroins except for flagelliform Fig.
We caution that absence of evidence is not evidence of absence. However, given the high completeness of our assemblies, the fact that flagelliform transcripts are absent from six separate Spiny Leg transcriptomes, and the absence of flagelliform spigots, we view it as likely that flagelliform spidroins are not expressed at appreciable levels.
It remains to be seen whether flagelliform spidroins are present in Spiny Leg genomes, or have become pseudogenes due to loss of function and a release from selective restraints. In contrast, one species sequenced in this study T. It is surprising that aggregate spidroins are expressed in species that cannot make aggregate silk. Spidroins are sometimes co-expressed in more than one silk gland [ 23 , 48 ], and this could suggest that aggregate spidroins play a role in the production of other types of silk.
Alternatively, it is likely that, because silk glands are derived from each other by serial homology, the ongoing transcription of aggregate spidroins is a remnant of past homology. This latter hypothesis is supported by the observation that aggregate transcripts in the Spiny Legs T. Other studies have reported a similar phenomenon in male theridiid spiders, where loss of aggregate glands occurs upon reaching maturity, yet aggregate spidroins continue to be expressed [ 19 ].
Our selection analyses show that one aggregate spidroin appears to have experienced episodic diversifying selection in the Spiny Leg T. On the other hand, another aggregate spidroin has experienced relaxed selection in the Spiny Leg T. Spidroins generally fall into one of seven monophyletic groups corresponding to the seven silk glands [ 14 ].
However, the recent genome of the golden orb-weaver Trichonephila clavipes revealed several novel spidroins that do not fall into these well-established clades [ 14 ]. Our Tetragnatha transcriptomes contain homologs of some of these uncharacterized spidroins. Sp is primarily expressed in the flagelliform gland in T. Another uncharacterized spidroin, Sp, shows evidence of relaxed selection in the entire Hawaiian Tetragnatha lineage Table 1.
A third spidroin, which forms a clade with T. Although spidroins make up the silk fibers themselves, many other genes play roles in silk production and have silk gland-specific expression. Previous studies have found that both peptidases and peptidase inhibitors are enriched among silk gland-specific genes. Clarke et al. Our results are consistent with this model, as both peptidases e. Interestingly, zonadhesins have been detected in the silk of the greater wax moth, which is not homologous to spider silk [ 50 ].
Silk gland-specific transcripts also include genes related to oxygen metabolism, at least in black widow spiders [ 18 , 51 ]. In the current study, we observe the downregulation of an amine oxidase and a monooxygenase in Spiny Legs, but the upregulation of a glutaredoxin and a dual oxidase. We also observed that Spiny Legs downregulate two genes that are highly expressed in the major ampullate glands of black widow spiders, a phosphoserine aminotransferase and a gamma-glutamyltransferase, the latter potentially involved in redox regulation in silk glands [ 48 ].
Genes with higher expression in Spiny Legs are enriched for functions related to chitin binding. While chitin serves primarily as a major structural component of arthropod bodies, forming the cuticle or exoskeleton, it is also found within the walls and ducts of silk glands, such as the major ampullate silk glands of Trichonephila clavipes and even the non-homologous silk glands of the silkworm [ 52 ].
Some spidroins also possess chitin-binding domains [ 53 ]. The close relationship between chitin and silk suggests that the changes in gene expression observed here may reflect morphological changes accompanying the loss of internal silk glands and external spigots. It is unclear why Spiny Legs have increased expression of chitin-binding genes. However, the loss of aggregate and flagelliform silk could be accompanied by increased expression of other types of silk such as dragline [ 19 ], leading to higher expression of some silk-related genes.
Consistent with the loss of aggregate glands, Spiny Legs exhibited reduced expression of genes with aggregate gland-specific expression in other spiders, including a pp-GalNAc-T, a type of transferase that participates in O-glycosylation [ 54 ]. O-glycosylation contributes to the adhesive qualities of aggregate glue [ 55 ], and pp-GalNAc-T is highly expressed in the aggregate glands of the orb-weaver Argiope trifasciata [ 41 ].
