Biodiversity and conservation of threatened freshwater bivalves using multidisciplinary approaches

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Publications

The first Margaritiferidae male (M-Type) mitogenome: Mitochondrial gene order as a potential character for determining higher-order phylogeny within Unionida (Bivalvia)

Publication . Lopes-Lima, Manuel; Fonseca, Miguel M.; Aldridge, David C.; Bogan, Arthur E.; Gan, Han Ming; Ghamizi, Mohamed; Sousa, Ronaldo; Teixeira, Amílcar; Varandas, Simone; Zanatta, David T.; Zieritz, Alexandra; Froufe, Elsa

2017Journal article

Open access

Phylogeny of the most species-rich freshwater bivalve family (Bivalvia: Unionida: Unionidae): defining modern subfamilies and tribes

Publication . Lopes-Lima, Manuel; Froufe, Elsa; Do, Van Tu; Ghamizi, Mohamed; Mock, Karen E.; Kebapçi, Ümit; Klishko, Olga; Kovitvadhi, Satit; Kovitvadhi, Uthaiwan; Paulo, Octávio S.; Pfeiffer, John; Raley, Morgan; Riccardi, Nicoletta; Şereflişan, Hülya; Sousa, Ronaldo; Teixeira, Amílcar; Varandas, Simone; Wu, Xiaoping; Zanatta, David T.; Zieritz, Alexandra; Bogan, Arthur E.

Freshwater mussels of the order Unionida are key elements of freshwater habitats and are responsible for important ecological functions and services. Unfortunately, these bivalves are among the most threatened freshwater taxa in the world. However, conservation planning and management are hindered by taxonomic problems and a lack of detailed ecological data. This highlights the urgent need for advances in the areas of systematics and evolutionary relationships within the Unionida. This study presents the most comprehensive phylogeny to date of the larger Unionida family, i.e., the Unionidae. The phylogeny is based on a combined dataset of 1032 bp (COI + 28S) of 70 species in 46 genera, with 7 of this genera being sequenced for the first time. The resulting phylogeny divided the Unionidae into 6 supported subfamilies and 18 tribes, three of which are here named for the first time (i.e., Chamberlainiini nomen novum, Cristariini nomen novum and Lanceolariini nomen novum). Molecular analyses were complemented by investigations of selected morphological, anatomical and behavioral characters used in traditional phylogenetic studies. No single morphological, anatomical or behavioral character was diagnostic at the subfamily level and few were useful at the tribe level. However, within subfamilies, many tribes can be recognized based on a subset of these characters. The geographical distribution of each of the subfamilies and tribes is also presented. The present study provides important advances in the systematics of these extraordinary taxa with implications for future ecological and conservation studies.

2017Journal article

Open access

Lifting the curtain on the freshwater mussel diversity of the Italian Peninsula and Croatian Adriatic coast

Publication . Froufe, Elsa; Lopes-Lima, Manuel; Riccardi, Nicoletta; Zaccara, Serena; Vanetti, Isabella; Lajtner, Jasna; Teixeira, Amílcar; Varandas, Simone; Prié, Vincent; Zieritz, Alexandra; Sousa, Ronaldo; Bogan, Arthur E.

Freshwater mussels of the order Unionida have been dramatically declining globally. Despite their ecological importance, conservation of these animals has been hindered by unresolved taxonomy and a lack of data on the distribution and status of populations, especially in southern Europe. Although the Italian Peninsula has been noted as a centre of endemism and one of the major refugia of the glacial ages for several taxa, few studies have been performed on the genetic diversity of Unionida. Most importantly, the taxonomic status of several freshwater mussel populations of the Italian Peninsula is still unresolved. Here we present the first comprehensive dataset for the Unionida of the region spanning Italy and the coastal Croatian region (west of the Dinaric Alps). In total, 191 specimens were collected (85 Anodonta, 64 Unio, 17 Microcondylaea bonellii and 25 Sinanodonta woodiana) from 34 sites across the Italian Peninsula and coastal Croatian river basins for molecular identification (COI, 16S and 28S). Genetic analyses were performed to understand major phylogenetic and phylogeographic patterns. Seven species were detected: three Anodonta species (A. anatina, A. cygnea and A. exulcerata), two Unio species (U. mancus and U. elongatulus), Microcondylaea bonellii, and the invasive Sinanodonta woodiana. The presence of three endemic species (A. exulcerata, U. elongatulus and M. bonellii) confirms the importance of the region as a centre of endemism for freshwater mussels. The Apennine Mountains act as an important biogeographic barrier.

