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- Divergence and gene flow history at two large chromosomal inversions underlying ecotype differentiation in the long‐snouted seahorsePublication . Meyer, Laura; Barry, Pierre; Riquet, Florentine; Foote, Andrew; Der Sarkissian, Clio; Cunha, Regina L.; Arbiol, Christine; Cerqueira, Frédérique; Desmarais, Erick; Bordes, Anaïs; Bierne, Nicolas; Guinand, Bruno; Gagnaire, Pierre‐AlexandreChromosomal inversions can play an important role in divergence and reproductive isolation by building and maintaining distinct allelic combinations between evolutionary lineages. Alternatively, they can take the form of balanced polymorphisms that segregate within populations until one arrangement becomes fixed. Many questions remain about how inversion polymorphisms arise, how they are maintained over the long term, and ultimately, whether and how they contribute to speciation. The long-snouted seahorse (Hippocampus guttulatus) is genetically subdivided into geographic lineages and marine-lagoon ecotypes, with shared structural variation underlying lineage and ecotype divergence. Here, we aim to characterize structural variants and to reconstruct their history and suspected role in ecotype formation. We generated a near chromosome-level genome assembly and described genome-wide patterns of diversity and divergence through the analysis of 112 whole-genome sequences from Atlantic, Mediterranean, and Black Sea populations. By also analysing linked-read sequencing data, we found evidence for two chromosomal inversions that were several megabases in length and showed contrasting allele frequency patterns between lineages and ecotypes across the species range. We reveal that these inversions represent ancient intraspecific polymorphisms, one likely being maintained by divergent selection and the other by pseudo-overdominance. A possible selective coupling between the two inversions was further supported by the absence of specific haplotype combinations and a putative functional interaction between the two inversions in reproduction. Lastly, we detected gene flux eroding divergence between inverted alleles at varying levels for the two inversions, with a likely impact on their dynamics and contribution to divergence and speciation.
- Drivers of Cape Verde archipelagic endemism in keyhole limpetsPublication . Lopes Da Cunha, Regina; Assis, J.; Madeira, Celine; Seabra, Rui; Lima, Fernando P.; Lopes, Evandro P.; Williams, Suzanne T.; Castilho, RitaOceanic archipelagos are the ideal setting for investigating processes that shape species assemblages. Focusing on keyhole limpets, genera Fissurella and Diodora from Cape Verde Islands, we used an integrative approach combining molecular phylogenetics with ocean transport simulations to infer species distribution patterns and analyse connectivity. Dispersal simulations, using pelagic larval duration and ocean currents as proxies, showed a reduced level of connectivity despite short distances between some of the islands. It is suggested that dispersal and persistence driven by patterns of oceanic circulation favouring self-recruitment played a primary role in explaining contemporary species distributions. Mitochondrial and nuclear data revealed the existence of eight Cape Verde endemic lineages, seven within Fissurella, distributed across the archipelago, and one within Diodora restricted to Boavista. The estimated origins for endemic Fissurella and Diodora were 10.2 and 6.7 MY, respectively. Between 9.5 and 4.5 MY, an intense period of volcanism in Boavista might have affected Diodora, preventing its diversification. Having originated earlier, Fissurella might have had more opportunities to disperse to other islands and speciate before those events. Bayesian analyses showed increased diversification rates in Fissurella possibly promoted by low sea levels during Plio-Pleistocene, which further explain differences in species richness between both genera.
- Genomics goes deeper in fisheries science: The case of the blackspot seabream (Pagellus bogaraveo) in the northeast AtlanticPublication . Cunha, Regina L.; Robalo, Joana I.; Francisco, Sara M.; Farias, Inês; Castilho, Rita; Figueiredo, IvoneRecent advances in genomics are an essential contributor to the assessment of fish stocks by providing a finescale identification of the species' genetic boundaries. The blackspot seabream, Pagellus bogaraveo, is a commercial sparid distributed across the northeast (NE) Atlantic and the Mediterranean. Within the NE Atlantic, three P. bogaraveo stocks are currently defined: Azores; Atlantic Iberian waters; Celtic Sea and the Bay of Biscay. We used a genotyping-by-sequencing (GBS) approach to better define the spatial scale at which the species occurs in the NE Atlantic. Our findings revealed the existence of an additional genetic cluster in the eastern Atlantic (Gulf of C ' adiz) that was not identified in previous studies based on mitochondrial DNA or microsatellite data. The combined effect of ocean circulation patterns, complex bathymetry and the existence of local upwelling may play an important role on the retention of blackspot seabream larvae and adults, providing an explanation for the genetic differentiation between the specimens caught off the Gulf of C ' adiz and Peniche (Portugal). Results presented here revealed hidden intra-specific genetic differentiation and can inform a finer-scale sampling to determine the new stock boundaries in the Atlantic Iberian coasts.
