Browsing by Author "Zardoya, Rafael"
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- Chromosome-level genome of the venomous snail Kalloconus canariensis: a valuable model for venomics and comparative genomicsPublication . Herráez-Pérez, Ana; Pardos-Blas, José Ramón; Afonso, Carlos; Tenorio, Manuel J; Zardoya, RafaelBackground: Genomes are powerful resources to understand the evolutionary mechanisms underpinning the origin and diversification of the venoms of cone snails (Conidae: Caenogastropoda) and could aid in the development of novel drugs. Findings: Here, we used PacBio continuous long reads and Omni-C data to assemble the chromosome-level genome of Kalloconus canariensis, a vermivorous cone endemic to the Canary Islands. The final genome size was 2.87 Gb, with a N50 of 79.75 Mb and 91% of the reads located into the 35 largest scaffolds. Up to 55.80% of the genome was annotated as repetitive regions, being class I of transposable elements (16.65%) predominant. The annotation estimated 34,287 gene models. Comparative analysis of this genome with the 2 cone snail genomes released to date (Dendroconus betulinus and Lautoconus ventricosus) revealed similar genome sizes and organization, although chromosome sizes tended to be shorter in K. canariensis. Phylogenetic relationships within subclass Caenogastropoda were recovered with strong statistical support. The family Conidae was recovered as a clade, with K. canariensis plus L. ventricosus sister to D. betulinus. Conclusions: Despite the great diversity of cone snails ( >900 species) and their venoms (hundreds of peptides per species), only 2 recently reported genomes are available for the group. The high-quality chromosome-level assembly of K. canariensis will be a valuable reference for studying the origin and evolution of conotoxin genes as well as whole-genome duplication events during gastropod evolution.
- Comparative transcriptomics of the venoms of continental and insular radiations of West African conesPublication . Abalde, Samuel; Tenorio, Manuel J.; Afonso, Carlos; Zardoya, RafaelThe transcriptomes of the venom glands of 13 closely related species of vermivorous cones endemic to West Africa from generaAfriconusandVarioconuswere sequenced and venom repertoires compared within a phylogenetic framework using oneKalloconusspecies as outgroup. The total number of conotoxin precursors per species varied between 108 and 221. Individuals of the same species shared about one-fourth of the total conotoxin precursors. The number of common sequences was drastically reduced in the pairwise comparisons between closely related species, and the phylogenetical signal was totally eroded at the inter-generic level (no sequence was identified as shared derived), due to the intrinsic high variability of these secreted peptides. A common set of four conotoxin precursor superfamilies (T, O1, O2 and M) was expanded in all studied cone species, and thus, they are considered the basic venom toolkit for hunting and defense in the West African vermivorous cone snails. Maximum-likelihood ancestral character reconstructions inferred shared conotoxin precursors preferentially at internal nodes close to the tips of the phylogeny (between individuals and between closely related species) as well as in the common ancestor ofVarioconus. Besides the common toolkit, the two genera showed significantly distinct catalogues of conotoxin precursors in terms of type of superfamilies present and the abundance of members per superfamily, but had similar relative expression levels indicating functional convergence. Differential expression comparisons between vermivorous and piscivorous cones highlighted the importance of the A and S superfamilies for fish hunting and defense.
