Figure 4 - uploaded by Silvia Adrián
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Summary phylogenetic tree from dataset S1 (lower levels of missing data). Bayesian inference (BI) tree obtained from the concatenated analysis of mitochondrial protein coding genes (PCGs) and ribosomal RNAs (rRNAs), summarizing maximum likelihood (ML) and BI (MrBayes) supports from the analyses based in PCGs and the analyses based in PCGs and rRNAs. Clade support: Left column: ML, PCG data (above), PCG + rRNA data (below); right column: BI, PCG data (above), PCG + rRNA data (below). Black square, node supported by ML bootstrap > 80%, and posterior probability > 0,95; grey square, clade recovered but support < 80 or 95%, respectively; white square, clade not recovered. LTC stands for Lost Tracheae Clade and SC for Scytodoidea. Assembled and annotated mitogenomes coded as * (Taxa from S1). Curated mitogenomes downloaded from NCBI without asterisk.
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The advent of high-throughput sequencing technologies (HTS) has generated an unprecedented
amount of genomic and transcriptomic information. A vast amount of
these data is not even used in targeted projects but is made available in public repositories.
Previous studies have demonstrated that HTS data constitute a valuable
resource to recover mitoge...
Citations
... phylogenetic comparative analysis has identified nine distinct cheliceral morphotypes, where species with cheliceral types A, D and E were classified as generalists, while those with types B, C, F, G and I were identified as specialists (Bellvert et al., 2023). Because of the single colonisation event inferred for these species (but see Adrián-Serrano et al., 2020) and the eco-phenotypic differences observed among relatives, this genus has been suggested to be a case of adaptive radiation in the islands (Bellvert et al., 2023), but this hypothesis has never been formally tested and the exact evolutionary drivers of this diversification remain poorly understood. ...
... To investigate the diversification mode in the Dysdera spiders from the Canary Islands, we used the timecalibrated phylogeny, following the removal of non-Canarian species and the endemic D. lancerotensis, as it has been shown to correspond to an independent colonisation not directly related to the rest of the Canarian species (Adrián-Serrano et al., 2020). To obtain a first view of how diversification proceeded across the history of the group, we extracted the branching times with the function branching. ...
The study of adaptive radiations has shed light on our current understanding of evolution. However, previous studies examining the mode in which species diversified, how diversification rates varied, and how ecological specialisation affected these processes have found few different results across different taxa and geographic and ecological systems, showing how complex this process is. To gain a more complete picture of how species evolve, additional model systems that encompass alternative ecological requirements are needed. Here, we present the results of a study aimed at unravelling the diversification mode and evolutionary drivers of the spider genus Dysdera , the red devil spiders, endemic to the Canary Islands. These species exhibit remarkable phenotypic variability in their mouthparts, which has been related to different levels of specialisation in the predation of isopods. We explored patterns of lineage diversification and assessed the role of trophic specialisation as a driver of species diversification. Additionally, we used climatic variables, occurrence data and morphological information to unravel the underlying mode of speciation by means of joint species distribution models and age‐range correlation methods. Our results reveal that red devil spiders underwent an early burst of diversification, followed by a slowdown of diversification rates, which is a hallmark of adaptive radiation. We also found evidence that the trophic morphology shaped diversification, with specialist species exhibiting higher rates of diversification. Finally, our analyses suggest that speciation occurred mostly in allopatry, with subsequent secondary sympatry following range expansion.
... Remarkably, this eco-phenotypic diversity has been observed in both mainland and oceanic islands (Hopkin and Martin 1985;Řezáč, Pekár, and Lubin 2008;Řezáč and Pekár 2007;Toft and Macías-Hernández 2017;Bellvert et al. 2023). However, most of the species in Canary Islands evolved from a single generalist common ancestor in a very short evolutionary period (Adrián-Serrano et al. 2021;Bellvert et al. 2023). At least nine cheliceral morphotypes clearly related to the preference for consuming isopods have evolved independently several times in this archipelago, with co-occurring endemic species tending to diverge in size and mouthpart morphology (Řezáč et al. 2021). ...