2017Journal article

Open access

Phylogeny, phylogeography, and evolution in the Mediterranean region: news from a freshwater mussel (Potomida, Unionida)

Publication . Froufe, Elsa; Prié, Vincent; Faria, João; Ghamizi, Mohamed; Gonçalves, Duarte V.; Gürlek, Mustafa Emre; Karaouzas, Ioannis; Kebapçi, Ümit; Şereflişan, Hülya; Sobral, Carina; Sousa, Ronaldo; Teixeira, Amílcar; Varandas, Simone; Zogaris, Stamatis; Lopes-Lima, Manuel

The Potomida genus (Bivalvia, Unionida) has a Circum-Mediterranean distribution and like other freshwater mussel species, its populations have suffered dramatic declines. Although this genus is currently considered as monotypic, it has a long history of taxonomic revisions and presently many aspects of its systematics and evolutionary history are unclear. We sampled a total of 323 individuals from 39 different sites across the Potomida genus distribution, and sequenced two mitochondrial (16S rDNA and Cytochrome c Oxidase Subunit I) and one nuclear (28S rDNA) genes to clarify its phylogeny and phylogeographic history. Our results show that the genus includes two well-supported clades, one comprising solely the western Mediterranean species Potomida littoralis, and the other including two eastern Mediterranean species, the Greek endemic P. acarnanica and the Anatolian and Middle Eastern P. semirugata. We suggest that Potomida started radiating during the upper Miocene, and that both vicariance and dispersal events shaped the diversification and distribution of the genus along the Mediterranean region. P. littoralis is further divided in two mitochondrial lineages, one restricted to Europe and the other occurring mostly in North Africa. Moreover, some European basins present both lineages in sympatry. The conservation status of the three recognized species should be reevaluated, particularly P. acarnanica, since it is restricted to two Greek river basins presenting a high risk of extinction. Overall, our results clarify some important gaps in knowledge concerning the phylogeny, phylogeography and evolution of the Potomida genus in the Mediterranean region with important taxonomical, ecological and conservational implications.

2016Journal article

Open access

Expansion and systematics redefinition of the most threatened freshwater mussel family, the Margaritiferidae

Publication . Lopes-Lima, Manuel; Bolotov, Ivan N.; Do, Van Tu; Aldridge, David C.; Fonseca, Miguel M.; Gan, Han Ming; Gofarov, Mikhail Y.; Kondakov, Alexander V.; Prié, Vincent; Sousa, Ronaldo; Varandas, Simone; Vikhrev, Ilya V.; Teixeira, Amílcar; Wu, Rui Wen; Wu, Xiaoping; Zieritz, Alexandra; Froufe, Elsa; Bogan, Arthur E.

Two Unionida (freshwater mussel) families are present in the Northern Hemisphere; the Margaritiferidae, representing the most threatened of unionid families, and the Unionidae, which include several genera of unresolved taxonomic placement. The recent reassignment of the poorly studied Lamprotula rochechouartii from the Unionidae to the Margaritiferidae motivated a new search for other potential species of margaritiferids from members of Gibbosula and Lamprotula. Based on molecular and morphological analyses conducted on newly collected specimens from Vietnam, we here assign Gibbosula crassa to the Margaritiferidae. Additionally, we reanalyzed all diagnostic characteristics of the Margaritiferidae and examined museum specimens of Lamprotula andGibbosula.As a result, two additional speciesarealsomovedtotheMargaritiferidae, i.e.Gibbosula confragosa and Gibbosula polysticta. We performed a robust ﬁve marker phylogeny with all available margaritiferid species and discuss the taxonomy within the family. The present phylogeny reveals the division of Margaritiferidae into four ancient clades with distinct morphological, biogeographical and ecological characteristics that justify the division of the Margaritiferidae into two subfamilies (Gibbosulinae and Margaritiferinae) and four genera (Gibbosula, Cumberlandia, Margaritifera, and Pseudunio). The systematics of the Margaritiferidae family is redeﬁned as well as their distribution, potential origin and main biogeographic patterns.

2018Journal article

Open access