Evidence of genetic isolation between two Mediterranean morphotypes of Parazoanthus axinellae

Ingrosso, G. et al. Mediterranean bioconstructions along the Italian coast. Adv. Mar. Biol. 79, 61–136 (2018).

PubMed  Google Scholar 

Giakoumi, S. et al. Ecoregion-based conservation planning in the mediterranean: dealing with large-scale heterogeneity. PLoS ONE 8, e76449 (2013).

ADS  CAS  PubMed  PubMed Central  Google Scholar 

Coll, M. et al. The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS ONE 5, e11842 (2010).

ADS  PubMed  PubMed Central  Google Scholar 

Airoldi, L. & Beck, M. W. Loss, status and trends for coastal marine habitats of Europe. Oceanogr. Mar. Biol. 45, 345–405 (2007).

Google Scholar 

Knowlton, N. Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420, 73–90 (2000).

CAS  Google Scholar 

Todd, P. A. Morphological plasticity in scleractinian corals. Biol. Rev. 83, 315–337 (2008).

PubMed  Google Scholar 

Stefani, F. et al. Comparison of morphological and genetic analyses reveals cryptic divergence and morphological plasticity in Stylophora (Cnidaria, Scleractinia). Coral Reefs 30, 1033–1049. https://doi.org/10.1007/s00338-011-0797-4 (2011).

ADS  Article  Google Scholar 

Pinzon, J. H. et al. Blind to morphology: genetics identifies several widespread ecologically common species and few endemics among Indo–Pacific cauliflower corals (Pocillopora, Scleractinia). J. Biogeogr. 40, 1595–1608 (2013).

Google Scholar 

Costantini, F., Gori, A., Lopez-gonzález, P. & Bramanti, L. Limited genetic connectivity between gorgonian morphotypes along a depth Gradient. PLoS ONE 11, 50–55. https://doi.org/10.1371/journal.pone.0160678 (2016).

CAS  Article  Google Scholar 

Boissin, E., Egea, E., Féral, J. P. & Chenuil, A. Contrasting population genetic structures in Amphipholis squamata, a complex of brooding, self-reproducing sister species sharing life history traits. Mar. Ecol. Prog. Ser. 539, 165–177 (2015).

ADS  CAS  Google Scholar 

Fukami, H. et al. Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58, 324–337 (2004).

CAS  PubMed  Google Scholar 

Costantini, F., Ferrario, F. & Abbiati, M. Chasing genetic structure in coralligenous reef invertebrates: patterns, criticalities and conservation issues. Sci. Rep. 8, 1–12 (2018).

Google Scholar 

Pante, E. et al. Species are hypotheses: avoid connectivity assessments based on pillars of sand. Mol. Ecol. 24, 525–544 (2015).

PubMed  Google Scholar 

Chenuil, A., Cahill, A. E., Délémontey, N., Du Salliant du Luc, E. & Fanton, H. Problems and questions posed by cryptic species. a framework to guide future studies. In From Assessing to Conserving Biodiversity. History. Philosophy and Theory of the Life Sciences (eds Casetta, E. et al.) 77–106 (Springer, New York, 2019).

Google Scholar 

Cowen, R. K. Population connectivity in marine systems. Oceanography 20, 14–21 (2007).

Google Scholar 

Ocaña, O. & Brito, A. Zoanthids parasitizing Anthozoa: taxonomy, ecology and morphological evolution by genomes acquisition. Rev. Acad. Canar. Cienc. 30, 103–134 (2018).

Google Scholar 

Ocaña, O. et al. Parazoanthus axinellae: a species complex showing different ecological requierements. Rev. Acad. Canar. Cienc. XXXI, 1–24 (2019).

Google Scholar 

Lwowsky, F. F. Revision der Gattung Sidisia Gray (Epizoanthus auct.). Ein Beitrag zur Kenntnis der Zoanthiden. Zool. Jahrbücher, Abteilung für Syst. Ökologie und Geogr. der Tiere 34, 557–614 (1913).

Google Scholar 

Herberts, C. Contribution a l’etude biologique de quelques zoantharies tempérés et tropicaux II. Relations entre la reproduction sexue ´e, la corissance somatique et le bourgeonnement. Tethys 4, 961–968 (1972).

Google Scholar 

Ryland, J. S. & Lancaster, J. E. A review of zoanthid nematocyst types and their population structure. Hydrobiologia 530, 179 (2004).

Google Scholar 

Cariello, L., Crescenzi, S., Prota, G. & Zanetti, L. Methylation of zoanthoxanthins. Tetrahedon 30, 3611–3614 (1974).

CAS  Google Scholar 

Cariello, L., Crescenzi, S., Prota, G. & Zanetti, L. Zoanthoxanthins of a new structural type from Epizoanthus arenaceus (Zoantharia). Tetrahedon 30, 9191–4196 (1974).