The reduced expression of this gene in Spiny Legs accompanied by their loss of aggregate glands suggests that this gene could play a similar role in aggregate silk production in tetragnathids. Spiny Legs also have reduced expression of a globin protein, a type of protein specifically expressed in the aggregate glands of Trichonephila clavipes [ 40 ]. However, further work is needed to understand gland-specific patterns of gene expression in Tetragnatha. Branch tests of single-copy orthologs identified targets of selection along branches where independent web loss events have occurred in Tetragnatha and related lineages species shown in Fig.
Many of the same genes, including ubiquitin ligases and proteasome components, appear to be targets of selection in both Spiny Legs and other non-web building families Table 2. Other genes in this category include pim-3, a kinase that regulates protein synthesis [ 56 ], and BYSL, which mediates ribosome biogenesis [ 57 ]. This suggests that the loss of web silk is accompanied by convergent selection on protein synthesis, processing, and degradation machinery in both Spiny Leg Tetragnatha and other non-web building araneoid spiders.
Since silk is a proteinaceous material, changes in the silk needs of a species may require changes in genes regulating protein metabolism. There is an interesting parallel in silkworms, where QTL analysis identified polymorphism in a ribosomal subunit associated with silk synthesis [ 58 ]. Another interesting category of genes with convergent selection is related to energy metabolism, including both ATP synthase and ATPases.
There may be an association between large-scale changes in silk production and changes in cellular metabolism. Other genes, including ribosomal components and genes related to vesicle transport, are targets of selection only in Spiny Leg Tetragnatha , suggesting that lineage-specific differences are also important. Still, it is notable that even in cases when selection has not acted on the same gene, it acts on genes with functions related to protein metabolism.
Relaxed selection can be caused not only by loss of function, but also by a change in functional constraints upon adaptation to a new ecological niche, or a reduction in effective population size [ 59 ].
Correa-Garwhal et al. It is important to note that the genes identified in this study are not exhaustive. Our gene expression analysis is limited by small sample sizes, meaning that we only have power to detect the largest changes in expression. Moreover, RNA-seq data can inflate expression estimates of spidroins when reads derived from repetitive regions map to fragments containing portions of the repetitive region [ 60 ].
Our selection analyses are constrained by the relative incompleteness of some transcriptomes, which limits the number of single-copy orthologs that we can recover. The transcriptomes sequenced in this study are quite complete, but other assemblies were generated with different goals where completeness was less important [ 47 , 61 ]. This type of analysis also neglects the roles of gene loss and duplication in character evolution.
Finally, transcriptomic data are rarely able to reconstruct full-length spidroins, which means that we cannot match N- and C-terminal sequences. The sequences in our phylogenetic and selection analyses correspond to internal, N-, or C-terminal fragments of full-length spidroins, which may have experienced different selection regimes.
Nonetheless, our complementary analyses provide a clearer picture of the types of genes involved in web loss and of the distribution of spidroins in non-web building Tetragnatha. In particular, protein synthesis and degradation machinery appear to be convergent targets of selection when capture webs are lost. The loss of web building behavior has occurred independently at many different levels: within the genus Tetragnatha , between genera within the Tetragnathidae, and between the related families shown in this study.
This system therefore provides an interesting opportunity to compare genomic shifts across phylogenetic scales. The American T. Future work comparing the genomic basis for these suites of convergent traits will provide insights into the interplay between genotype and phenotype that allows these characters to evolve together.
Phenotypic convergence has been broadly defined as the independent evolution of similar phenotypes. There are numerous examples of convergence, though only a small fraction of studies have examined whether convergent events are based on shared genetic mechanisms [ 12 ]. Our study is the first to systematically characterize silk genes in Spiny Leg Tetragnatha , and determine associations with convergent adaptation of a cursorial lifestyle.