- Distinctive genetic signatures of two fairy shrimp species with overlapping ranges in Iberian temporary pondsPublication . Lopes Da Cunha, Regina; Sala, Jordi; Machado, Margarida; Boix, Dani; Madeira, Celine; Madeira, Pedro M.; Cristo, Margarida; Cancela Da Fonseca, Luís; Castilho, RitaTemporary lentic water bodies host biotic assemblages adapted to the transient nature of these freshwater habitats. Fairy shrimps (Crustacea, Branchiopoda, Anostraca) are one of the most important biological components of these unique environments and have a fossil record dating back to the Middle Jurassic (>150 million years). Some anostracan species show a geographically restricted distribution, whereas others are widely dispersed. We aimed to investigate the relationship between different geographic extents and patterns of genetic structure in species of Anostraca. Following this objective, we selected two species with contrasting ranges but overlapping geographic distributions and similar life-history traits in the study area. We analysed additional information that, from an ecological (e.g. egg-bank, niche breadth, and pond connectivity) and evolutionary (e.g. crown-group age of each species) perspective, may explain the obtained phylogeographic patterns. Between 2005 and 2018, we sampled two species of fairy shrimps (309 specimens of Branchipus cortesi and 264 specimens of Tanymastix stagnalis) from 53 temporary ponds of Portugal. We added five other locations from Spain and France to include other European locations for T. stagnalis. Additionally, we also sampled Branchipus schaefferi from two temporary water bodies (Spain and Morocco) to include in the dating analysis. Reconstructed phylogenies based on mitochondrial sequence data indicate the existence of deeply divergent clades with an unequivocal phylogeographic structure in T. stagnalis and shallower divergences in B. cortesi with a less clear geographic correspondence. We found evidence of frequent local and rare long-distance dispersal events in both species and limited intermediate dispersal, which was more common in B. cortesi. A Bayesian dating analysis using the Branchiopoda fossil record estimated the age of the most recent common ancestors of T. stagnalis and B. cortesi at 32.4 and 12.8 million years, respectively. Haplotype accumulation curves indicated that only a portion of the genetic composition of the species was sampled on each hydroperiod and showed the existence of large, genetically diverse egg banks that remain in the soil. These egg banks represent a genetic reservoir that guarantees the survival of the species because active populations from different hydroperiods may be genetically different and adapt to a changing environment. We hypothesise that the contrasting phylogeographic patterns displayed by the two fairy shrimp species may result from: (1) the earlier age of the most recent common ancestor of T. stagnalis, as older species have more time to accumulate mutations and, thus, are expected to exhibit higher genetic differentiation among populations; (2) slight differences in adult behaviour, life-history traits and cyst morphologies of T. stagnalis and B. cortesi favouring different animal dispersal vectors with distinct dispersal abilities. Therefore, phylogeographic patterns may be explained by both evolutionary and ecological processes, which operate in different time scales.