The spider genus Dysdera has undergone a remarkable diversification in the oceanic archipelago of the Canary Islands, with ~60 endemic species having originated during the 20 million years since the origin of the archipelago. This evolutionary radiation has been accompanied by substantial dietary shifts, often characterised by phenotypic modifications encompassing morphological, metabolic and behavioural changes. Hence, these endemic spiders represent an excellent model for understanding the evolutionary drivers and to pinpoint the genomic determinants underlying adaptive radiations. Recently, we achieved the first chromosome‐level genome assembly of one of the endemic species, D. silvatica , providing a high‐quality reference sequence for evolutionary genomics studies. Here, we conducted a low coverage‐based resequencing study of a natural population of D. silvatica from La Gomera island. Taking advantage of the new high‐quality genome, we characterised genome‐wide levels of nucleotide polymorphism, divergence and linkage disequilibrium, and inferred the demographic history of this population. We also performed comprehensive genome‐wide scans for recent positive selection. Our findings uncovered exceptionally high levels of nucleotide diversity and recombination in this geographically restricted endemic species, indicative of large historical effective population sizes. We also identified several candidate genomic regions that are potentially under positive selection, highlighting relevant biological processes, such as vision and nitrogen extraction as potential adaptation targets. These processes may ultimately drive species diversification in this genus. This pioneering study of spiders that are endemic to an oceanic archipelago lays the groundwork for broader population genomics analyses aimed at understanding the genetic mechanisms driving adaptive radiation in island ecosystems.
... To date, 47 valid species have been described in the Canarian archipelago (Macías-Hernández et al. 2016), most of which are single-island endemics. The Canarian species assemblage offers an ideal experimental model to study patterns in species radiation as most of their species have diversified from a single common ancestor in the archipelago (Adrián-Serrano et al. 2020), and show a high variability of phenotypic modifications related to ecological performances (Toft andMacías-Hernández 2017, 2021;Řezáč et al. 2021). A former study based on traditional morphometric analysis suggested the existence of 5 cheliceral morphotypes in the islands and linked them to different prey capture strategies (Řezáč et al. 2021). ...
... In addition, we gathered new Low-Coverage Whole Genome Sequencing data for selected species (see Molecular_Sampling of the Supplementary material available on Dryad). We recovered mitochondrial genes using the pipeline detailed in Adrián-Serrano et al. (2020). The concatenated data matrix was further completed by adding species represented by at least one of the following genes obtained by Sanger sequencing: cytochrome c oxidase 1 (COI), the NADH dehydrogenase subunit (nad1), and the large (16S) and small (12S) ribosomal subunits, available either from public databases or generated in house. ...
Natural selection plays a key role in deterministic evolution, as clearly illustrated by the multiple cases of repeated evolution of ecomorphological characters observed in adaptive radiations. Unlike most spiders, Dysdera species display a high variability of cheliceral morphologies, which has been suggested to reflect different levels of specialisation to feed on isopods. In this study, we integrate geometric morphometrics and experimental trials with a fully resolved phylogeny of the highly diverse endemic species from the Canary Islands to 1) quantitatively delimit the different cheliceral morphotypes present in the archipelago, 2) test their association with trophic specialisation, as reported for continental species, 3) reconstruct the evolution of these ecomorphs throughout the diversification of the group, 4) test the hypothesis of convergent evolution of the different morphotypes, and 5) examine whether specialisation constitutes a case of evolutionary irreversibility in this group. We show the existence of nine cheliceral morphotypes and uncovered their significance for trophic ecology. Further, we demonstrate that similar ecomorphs evolved multiple times in the archipelago, providing a novel study system to explain how convergent evolution and irreversibility due to specialization may be combined to shape phenotypic diversification in adaptive radiations.
... Due to the small number of spiders mitogenomes sequenced, it is not clear both the phylogenetic relationships and the types of rearrangements in this genome. Previous studies have focused on studying phylogenetic relationships from complete or partial mitogenomes in spiders and arachnids; resolving key positions of some orders in the Arachnida and new insights into their ancient evolution (Adrián-Serrano et al., 2021;Ban et al., 2022) or through Genome-scale data sets of hundreds of Araneae species (Kulkarni et al., 2021); providing robust phylogenetic relationships, which allow to elucidate the evolution of this important taxonomic group. However, in these studies there is a low number of species analyzed in some taxa, as in the case of the family Ctenidae, among others. ...