Web loss is associated with a series of morphological, ecological, and behavioral traits, and we show that web loss is accompanied by shifts in the expression of silk-associated genes within Tetragnatha. Our results further show that selection has acted on many of the same protein-coding genes in independent lineages that have lost webs and shifted to a cursorial lifestyle.
Scanning electron microscopy was conducted on the spinnerets of single individual females of seven web spinners: Tetragnatha acuta , T. These are shown in Fig. Specimens were imaged either in or , following slightly different protocols. In the early study , live spiders were boiled in water for 40 s in order to cause the spinneret spigots to evert. The spinnerets were then cut from the body and placed in plastic capsules with the central portion removed and nylon mesh placed inside the capsule to allow exchange of alcohol and CO 2 , while retaining the specimen.
The structures were then removed from the capsules, mounted on stubs and sputtered with gold, and then viewed using a Hitachi S in or a Philips XL ESEM in scanning electron microscope. We sequenced total RNA from two individuals of each species, for a total of twelve sequence libraries. All individuals were females and sexually mature at the time of extraction.
The spiders were kept in the lab in Berkeley, California until they were extracted in November and December of that year. Animals were maintained under a common temperature, humidity, and light regime and fed at the same time each day.
Extractions were performed on two days, at the same time each day. Live spiders were anesthetized with carbon dioxide and their abdomens were severed at the narrowest point of connection with the cephalothorax. Silk glands were dissected out as one mass in the presence of SSC buffer and preserved in RNAlater procedure adapted from [ 65 ]. Due to the small size of the abdomens approximately 5 mm in length , not all skin and abdominal tissue was excised.
RNA concentration and quality were verified for each sample using a Qubit fluorometer and a NanoDrop spectrophotometer. We also included a set of Tetragnatha spiders that were collected from different areas in Japan. For collecting information and accession numbers, see Additional file 5. RNA was fragmented to the desired size approx. The adapter-ligated libraries were amplified with 10 PCR cycles. Finally, library concentration and fragment size were assessed with a Bioanalyzer and Qubit fluorometer.
Sequencing for Japanese Tetragnatha unpublished data was performed as described previously in [ 66 ]. Quality filtering was conducted with Trimmomatic v0. The six species transcriptomes were each assembled using Trinity v2. To evaluate assembly quality, we mapped trimmed reads back to their assembly using Bowtie v2. We used TransDecoder v5. We also used hmmscan v3. TransDecoder retained the single best ORF for each transcript, and any predicted peptides with an e-value of less than 1e against any database were also retained in the final set.
We used the program OrthoFinder v2. An orthogroup is a monophyletic group of genes descended from an ancestral gene in the last common ancestor of the species being analyzed, and can include both orthologs and paralogs. OrthoFinder also infers a species tree from the single-copy gene trees. We then used PhyloTreePruner v1. For gene trees with monophyletic species-specific gene duplications in-paralogs , PhyloTreePruner retains only the longest paralog sequence. This approach is particularly relevant for transcriptomic data, as apparent in-paralogs are often alternative splice variants of the same gene.
Transcript abundance for each library was quantified using Salmon v0. We used the R package tximport v1. In order to combine the data from different transcriptomes, we edited transcript names to append a species identifier to the Trinity contig name. For each library, we then added the transcript names for the other five species, with a count of zero.
For example, a T. This means that only transcripts belonging to one of the single-copy orthologs were retained for differential expression analysis, although reads were originally mapped to the entire transcriptome.
Importantly, tximport corrects for differences in transcript length when summarizing to the gene level. We used the R package DESeq2 v1. The six individuals within each group belonging to three species were treated as replicates. We were able to compare gene expression across species due to the use of common garden conditions and use of a single life stage. Genes single-copy orthologs with log-fold change greater than or equal to 0.
