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The lush Fucales underwater forests off the Cilento Coast: An overlooked mediterranean biodiversity hotspot

Publication . Rendina, Francesco; Falace, Annalisa; Alongi, Giuseppina; Buia, Maria Cristina; Neiva, J.; Appolloni, Luca; Marletta, Giuliana; Russo, Giovanni Fulvio

Fucales (Phaeophyceae) are ecosystem engineers and forest-forming macroalgae whose populations are declining dramatically. In the Mediterranean Sea, Cystoseira sensu lato (s.l.)—encompassing the genera Cystoseira sensu stricto, Ericaria, and Gongolaria—is the most diverse group, and many species have been shown to be locally extinct in many areas, resulting in a shift toward structurally less complex habitats with the consequent loss of ecosystem functions and services. In this study, we report on the extensive occurrence of healthy and dense marine forests formed by Fucales in the Santa Maria di Castellabate Marine Protected Area in Cilento, Italy (Tyrrhenian Sea, Mediterranean). On a total area of 129.45 ha, 10 Cystoseira s.l. taxa were detected using a combined morphological and molecular approach, with an average cover of more than 70%. One of these taxa has been sequenced for the first time. These findings underline the high ecological value of this area as a hotspot of benthic biodiversity and highlight the importance of marine protected area management and regional monitoring programs to ensure the conservation of these valuable yet fragile coastal ecosystems.

2023-03-29Journal article

Open Access

A low‐latitude species pump: Peripheral isolation, parapatric speciation and mating‐system evolution converge in a marine radiation

Publication . Almeida, Susana C.; Neiva, João; Sousa, Filipe; Martins, Neusa; Cox, Cymon; Melo‐Ferreira, José; Guiry, Michael D.; Serrao, Ester; Pearson, Gareth

Geologically recent radiations can shed light on speciation processes, but incomplete lineage sorting and introgressive gene flow render accurate evolutionary reconstruction and interpretation challenging. Independently evolving metapopulations of low dispersal taxa may provide an additional level of phylogeographic information, given sufficiently broad sampling and genome-wide sequencing. Evolution in the marine brown algal genus Fucus in the south-eastern North Atlantic was shaped by Quaternary climate-driven range shifts. Over this timescale, divergence and speciation occurred against a background of expansion-contraction cycles from multiple refugia, together with mating-system shifts from outcrossing (dioecy) to selfing hermaphroditism. We tested the hypothesis that peripheral isolation of range edge (dioecious) F. vesiculosus led to parapatric speciation and radiation of hermaphrodite lineages. Species tree methods using 876 single-copy nuclear genes and extensive geographic coverage produced conflicting topologies with respect to geographic clades of F. vesiculosus. All methods, however, revealed a new and early diverging hermaphrodite species, Fucus macroguiryi sp. nov. Both the multispecies coalescent and polymorphism-aware models (in contrast to concatenation) support sequential paraphyly in F. vesiculosus resulting from distinct evolutionary processes. Our results support (1) peripheral isolation of the southern F. vesiculosus clade prior to parapatric speciation and radiation of hermaphrodite lineages-a "low-latitude species pump". (2) Directional introgressive gene flow into F. vesiculosus around the present-day secondary contact zone (sympatric-allopatric boundary) between dioecious/hermaphrodite lineages as hermaphrodites expanded northwards, supported by concordance analysis and statistical tests of introgression. (3) Species boundaries in the extensive sympatric range are probably maintained by reproductive system (selfing in hermaphrodites) and reinforcement.

2022Journal article

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The genus Cystoseira s.l. (Ochrophyta, Fucales, Sargassaceae) in the Black Sea: morphological variability and molecular taxonomy of Gongolaria barbata and endemic Ericaria crinita f. bosphorica comb. nov.

Publication . Sadogurska, Sofia S.; Neiva, João; Falace, Annalisa; Serrao, Ester; Israel, Alvaro

Brown algae of the genus Cystoseira sensu lato form the most diverse and productive marine ecosystems throughout the Mediterranean Sea and have equal roles also in the Black Sea where they have been decreasing in the recent years. The taxonomy of Cystoseira s.l. taxa from the Black Sea is still not well understood, and questions arise when related taxa have to be delimited. In addition to morphological descriptions, this study provides for the first time molecular data of the Black Sea Cystoseira s.l. distinct morphologies as an additional tool to clarify their identities and phylogenetic affinities. The analysis of two mitochondrial markers (cytochrome oxidase subunit 1-COI, and 23S-tRNAVal intergenic spacer-mt-spacer) showed that Cystoseira s.l. specimens from the Black Sea belong to two recently resurrected genera, namely Gongolaria and Ericaria. Molecular data confirm the morphological identification of G. barbata, which is characterized by high morphological plasticity in the Black Sea. The morphological data presented in this study support the transition of G. barbata to the genus Gongolaria, which was previously proposed based solely on genetic data. For the Black Sea endemic taxon C. bosphorica, sequence divergence suggests conspecificity with Mediterranean Sea species E. crinita and E. barbatula. However, considering original morphological characteristics of the taxon, its geographical isolation, and endemism, the new combination Ericaria crinita f. bosphorica comb. nov. is proposed.

