Molecular phylogenies confirm the presence of two crypticHemimycalespecies in the Mediterranean and reveal the polyphyly of the generaCrellaandHemimycale(Demospongiae: Poecilosclerida)

Abstract

BackgroundSponges are particularly prone to hiding cryptic species as their paradigmatic plasticity often favors species phenotypic convergence as a result of adaptation to similar habitat conditions. Hemimycale is a sponge genus (Family Hymedesmiidae, Order Poecilosclerida) with four formally described species, from which only Hemimycale columella has been recorded in the Atlanto-Mediterranean basin, on shallow to 80 m deep bottoms. Contrasting biological features between shallow and deep individuals of Hemimycale columella suggested larger genetic differences than those expected between sponge populations. To assess whether shallow and deep populations indeed belong to different species, we performed a phylogenetic study of Hemimycale columella across the Mediterranean. We also included other Hemimycale and Crella species from the Red Sea, with the additional aim of clarifying the relationships of the genus Hemimycale.MethodsHemimycale columella was sampled across the Mediterranean, and Adriatic Seas. Hemimycale arabica and Crella cyathophora were collected from the Red Sea and Pacific. From two to three specimens per species and locality were extracted, amplified for Cytochrome C Oxidase I (COI) (M1–M6 partition), 18S rRNA, and 28S (D3–D5 partition) and sequenced. Sequences were aligned using Clustal W v.1.81. Phylogenetic trees were constructed under neighbor joining (NJ), Bayesian inference (BI), and maximum likelihood (ML) criteria as implemented in Geneious software 9.01. Moreover, spicules of the target species were observed through a Scanning Electron microscope.ResultsThe several phylogenetic reconstructions retrieved both Crella and Hemimycale polyphyletic. Strong differences in COI sequences indicated that C. cyathophora from the Red Sea might belong in a different genus, closer to Hemimycale arabica than to the Atlanto-Mediterranean Crella spp. Molecular and external morphological differences between Hemimycale arabica and the Atlanto-Mediterranean Hemimycale also suggest that Hemimycale arabica fit in a separate genus. On the other hand, the Atlanto-Mediterranean Crellidae appeared in 18S and 28S phylogenies as a sister group of the Atlanto-Mediterranean Hemimycale. Moreover, what was known up to now as Hemimycale columella, is formed by two cryptic species with contrasting bathymetric distributions. Some small but consistent morphological differences allow species distinction.ConclusionsA new family (Hemimycalidae) including the genus Hemimycale and the two purported new genera receiving C. cyathophora and Hemimycale arabica might be proposed according to our phylogenetic results. However, the inclusion of additional Operational Taxonomic Unit (OTUs) appears convenient before taking definite taxonomical decisions. A new cryptic species (Hemimycale mediterranea sp. nov.) is described. Morphologically undifferentiated species with contrasting biological traits, as those here reported, confirm that unidentified cryptic species may confound ecological studies.

Redescription and establishment of a holotype and three paratypes for the species Hemimycale mediterranea sp. nov.

“…A complete description of the new species Hemimycale mediterranea is provided by Uriz, Garate & Agell (2017) , and we reference that publication in accordance with Article 13.1.2 of the ICZN Code. However, no holotype was designated for the new species in the previous publication.…”

“…The new species, named Hemimycale mediterranea, was extensively described in the above mentioned paper by Uriz, Garate & Agell (2017) (LSID: urn:lsid:zoobank.org:pub:69255188-5A55-4D5C-9DC2-43E2B6CF6997) based on morphological and molecular characters, but the authors did not include a designation of the holotype specimen of Hemimycale mediterranea . Therefore, this nomenclatural act cannot be considered as published under International Commission on Zoological Nomenclature (ICZN) regulations, and the species name is not available from the earlier version of this work.…”

“…In an earlier version of this article published on 7 March 2017, Uriz, Garate & Agell (2017) reassessed the taxonomy of the genus Hemimycale Burton, 1934 (Porifera: Poecilosclerida), and describe a new species of Hemimycale, which is morphologically cryptic with the Atlanto-Mediterranean Hemimycale columella . The new species, named Hemimycale mediterranea, was extensively described in the above mentioned paper by Uriz, Garate & Agell (2017) (LSID: urn:lsid:zoobank.org:pub:69255188-5A55-4D5C-9DC2-43E2B6CF6997) based on morphological and molecular characters, but the authors did not include a designation of the holotype specimen of Hemimycale mediterranea . Therefore, this nomenclatural act cannot be considered as published under International Commission on Zoological Nomenclature (ICZN) regulations, and the species name is not available from the earlier version of this work.…”

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Background In a recent paper, we described a new sponge species named Hemimycale mediterranea Uriz, Garate & Agell, 2017 . However, we failed to designate a holotype and a type locality, as required by the International Commission on Zoological Nomenclature (ICZN).

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Contrasting biological features in morphologically cryptic Mediterranean sponges

“…H. mediterranea dwells on shallow waters (4–17 m deep) while H. columella is preferentially found from 25 to 60 m depth (Uriz, Garate & Agell, 2017). Thus, these species represented suitable targets to determine whether some depth-related environmental factors might account for contrasting ecological distribution of sponges.…”