The code for this analysis is available in Additional file 6. This was done for each transcriptome, and orthogroups were annotated by combining the GO terms from all transcripts belonging to that orthogroup. Of the single-copy orthologs, received at least one GO annotation. We aligned N- and C-terminal domain amino acid sequences with the M-Coffee web server [ 80 ]. Bayesian majority consensus trees were constructed using Mr. Trees were visualized on the iTOL web server [ 82 ] and rooted with a mygalomorph spidroin B.
These analyses set out to look at signatures of selection operating on the different silks. In particular, we tested for diversifying and relaxed selection associated with shifts from web building to cursorial lifestyle and with the loss of web building behavior. Moreover, we tested to see whether similar patterns of selection operated in different lineages where web loss has been documented. We included other published from [ 47 , 83 ] and unpublished Tetragnatha transcriptomes, as well as transcriptomes from three other non-web building families Arkyidae, Malkaridae, and Mimetidae and two Araneoid web-building outgroups in the analyses from [ 61 ].
We used several complementary approaches to test for selection in silk genes. First, we used a gene family clustering approach implemented in the FUSTr pipeline Families Under Selection in Transcriptomes [ 42 ] , which clusters sequences from all available transcriptomes into putative gene families. These gene families do not necessarily contain sequences from all taxa, and given the structure of spidroins discussed in the introduction are likely to contain only fragments of a larger gene.
As input, we used our six new Tetragnatha transcriptomes, 23 additional Tetragnatha transcriptomes corresponding to 22 species T. For each gene family with at least 15 sequences, we then conducted site tests for positive selection using FUBAR [ 87 ]. An additional strategy was used to test for selection in single-copy orthologs in the context of the species tree, using the COATS pipeline unpublished, Brewer et al.
Branch tests were then conducted using the codeml module of PAML [ 91 ]. We limited our analysis to orthologs consistent with the species tree, as evaluated with the approximately unbiased test in IQTREE v2. None of these single-copy orthologs were spidroins, likely because of the relative incompleteness of many of the transcriptomes included in the analysis.
We tested selection in two scenarios, one in which selection acts on the branch leading to the Spiny Leg clade, and another in which selection acts on the branches leading to Spiny Legs and to the other non-web builders essentially, testing for convergence. The versions described in this paper are the first versions, numbered GITM and so on.
All sample information and accession numbers are given in Additional file 5. Homoplasy: from detecting pattern to determining process and mechanism of evolution. Losos J. Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. Berkeley: University of California Press; Google Scholar. Gillespie R. Community assembly through adaptive radiation in Hawaiian spiders. The chronicle of marsupial evolution. Molecular evolution and adaptive eadiation; Hundreds of genes experienced convergent shifts in selective pressure in marine mammals.
Mol Biol Evol. Convergent evolution of hemoglobin function in high-altitude Andean waterfowl involves limited parallelism at the molecular sequence level. PLOS Genet. Genes involved in convergent evolution of eusociality in bees. Genome-wide signatures of convergent evolution in echolocating mammals.
Convergent regulatory evolution and loss of flight in paleognathous birds. Jeffery WR. Regressive evolution in Astyanax cavefish. Annu Rev Genet. Regressive evolution in the Mexican cave tetra, Astyanax mexicanus. Curr Biol CB. The molecular basis of phenotypic convergence. Annu Rev Ecol Evol Syst. Article Google Scholar.
Elmer KR, Meyer A. Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends Ecol Evol. PubMed Article Google Scholar. The Nephila clavipes genome highlights the diversity of spider silk genes and their complex expression. Nat Genet.
Spiders did not repeatedly gain, but repeatedly lost, foraging webs. Silk properties determined by gland-specific expression of a spider fibroin gene family. Extreme dversity, conservation, and convergence of spider silk fibroin sequences. Multi-tissue transcriptomics of the black widow spider reveals expansions, co-options, and functional processes of the silk gland gene toolkit.
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