Spiders (Araneae) are the most abundant terrestrial predators and megadiverse on earth. In recent years, the mitochondrial genome of a great diversity of species has been sequenced, mainly for ecological and commercial purposes. These studies have uncovered the existence of a variety of mitochondrial genome rearrangements. However, there is poor genetic information in several taxonomic families of spiders. We have sequenced the complete genome of Phoneutria depilata (Ctenidae) and, based on this, extract the mitogenomes of other ctenid species from published transcriptomes to perform a comparative study among spider species to determine the relationship between the level of mitochondrial rearrangements and its possible relationship with molecular variability in spiders. Complete mitochondrial genomes of eighteen spiders (including eight Ctenidae species) were obtained by two different methodologies (sequencing and transcriptome extraction). Fifty-eight spider mitochondrial genomes were downloaded from the NCBI database for gene order analysis. After verifying the annotation of each mitochondrial gene, a phylogenetic and a gene order analysis from 76 spider mitochondrial genomes were carried out. Our results show a high rate of annotation error in the published spider mitochondrial genomes, which could lead to errors in phylogenetic inference. Moreover, to provide new mitochondrial genomes in spiders by two different methodologies to obtain them, our analysis identifies six different mitochondrial architectures among all spiders. Translocation or tandem duplication random loss (TDRL) events in tRNA genes were identified to explain the evolution of the spider mitochondrial genome. In addition, our findings provide new insights into spider mitochondrial evolution.
... Mitochondrial genomes have become an important tool for inferring phylogenetic relationships within crustaceans (González-Castellano et al., 2020;Kilpert & Podsiadlowski, 2006;Lavrov et al., 2004;Shen et al., 2015;Tan et al., 2019). Not only the high number of easily aligned nucleotides and genes, but also the secondary structure of tRNA genes or the arrangement of genes yields data for inferring phylogenetic relationships (Adrián-Serrano et al., 2021;Boore et al., 1995Kilpert & Podsiadlowski, 2006). For some malacostracan crustaceans, such as decapods (>240, Tan et al., 2019), isopods (>40, NCBI, 09.03.2022) and amphipods (>110, NCBI, 09.03.2022), a high number of complete or nearly complete mitochondrial genomes are available, while for other groups like Euphausiacea or Mysida only few species (4 species each, NCBI) were studied. ...
Here, we provide the first complete mitochondrial genomes for two higher taxa of Peracarida, Lophogastrida and Stygiomysida. We examined Lophogaster typicus as a representative of Lophogastrida and Spelaeomysis bottazzii as a representative of Stygiomysida. Both mitogenomes have all typical metazoan genes (13 protein‐coding genes, two ribosomal RNA genes and 22 transfer RNAs). The mitogenomes have a length of 15,076 bp in L. typicus and 14,806 bp in S. bottazzii. Gene order differs markedly from the hypothetical pancrustacean/malacostracan ground pattern in both species, and in L. typicus, all genes were encoded on the heavy strand. This is the first time this is described for a crustacean. We also reconstruct eumalacostracan phylogenies using a data set consisting of 98 species based on alignments comprising all protein‐encoding genes as well as the protein‐encoding genes and the two ribosomal RNAs. We find support for the monophyly of Mysidacea based on species from all three higher taxa (Mysida, Lophogastrida, Stygiomysida). Moreover, our analyses also support a monophyletic Peracarida with Amphipoda or Amphipoda + Mysidacea as the sister group to the remaining Peracarida.
... In A. aquatica mitogenome, the tRNAs are characterized by mismatched aminoacyl acceptor stem, and excepting trnS1 and trnS2 (both with only TΨC loop), the remaining tRNAs lack a TΨC arm 25 . The armless tRNA secondary structures are conserved across the family Dysderidae 36 . and T. vitiana (511 bp) is much shorter than that of T. clavata (848 bp) ( Table 1; Table S2). ...