Google Scholar 

Cariello, L. et al. Zoanthoxanthin, a natural 1,2,5,7-tetrazacyclopent[f]-azulene from Parazoanthus axinellae. Tetrahedon 30, 3281–3287 (1974).

CAS  Google Scholar 

Carreiro-Silva, M. et al. Zoantharians (Hexacorallia: Zoantharia) associated with cold-water corals in the azores region: New species and associations in the deep sea. Front. Mar. Sci. 4, 88 (2017).

Google Scholar 

Montenegro, J., Low, M. E. Y. & Reimer, J. D. The resurrection of the genus Bergia (Anthozoa, Zoantharia, Parazoanthidae). Syst. Biodivers. 14, 63–73 (2016).

Google Scholar 

Sinniger, F., Montoya-Burgos, J., Chevaldonné, P. & Pawlowski, J. Phylogeny of the order Zoantharia (Anthozoa, Hexacorallia) based on the mitochondrial ribosomal genes. Mar. Biol. 147, 1121–1128 (2005).

CAS  Google Scholar 

Sinniger, F., Reimer, J. D. & Pawlowski, J. Potential of DNA Sequences to Identify Zoanthids (Cnidaria: Zoantharia). Zoolog. Sci. 25, 1253–1260 (2008).

CAS  PubMed  Google Scholar 

Pax, F. Die Zoanthanen des Golfes von Neapel. Pubbl. della Stn. Zool. di Napoli 30, 309–329 (1957).

Google Scholar 

Gili, J. M., Pages, F. & Barange, M. Zoantharios (Cnidaria, Anthozoa) de la costa y de la plataforma continental catalanas (Mediterraneo Occidental). Misc. Zool. 11, 13–24 (1987).

Google Scholar 

Abel, E. F. Zur Kenntnis der mannen Höhlenfauna unter besonderer Berücksichtigung der Anthozoen. Pubbl. della Stn. Zool. di Napoli 30, 1–94 (1959).

Google Scholar 

Cachet, N. et al. Metabolomic profiling reveals deep chemical divergence between two morphotypes of the zoanthid Parazoanthus axinellae. Sci. Rep. 5, 8282 (2015).

CAS  PubMed  PubMed Central  Google Scholar 

Cerrano, C., Totti, C., Sponga, F. & Bavestrello, G. Summer disease in Parazoanthus axinellae (Schmidt, 1862) (Cnidaria, Zoanthidea). Ital. J. Zool. 73, 355–361 (2006).

Google Scholar 

Fu, Y.-X. & Li, W.-H. Statistical tests of neutrality of mutations. Genetics 133, 693–770 (1993).

CAS  PubMed  PubMed Central  Google Scholar 

Rogers, A. R. & Harpending, H. Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 9, 552–569 (1992).

CAS  PubMed  Google Scholar 

Paradis, E. Pegas: An R package for population genetics with an integrated-modular approach. Bioinformatics 26, 419–420 (2010).

CAS  PubMed  Google Scholar 

Costantini, F., Fauvelot, C. & Abbiati, M. Fine-scale genetic structuring in Corallium rubrum: evidence of inbreeding and limited effective larval dispersal. Mar. Ecol. Prog. Ser. 340, 109–119 (2007).

ADS  CAS  Google Scholar 

Mokhtar-Jamaï, K. et al. From global to local genetic structuring in the red gorgonian Paramuricea clavata: the interplay between oceanographic conditions and limited larval dispersal. Mol. Ecol. 20, 3291–3305 (2011).

PubMed  Google Scholar 

Villamor, A., Costantini, F. & Abbiati, M. Multilocus phylogeography of Patella caerulea (Linnaeus, 1758) reveals contrasting connectivity patterns across the Eastern-Western Mediterranean transition. J. Biogeogr. 45, 1301–1312 (2018).

Google Scholar 

Rossi, V., Ser-Giacomi, E., Lõpez, C. & Hernández-García, E. Hydrodynamic provinces and oceanic connectivity from a transport network help designing marine reserves. Geophys. Res. Lett. 41, 2883–2891 (2014).

ADS  Google Scholar 

Pax, F. & Muller, I. Die Anthozoenfauna der Adria. Fauna Flora Adriat. 3, 1–343 (1962).

Google Scholar 

Ryland, J. S. Reproduction in Zoanthidea (Anthozoa: Hexacorallia). Invertebr. Reprod. Dev. 31, 177–188 (1997).

Google Scholar 

Previati, M., Palma, M., Bavestrello, G., Falugi, C. & Cerrano, C. Reproductive biology of Parazoanthus axinellae (Schmidt, 1862) and Savalia savaglia (Bertoloni, 1819) (Cnidaria, Zoantharia) from the NW Mediterranean coast. Mar. Ecol. 31, 555–565 (2010).

ADS  Google Scholar 

Sinniger, F., Reimer, J. D. & Pawlowski, J. The Parazoanthidae (Hexacorallia: Zoantharia) DNA taxonomy: description of two new genera. Mar. Biodivers. 40, 57–70 (2010).