- Uncovering the shell game with barcodes: diversity of meiofaunal Caecidae snails (Truncatelloidea, Caenogastropoda) from Central AmericaPublication . Egger, Christina; Neusser, Timea P.; Norenburg, Jon; Leasi, Francesca; Buge, Barbara; Vannozzi, Angelo; Cunha, Regina L.; Cox, Cymon J.; Jörger, Katharina M.Caecidae is a species-rich family of microsnails with a worldwide distribution. Typical for many groups of gastropods, caecid taxonomy is largely based on overt shell characters. However, identification of species using shell characteristics is problematic due to their rather uniform, tubular shells, the presence of different growth stages, and a high degree of intraspecific variability. In the present study, a first integrative approach to caecid taxonomy is provided using light-microscopic investigation with microsculptural analyses and multi-marker barcoding, in conjunction with molecular species delineation analyses (ABGD, haplotype networks, GMYC, and bPTP). In total 132 specimens of Caecum and Meioceras collected during several sampling trips to Central America were analyzed and delineated into a minimum of 19 species to discuss putative synonyms, and supplement the original descriptions. Molecular phylogenetic analyses suggest Meioceras nitidum and M. cubitatum should be reclassified as Caecum, and the genus Meioceras might present a junior synonym of Caecum. Meiofaunal caecids morphologically resembling C. glabrum from the Northeast Atlantic are a complex of cryptic species with independent evolutionary origins, likely associated with multiple habitat shifts to the mesopsammic environment. Caecum invisibile Egger & Jörger, sp. nov. is formally described based on molecular diagnostic characters. This first integrative approach towards the taxonomy of Caecidae increases the known diversity, reveals the need for a reclassification of the genus Caecum and serves as a starting point for a barcoding library of the family, thereby enabling further reliable identifications of these taxonomically challenging microsnails in future studies.
- Invasion genetics of the mummichog (Fundulus heteroclitus): recent anthropogenic introduction in IberiaPublication . Morim, Teófilo; Bigg, Grant R.; Madeira, Pedro M.; Palma, Jorge; Duvernell, David D.; Gisbert, Enric; Lopes Da Cunha, Regina; Castilho, RitaHuman activities such as trade and transport have increased considerably in the last decades, greatly facilitating the introduction and spread of non-native species at a global level. In the Iberian Peninsula, Fundulus heteroclitus, a small euryhaline coastal fish with short dispersal, was found for the first time in the mid-1970s. Since then, F. heteroclitus has undergone range expansions, colonizing the southern region of Portugal, southwestern coast of Spain and the Ebro Delta in the Mediterranean Sea. Cytochrome b sequences were used to elucidate the species invasion pathway in Iberia. Three Iberian locations (Faro, Cádiz and Ebro Delta) and 13 other locations along the native range of F. heteroclitus in North America were sampled. Results revealed a single haplotype, common to all invasive populations, which can be traced to the northern region of the species' native range. We posit that the origin of the founder individuals is between New York and Nova Scotia. Additionally, the lack of genetic structure within Iberia is consistent with a recent invasion scenario and a strong founder effect. We suggest the most probable introduction vector is associated with the aquarium trade. We further discuss the hypothesis of a second human-mediated introduction responsible for the establishment of individuals in the Ebro Delta supported by the absence of adequate muddy habitats linking Cádiz and the Ebro Delta. Although the species has a high tolerance to salinity and temperature, ecological niche modelling indicates that benthic habitat constraints prevent along-shore colonisation suggesting that such expansions would need to be aided by human release.
- Different diversity-dependent declines in speciation rate unbalances species richness in terrestrial slugsPublication . Lopes Da Cunha, Regina; Patrao, Claudia; Castilho, RitaTwo genera of terrestrial slugs (Arion and Geomalacus) display a striking disproportion in species richness in the Iberian Peninsula. While there are 17 Iberian endemic species in Arion, morphological criteria only recognize four species within Geomalacus. Sequence data were used to test whether these differences could result from: (1) cryptic diversity within Geomalacus; (2) an earlier origin for Arion (older clades are expected to accumulate more species); (3) distinct patterns of diversification rates (higher initial speciation rates in Arion), and (4) some combination of the above factors (e.g., an older clade with higher speciation rates). Species delimitation tests based on mitochondrial and nuclear data revealed eight cryptic lineages within Geomalacus that lessened the asymmetry; nevertheless, the disparity required further investigation. No meaningful differences in crown group ages of each recovered clade were found. Regardless the different premises of the two equally plausible diversification models (similar initial speciation rates vs. higher initial speciation rates in Geomalacus), both coincide on diversity-dependent diversification for the two groups but weaker rate declines in Arion best explains the observed asymmetry in species richness. Also, the broader environmental tolerance combined with a faster dispersal and wider distribution may have represented an evolutionary advantage for Arion.