- Conotoxin diversity in Chelyconus ermineus (Born, 1778) and the convergent origin of Piscivory in the Atlantic and Indo-Pacific conesPublication . Abalde, Samuel; Tenorio, Manuel J.; Afonso, Carlos; Zardoya, RafaelThe transcriptome of the venom duct of the Atlantic piscivorous cone species Chelyconus ermineus (Born, 1778) was determined. The venom repertoire of this species includes at least 378 conotoxin precursors, which could be ascribed to 33 known and 22 new (unassigned) protein superfamilies, respectively. Most abundant superfamilies were T, W, O1, M, O2, and Z, accounting for 57% of all detected diversity. A total of three individuals were sequenced showing considerable intraspecific variation: each individual had many exclusive conotoxin precursors, and only 20% of all inferred mature peptides were common to all individuals. Three different regions (distal, medium, and proximal with respect to the venom bulb) of the venom duct were analyzed independently. Diversity (in terms of number of distinct members) of conotoxin precursor superfamilies increased toward the distal region whereas transcripts detected toward the proximal region showed higher expression levels. Only the superfamilies A and I3 showed statistically significant differential expression across regions of the venom duct. Sequences belonging to the alpha (motor cabal) and kappa (lightning-strike cabal) subfamilies of the superfamily A were mainly detected in the proximal region of the venom duct. The mature peptides of the alpha subfamily had the α4/4 cysteine spacing pattern, which has been shown to selectively target muscle nicotinic-acetylcholine receptors, ultimately producing paralysis. This function is performed by mature peptides having a α3/5 cysteine spacing pattern in piscivorous cone species from the Indo-Pacific region, thereby supporting a convergent evolution of piscivory in cones.
- Hidden species diversity and mito-nuclear discordance within the Mediterranean cone snail, Lautoconus ventricosusPublication . Abalde, Samuel; Crocetta, Fabio; Tenorio, Manuel J.; D'Aniello, Salvatore; Fassio, Giulia; Rodríguez-Flores, Paula C.; Uribe, Juan E.; Afonso, Carlos; Oliverio, Marco; Zardoya, RafaelThe Mediterranean cone snail, Lautoconus ventricosus, is currently considered a single species inhabiting the whole Mediterranean basin and the adjacent Atlantic coasts. Yet, no population genetic study has assessed its taxonomic status. Here, we collected 245 individuals from 75 localities throughout the Mediterranean Sea and used cox1 barcodes, complete mitochondrial genomes, and genome skims to test whether L. ventricosus represents a complex of cryptic species. The maximum likelihood phylogeny based on complete mitochondrial genomes recovered six main clades (hereby named blue, brown, green, orange, red, and violet) with sufficient sequence divergence to be considered putative species. On the other hand, phylogenomic analyses based on 437 nuclear genes only recovered four out of the six clades: blue and orange clades were thoroughly mixed and the brown one was not recovered. This mito-nuclear discordance revealed instances of incomplete lineage sorting and introgression, and may have caused important differences in the dating of main cladogenetic events. Species delimitation tests proposed the existence of at least three species: green, violet, and red + blue + orange (i.e., cyan). Green plus cyan (with sympatric distributions) and violet, had West and East Mediterranean distributions, respectively, mostly separated by the Siculo-Tunisian biogeographical barrier. Morphometric analyses of the shell using species hypotheses as factor and shell length as covariate showed that the discrimination power of the studied parameters was only 70.2%, reinforcing the cryptic nature of the uncovered species, and the importance of integrative taxonomic approaches considering morphology, ecology, biogeography, and mitochondrial and nuclear population genetic variation.
- Island survivors: population genetic structure and demography of the critically endangered giant lizard of La Gomera, Gallotia bravoanaPublication . Gonzalez, Elena G.; Ceron-Souza, Ivania; Mateo, Jose A.; Zardoya, RafaelBackground: The giant lizard of La Gomera (Gallotia bravoana), is an endemic lacertid of this Canary Island that lives confined to a very restricted area of occupancy in a steep cliff, and is catalogued as Critically Endangered by IUCN. We present the first population genetic analysis of the wild population as well as of captive-born individuals (for which paternity data are available) from a recovery center. Current genetic variability, and inferred past demographic changes were determined in order to discern the relative contribution of natural versus human-mediated effects on the observed decline in population size. Results: Genetic analyses indicate that the only known natural population of the species shows low genetic diversity and acts as a single evolutionary unit. Demographic analyses inferred a prolonged decline of the species for at least 230 generations. Depending on the assumed generation time, the onset of the decline was dated between 1200-13000 years ago. Pedigree analyses of captive individuals suggest that reproductive behavior of the giant lizard of La Gomera may include polyandry, multiple paternity and female long-term sperm retention. Conclusions: The current low genetic diversity of G. bravoana is the result of a long-term gradual decline. Because generation time is unknown in this lizard and estimates had large credibility intervals, it is not possible to determine the relative contribution of humans in the collapse of the population. Shorter generation times would favor a stronger influence of human pressure whereas longer generation times would favor a climate-induced origin of the decline. In any case, our analyses show that the wild population has survived for a long period of time with low levels of genetic diversity and a small effective population size. Reproductive behavior may have acted as an important inbreeding avoidance mechanism allowing the species to elude extinction. Overall, our results suggest that the species retains its adaptive potential and could restore its ancient genetic diversity under favorable conditions. Therefore, management of the giant lizard of La Gomera should concentrate efforts on enhancing population growth rates through captive breeding of the species as well as on restoring the carrying capacity of its natural habitat.