Google Scholar 

Aurelle, D. et al. Fuzzy species limits in Mediterranean gorgonians (Cnidaria, Octocorallia): inferences on speciation processes. Zool. Scr. 46, 767–778 (2017).

Google Scholar 

Swain, T. D. Revisiting the phylogeny of Zoanthidea (Cnidaria: Anthozoa): staggered alignment of hypervariable sequences improves species tree inference. Mol. Phylogenet. Evol. 118, 1–12 (2018).

PubMed  Google Scholar 

Sinniger, F. & Häussermann, V. Zoanthids (Cnidaria: Hexacorallia: Zoantharia) from shallow waters of the southern Chilean fjord region, with descriptions of a new genus and two new species. Org. Divers. Evol. 9, 23–36 (2009).

Google Scholar 

Jaramillo, K. B. et al. Assessing the zoantharian diversity of the Tropical Eastern Pacific through an integrative approach. Sci. Rep. 8, 1–15 (2018).

CAS  Google Scholar 

Swain, T. D. Evolutionary transitions in symbioses: dramatic reductions in bathymetric and geographic ranges of Zoanthidea coincide with loss of symbioses with invertebrates. Mol. Ecol. 19, 2587–2598 (2010).

CAS  PubMed  Google Scholar 

Samorì, C., Costantini, F., Galletti, P., Tagliavini, E. & Abbiati, M. Inter- and intraspecific variability of nitrogenated compounds in gorgonian corals via application of a fast one-step analytical protocol. Chem. Biodivers. 15, e1700449 (2018).

Google Scholar 

Pante, E. et al. Use of RAD sequencing for delimiting species. Heredity 14, 450–459. https://doi.org/10.1038/hdy.2014.105 (2014).

CAS  Article  Google Scholar 

Poliseno, A. et al. Evolutionary implications of analyses of complete mitochondrial genomes across order Zoantharia (Cnidaria: Hexacorallia). J. Zool. Syst. Evol. Res. 10, 1–11. https://doi.org/10.1111/jzs.12380 (2020).

Article  Google Scholar 

Taboada, S. & Pérez-Portela, R. Contrasted phylogeographic patterns on mitochondrial DNA of shallow and deep brittle stars across the Atlantic-Mediterranean area. Sci. Rep. 6, 32425 (2016).

ADS  CAS  PubMed  PubMed Central  Google Scholar 

Cerrano, C., Milanese, M. & Ponti, M. Diving for science–science for diving: volunteer scuba divers support science and conservation in the Mediterranean Sea. Aquat. Conserv. Mar. Freshw. Ecosyst. 27, 303–323 (2017).

Google Scholar 

Swain, T. D. Phylogeny-based species delimitations and the evolution of host associations in symbiotic zoanthids (Anthozoa, Zoanthidea) of the wider Caribbean region. Zool. J. Linn. Soc. 156, 223–238 (2009).

Google Scholar 

Katoh, K., Rozewicki, J. & Yamada, K. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 20, 1160–1166 (2017).

PubMed Central  Google Scholar 

Heibl, C. PHYLOCH: R language tree plotting tools and interfaces to diverse phylogenetic software packages. http://www.christophheibl.de/Rpackages.html (2008).

Librado, P. & Rozas, J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452 (2009).

CAS  PubMed  PubMed Central  Google Scholar 

Team, R. C. R: a language and environment for statistical computing (2018).

Mauri, M., Elli, T., Caviglia, G., Uboldi, G. & Azzi, M. RAWGraphs: a visualisation platform to create open outputs. ACM Int. Conf. Proceeding Ser. Part F1313 (2017).

Paradis, E. Analysis of haplotype networks: The randomized minimum spanning tree method. Methods Ecol. Evol. 9, 1308–1317 (2018).

Google Scholar 

Excoffier, L. & Lischer, H. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010).

PubMed  Google Scholar 

Narum, S. R. Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv. Genet. 7, 783–787 (2006).

CAS  Google Scholar 

Tajima, F. Statistical methods for testing the neutral mutation hypothesis by DNA polymorphisms. Genetics 123, 585–595 (1989).

CAS  PubMed  PubMed Central  Google Scholar 

Montenegro, J., Sinniger, F. & Reimer, J. D. Unexpected diversity and new species in the sponge-Parazoanthidae association in southern Japan. Mol. Phylogenet. Evol. 89, 73–90 (2015).

CAS  PubMed  Google Scholar 

Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552 (2000).

CAS  PubMed  Google Scholar 

Schliep, K. Phangorn: phylogenetic analysis in R. Bioinformatics 27, 592–593 (2011).

CAS  PubMed  PubMed Central  Google Scholar 

Schliep, K., Potts, A., Morrison, D. & Grimm, G. Intertwining phylogenetic trees and networks. Methods Ecol. Evol. 8, 212–1220 (2017).

Google Scholar 

Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).

PubMed  PubMed Central  Google Scholar