- Three mitochondrial lineages and no Atlantic-Mediterranean barrier for the bogue Boops boops across its widespread distributionPublication . Cunha, Regina L.; Faleh, Abderraouf Ben; Francisco, Sara; Šanda, Radek; Vukić, Jasna; Corona, Luana; Dia, Mamadou; Glavičić, Igor; Kassar, Abderrahmane; Castilho, Rita; Robalo, Joana I.Marine species exhibiting wide distributional ranges are frequently subdivided into discrete genetic units over limited spatial scales. This is often due to specific life-history traits or oceanographic barriers that prevent gene flow. Fine-scale sampling studies revealed distinct phylogeographic patterns in the northeastern Atlantic and the Mediterranean, ranging from panmixia to noticeable population genetic structure. Here, we used mitochondrial sequence data to analyse connectivity in the bogue Boops boops throughout most of its widespread distribution. Our results identified the existence of three clades, one comprising specimens from the Azores and eastern Atlantic/Mediterranean, another with individuals from the Canary Islands, Madeira and Cape Verde archipelagos, and the third with samples from Mauritania only. One of the branches of the northern subtropical gyre (Azores Current) that drifts towards the Gulf of Cadiz promotes a closer connection between the Azores, southern Portugal and the Mediterranean B. boops populations. The Almeria-Oran Front, widely recognised as an oceanographic barrier for many organisms to cross the Atlantic-Mediterranean divide, does not seem to affect the dispersal of this benthopelagic species. The southward movement of the Cape Verde Frontal Zone during the winter, combined with the relatively short duration of the pelagic larval stage of B. boops, may be potential factors for preventing the connectivity between the Atlantic oceanic archipelagos and Mauritania shaping the genetic signature of this species.
- Phylogeny and diversification patterns among vesicomyid bivalvesPublication . Decker, Carole; Olu, Karine; Cunha, Regina L.; ARNAUD-HAOND, SophieVesicomyid bivalves are among the most abundant and diverse symbiotic taxa in chemosynthetic-based ecosystems: more than 100 different vesicomyid species have been described so far. In the present study, we investigated the phylogenetic positioning of recently described vesicomyid species from the Gulf of Guinea and their western Atlantic and Pacific counterparts using mitochondrial DNA sequence data. The maximum-likelihood (ML) tree provided limited support for the recent taxonomic revision of vesicomyids based on morphological criteria; nevertheless, most of the newly sequenced specimens did not cluster with their morphological conspecifics. Moreover, the observed lack of geographic clustering suggests the occurrence of independent radiations followed by worldwide dispersal. Ancestral character state reconstruction showed a significant correlation between the characters "depth'' and "habitat'' and the reconstructed ML phylogeny suggesting possible recurrent events of 'stepwise speciation' from shallow to deep waters in different ocean basins. This is consistent with genus or species bathymetric segregation observed from recent taxonomic studies. Altogether, our results highlight the need for ongoing re-evaluation of the morphological characters used to identify vesicomyid bivalves.
- Hidden diversity of the olive ridley sea turtle (Lepidochelys olivacea) from Angola, West AfricaPublication . Cunha, Regina L.; Costa, Adjany; Godinho, Filipa; Santos, Carmen; Castilho, RitaThe olive ridley sea turtle (Lepidochelys olivacea) occupies a wide range within the tropical and subtropical areas of the Pacific, Indian, and Southern Atlantic Oceans. Although occurring in large numbers, the IUCN status for this species is "vulnerable" due to existing threats in their nesting sites. We report the first genetic data on L. olivacea from Palmeirinhas-Onca beach, Angola, West Africa. Genetic diversity based on a 400 bp-fragment of the mitochondrial control region of 39 individuals indicated low nucleotide and haplotype diversities compared to other Atlantic populations. We detected a new haplotype present in two individuals from Angola, while the remaining specimens shared a haplotype that is distributed in both sides of the Atlantic and in the Mediterranean, suggesting connectivity between these populations. The baseline data we are generating have a broader significance for characterizing intraspecific biodiversity in the olive ridley sea turtle, which is vital for developing effective conservation policies.