- Mitogenomic phylogeny of cone snails endemic to SenegalPublication . Abalde, Samuel; Tenorio, Manuel J.; Afonso, Carlos; Zardoya, RafaelCone snails attain in Senegal one of their highest peaks of species diversity throughout the continental coast of Western Africa. A total of 15 endemic species have been described, all placed in the genus Lautoconus. While there is ample data regarding the morphology of the shell and the radular tooth of these species, virtually nothing is known regarding the genetic diversity and phylogenetic relationships of one of the most endangered groups of cones. In this work, we determined the complete or near complete (only lacking the control region) mitochondrial (mt) genomes of 17 specimens representing 11 endemic species (Lautoconus belairensis, Lautoconus bruguieresi, Lautoconus cacao, Lautoconus cloveri, Lautoconus cf. echinophilus, Lautoconus guinaicus, Lautoconus hybridus, Lautoconus senegalensis, Lautoconus mercator, Lautoconus taslei, and Lautoconus unifasciatus). We also sequenced the complete mt genome of Lautoconus guanche from the Canary Islands, which has been related to the cones endemic to Senegal. All mt genomes share the same gene arrangement, which conforms to the consensus reported for Conidae, Neogastropoda and Caenogastropoda. Phylogenetic analyses using probabilistic methods recovered three major lineages, whose divergence coincided in time with sea level and ocean current changes as well as temperature fluctuations during the Messinian salinity crisis and the PlioPleistocene transition. Furthermore, the three lineages corresponded to distinct types of radular tooth (robust, small, and elongated), suggesting that dietary specialization could be an additional evolutionary driver in the diversification of the cones endemic to Senegal. The reconstructed phylogeny showed several cases of phenotypic convergence (cryptic species) and questions the validity of some species (ecotypes or phenotypic plasticity), both results having important taxonomic and conservation consequences. (C) 2017 Elsevier Inc. All rights reserved.