2021-01Journal article

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DNA barcoding reveals cryptic diversity, taxonomic conflicts and novel biogeographical insights in Cystoseira s.l. (Phaeophyceae)

Publication . Neiva, J.; Bermejo, Ricardo; Medrano, Alba; Capdevila, Pol; Milla-Figueras, David; Afonso, Pedro; Ballesteros, Enric; Sabour, Brahim; Serio, Donatella; Nóbrega, Eduardo; Soares, João; Valdazo, José; Tuya, Fernando; Mulas, Martina; Israel, Álvaro; Sadogurska, Sofia S.; Guiry, Michael D.; Pearson, Gareth; Serrao, Ester

Cystoseira sensu lato (s.l.) - encompassing the genera Cystoseira sensu stricto (s.s.), Ericaria and Gongolaria - is a diverse group of forest-forming brown macroalgae endemic to the warm-temperate North-east Atlantic. These algae have immense biogeographic and ecological significance and have been experiencing recent regional declines. Most Cystoseira s.l. display important morphological plasticity and can be confused with similar species. Therefore, species boundaries, geographic ranges and phylogenetic affinities remain imprecise for most. In the face of persistent taxonomic difficulties, several authors underlined the necessity for new molecular-based approaches, but studies so far lacked representativity, resolution and standardization. To fill in these gaps, in this study we sequenced a comprehensive collection of Cystoseira s.l. spanning its entire North-east Atlantic range for a similar to 1200 bp cox1 barcode, and sequenced selected individuals representing major genetic entities for a few additional plastid markers. Phylogeographic, phylogenetic and species delimitation methods revealed 27 Molecular Operational Taxonomic Units, including unaccounted cryptic diversity, and elucidated with unprecedented resolution species compositions and phylogenetic relationships within each genus. Some entities within the lineages Cystoseira compressa/humilis, Ericaria brachycarpa/crinita, E selaginoides and tophulose Gongolaria, as well as among free-living algae, conflicted with a priori taxonomic assignments, and required the redefinition, reinstatement and recognition of new taxa. For some, diagnostic mutations and biogeography were more useful for species identifications than morphological characters or conventional barcoding gaps. A few species showed narrow geographic ranges and others were the sole representatives of their respective lineages. Several sister-species showed Atlantic vs Mediterranean complementary ranges. phylogenetic signal of coxl was nevertheless insufficient to confidently determine patterns of lineage splitting in several lineages and species complexes and did not improve significantly with additional plastid markers. We discuss novel systematics and biogeography insights considering the advantages and shortcomings of the barcoding approach employed, and how this comprehensive baseline study can be expanded to address multiple questions still left unanswered.

2022Journal article

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eDNA metabarcoding for diet analyses of green sea turtles (Chelonia mydas)

Publication . Díaz-Abad, Lucía; Bacco-Mannina, Natassia; Madeira, Fernando Miguel; Neiva, J.; Aires, Tania; Serrao, Ester; Regalla, Aissa; Patrício, Ana R.; Rodrigues Frade, Pedro

Understanding sea turtle diets can help conservation planning, but their trophic ecology is complex due to life history characteristics such as ontogenetic shifts and large foraging ranges. Studying sea turtle diet is challenging, particularly where ecological foraging observations are not possible. Here, we test a new minimally invasive method for the identifcation of diet items in sea turtles. We fngerprinted diet content using DNA from esophageal and cloacal swab samples by metabarcoding the 18S rRNA gene. This approach was tested on samples collected from green turtles (Chelonia mydas) from a juvenile foraging aggregation in the Bijagós archipelago in Guinea-Bissau. Esophagus samples (n=6) exhibited a higher dietary richness (11±5 amplicon sequence variants (ASVs) per sample; average±SD) than cloacal ones (n=5; 8±2 ASVs). Overall, the diet was dominated by red macroalgae (Rhodophyta; 48.2±16.3% of all ASVs), with the main food item in the esophagus and cloaca being a red alga belonging to the Rhodymeniophycidae subclass (35.1±27.2%), followed by diatoms (Bacillariophyceae; 7.5±7.3%), which were presumably consumed incidentally. Seagrass and some invertebrates were also present. Feeding on red algae was corroborated by feld observations and barcoding of food items available in the benthic habitat, validating the approach for identifying diet content. We conclude that identifcation of food items using metabarcoding of esophageal swabs is useful for a better understanding of the relationships between the feeding behavior of sea turtles and their environment.

2021Journal article

Open Access