Spiders of the genera Nephila and Trichonephila are large orb-weaving spiders. In view of the lack of study on the mitogenome of these genera, and the conflicting systematic status, we sequenced (by next generation sequencing) and annotated the complete mitogenomes of N. pilipes, T. antipodiana and T. vitiana (previously N. vitiana) to determine their features and phylogenetic relationship. Most of the tRNAs have aberrant clover-leaf secondary structure. Based on 13 protein-coding genes (PCGs) and 15 mitochondrial genes (13 PCGs and two rRNA genes), Nephila and Trichonephila form a clade distinctly separated from the other araneid subfamilies/genera. T. antipodiana forms a lineage with T. vitiana in the subclade containing also T. clavata, while N. pilipes forms a sister clade to Trichonephila. The taxon vitiana is therefore a member of the genus Trichonephila and not Nephila as currently recognized. Studies on the mitogenomes of other Nephila and Trichonephila species and related taxa are needed to provide a potentially more robust phylogeny and systematics.
The family Dysderidae is a highly diverse group of nocturnal ground‐dwelling and active‐hunter spiders. Dysderids are mostly restricted to the Western Palearctic, and particularly rich and abundant around the Mediterranean region. Interestingly, the distribution of species richness among its 24 genera and three subfamilies is highly biased—80% of its 644 documented species belong to just two genera, Dysdera (326) and Harpactea (211). Dysderidae provides an excellent study case for evolutionary and ecological research. It includes cases of trophic specialization, which are uncommon among spiders, and exhibit other remarkable biological (e.g. holocentric chromosomes), behavioural (e.g. cryptic female choice), evolutionary (e.g. adaptive radiation) and ecological features (e.g. recurrent colonization of the subterranean environment). The lack of a quantitative hypothesis on its phylogenetic structure has hampered its potential as a testing ground for evolutionary, biogeographical and ecological hypotheses. Here, we present the results of a target, multi‐locus phylogenetic analysis, using mitochondrial (cox1, 16s and 12s) and nuclear genes (h3, 28s and 18s), of the most exhaustive taxonomic sample within Dysderidae (104 spp.) to date and across related families (Synspermiata) (83 spp.). We estimate divergence times using a combination of fossil and biogeographic node calibrations and use this timeline to identify shifts in diversification rates. Our results support the monophyly of the Dysderidae subfamilies Rhodinae and Dysderinae but reject Harpacteinae as currently defined. Moreover, the clades recovered within Harpacteinae do not support its current taxonomy. The origin of the family most likely post‐dated the break‐up of Pangea, and cave colonization may be older than previously considered. After correcting for the taxonomic artefacts, we identified a significant shift in diversification rates at the base of the genus Dysdera . Although the unique coexistence of specialist and generalist diets within the lineage could be suggested as the potential driver for the rate acceleration, further quantitative analyses would be necessary to test this hypothesis.
We present the chromosome-level genome assembly of Dysdera silvatica Schmidt, 1981, a nocturnal ground-dwelling spider endemic from the Canary Islands. The genus Dysdera has undergone a remarkable diversification in this archipelago mostly associated with shifts in the level of trophic specialization, becoming an excellent model to study the genomic drivers of adaptive radiations. The new assembly (1.37 Gb; scaffold N50 of 174.2 Mb), was performed using the chromosome conformation capture scaffolding technique, represents a continuity improvement of more than 4,500 times with respect to the previous version. The seven largest scaffolds or pseudochromosomes, which cover 87% of the total assembly size, likely correspond with the seven chromosomes of the karyotype of this species, including a characteristic large X chromosome.
To illustrate the value of this new resource we performed a comprehensive analysis of the two major arthropod chemoreceptor gene families (i.e., gustatory and ionotropic receptors). We identified 545 chemoreceptor sequences distributed across all pseudochromosomes, with a notable underrepresentation in the X chromosome. At least 54% of them localize in 83 genomic clusters with a significantly lower evolutionary distances between them than the average of the family, suggesting a recent origin of many of them. This chromosome-level assembly is the first high-quality genome representative of the Synspermiata clade, and just the third among spiders, representing a new valuable resource to gain insights into the structure and organization of chelicerate genomes, including the role that structural variants, repetitive elements and large gene families played in the extraordinary biology of spiders.