- Mitogenomic phylogeny of mud snails of the mostly Atlantic/Mediterranean genus Tritia (Gastropoda: Nassariidae)Publication . Yang, Yi; Abalde, Samuel; Afonso, Carlos L. M.; Tenorio, Manuel J.; Puillandre, Nicolas; Templado, Jose; Zardoya, RafaelThe mud snails endemic to the East Atlantic/Mediterranean region (genus Tritia; subfamily Nassariinae) account for the second highest diversity within the family Nassariidae (Gastropoda: Buccinoidea). In order to understand how the diversity of species, shell morphologies and ecological traits evolved within this genus, a robust phylogenetic framework is needed, yet still unavailable due to high levels of homoplasy in shell morphology, the main trait used for their taxonomic classification. Here, the near-complete mitogenomes of 20 species representing more than half of the diversity of Tritia were sequenced. All mitogenomes of Tritia shared the same gene order, which is identical to the consensus reported for caenogastropods. The reconstructed phylogeny indicates that all analysed Tritia species formed a natural group except Tritia vaucheri, which was sister to an early diverging clade within subfamily Nassariinae that includes species of genus Reticunassa sister to Nassarius jacksonianus and Nassarius sp. Within Tritia, the North-west Atlantic species Tritia obsoleta was placed as the sister group of three mostly East Atlantic/Mediterranean clades (I-III), prompting the reinstatement of the genus Ilyanassa. The latter three clades corresponded to different shell features (I, shell mostly with marked sculpture; II, shell with strong nodules and small size; and III, smooth shell). For Tritia incrassata, the analysed specimens from Norway and from the Spanish Mediterranean coasts showed notable genetic divergence, which may indicate the existence of cryptic species. The ancestral character state reconstruction of protoconch inferred that the ancestor of Tritia had planktotrophic larvae and that a transition to lecithotrophy occurred independently at least three times within Nassariinae. The reconstructed chronogram dated the origin of Tritia in the Oligocene and main diversification events during the Miocene to Pleistocene, correlated with drastic shifts in local paleoecosystems caused by cooling events, eustatic sea level changes and the Messinian Salinity Crisis that favoured temperate taxa.
- Phylogenetic relationships of cone snails endemic to Cabo Verde based on mitochondrial genomesPublication . Abalde, Samuel; Tenorio, Manuel J.; Afonso, Carlos; Uribe, Juan E.; Echeverry, Ana M.; Zardoya, RafaelBackground: Due to their great species and ecological diversity as well as their capacity to produce hundreds of different toxins, cone snails are of interest to evolutionary biologists, pharmacologists and amateur naturalists alike. Taxonomic identification of cone snails still relies mostly on the shape, color, and banding patterns of the shell. However, these phenotypic traits are prone to homoplasy. Therefore, the consistent use of genetic data for species delimitation and phylogenetic inference in this apparently hyperdiverse group is largely wanting. Here, we reconstruct the phylogeny of the cones endemic to Cabo Verde archipelago, a well-known radiation of the group, using mitochondrial (mt) genomes. Results: The reconstructed phylogeny grouped the analyzed species into two main clades, one including Kalloconus from West Africa sister to Trovaoconus from Cabo Verde and the other with a paraphyletic Lautoconus due to the sister group relationship of Africonus from Cabo Verde and Lautoconus ventricosus from Mediterranean Sea and neighboring Atlantic Ocean to the exclusion of Lautoconus endemic to Senegal (plus Lautoconus guanche from Mauritania, Morocco, and Canary Islands). Within Trovaoconus, up to three main lineages could be distinguished. The clade of Africonus included four main lineages (named I to IV), each further subdivided into two monophyletic groups. The reconstructed phylogeny allowed inferring the evolution of the radula in the studied lineages as well as biogeographic patterns. The number of cone species endemic to Cabo Verde was revised under the light of sequence divergence data and the inferred phylogenetic relationships. Conclusions: The sequence divergence between continental members of the genus Kalloconus and island endemics ascribed to the genus Trovaoconus is low, prompting for synonymization of the latter. The genus Lautoconus is paraphyletic. Lautoconus ventricosus is the closest living sister group of genus Africonus. Diversification of Africonus was in allopatry due to the direct development nature of their larvae and mainly triggered by eustatic sea level changes during the Miocene-Pliocene. Our study confirms the diversity of cone endemic to Cabo Verde but significantly reduces the number of valid species. Applying a sequence divergence threshold, the number of valid species within the sampled Africonus is reduced to half.
- The genome of the venomous snail Lautoconus ventricosus sheds light on the origin of conotoxin diversityPublication . Pardos-Blas, José Ramón; Irisarri, Iker; Abalde, Samuel; Afonso, Carlos; Jimenez-Tenorio, M.; Zardoya, RafaelVenoms are deadly weapons to subdue prey or deter predators that have evolved independently in many animal lineages. The genomes of venomous animals are essential to understand the evolutionary mechanisms involved in the origin and diversification of venoms.