Knowledge of the biogeography of marine taxa has lagged significantly behind terrestrial ecosystems. A hotspot of marine biodiversity associated with coral reefs is known in the Coral Triangle of the Indo-West Pacific, but until now there was little data with which to evaluate broad patterns of species richness in the coastal fauna of ecosystems other than coral reefs. This data is critically needed for fauna with low functional redundancy like that of mangroves, that are vulnerable to habitat loss and rising sea levels. Here we show that the diversity of mangrove fauna is characterized by two distinct hotspots in the Indo-West Pacific, associated with two habitat types: fringe mangroves in the Coral Triangle, and riverine mangroves in the Strait of Malacca, between the west coast of Peninsular Malaysia and Sumatra. This finding, based on a family of slugs of which the systematics has been completely revised, illustrates an unexpected biogeographic pattern that emerged only after this taxon was studied intensively. Most organisms that live in the mangrove forests of Southeast Asia remain poorly known both taxonomically and ecologically, and the hotspot of diversity of onchidiid slugs in the riverine mangroves of the Strait of Malacca indicates that further biodiversity studies are needed to support effective conservation of mangrove biodiversity.
A new genus of onchidiid slugs, Wallaconchis Goulding & Dayrat, gen. n., is described, including ten species. Five species were previously described but known only from the type material: Wallaconchis ater (Lesson, 1830), W. graniferum (Semper, 1880), W. nangkauriense (Plate, 1893), W. buetschlii (Stantschinsky, 1907), and W. gracile (Stantschinsky, 1907), all of which were originally classified in Onchidium Buchannan, 1800. Many new records are provided for these five species, which greatly expand their known geographic distributions. Five species are new: Wallaconchis achleitneri Goulding, sp. n., W. comendadori Goulding & Dayrat, sp. n., W. melanesiensis Goulding & Dayrat, sp. n., W. sinanui Goulding & Dayrat, sp. n., and W. uncinus Goulding & Dayrat, sp. n. Nine of the ten Wallaconchis species are found in the Coral Triangle (eastern Indonesia and the Philippines). Sympatry is high, with up to six species found on the island of Bohol (Philippines) and eight species overlapping in northern Sulawesi (Indonesia). Wallaconchis is distinguished from other onchidiids by its bright dorsal colors (red, yellow, orange) but those are extremely variable and not useful for specific identification. Internally, the reproductive system can be used to identify all Wallaconchis species. The copulatory organs of Wallaconchis species are especially diverse compared to other onchidiid genera, and the possible role of reproductive incompatibility in species diversification is discussed. All specimens examined were freshly collected for the purpose of a worldwide revision of the Onchidiidae Rafinesque, 1815. The species are well delineated using DNA sequences and comparative anatomy. Mitochondrial DNA analysis yields thirteen molecular units separated by a large barcode gap, while nuclear DNA yields nine units. By integrating nuclear DNA and mitochondrial DNA with morphology, ten species are recognized. The natural history of each species (e.g., the microhabitat where they are found) is also documented. Nomenclature is addressed thoroughly (the types of all onchidiid species were examined, lectotypes were designated when needed, nomina dubia are discussed). Morphological characters, transitions to new microhabitats, and diversification processes are discussed in the context of a robust molecular phylogeny.
A new species, Onchidium melakense Dayrat & Goulding, sp. nov., is described, bringing the total to four known species in the genus Onchidium Buchannan, 1800. Onchidium melakense is a rare species with only nine individuals found at three mangrove sites in the Andaman Islands and the Strait of Malacca (western Peninsular Malaysia and eastern Sumatra). The new species is delineated based on mitochondrial (COI and 16S) and nuclear (ITS2 and 28S) DNA sequences as well as comparative anatomy. Each Onchidium species is characterized by a distinct color and can easily be identified in the field, even in the Strait of Malacca where there are three sympatric Onchidium species. An identification key is provided. In addition, Onchidium stuxbergi (Westerlund, 1883) is recorded for the first time from eastern Sumatra, and Onchidium pallidipes Tapparone-Canefri, 1889, of which the type material is described and illustrated here, is regarded as a new junior synonym of O. stuxbergi.
As part of an ongoing effort to revise the taxonomy of air-breathing, marine, onchidiid slugs, a new genus, Laspionchis Dayrat & Goulding, gen. nov., is described from the mangroves of South-East Asia. It includes two new species, Laspionchis boucheti Dayrat & Goulding, sp. nov., and Laspionchis bourkei Dayrat & Goulding, sp. nov., both distributed from the Malacca Strait to the Philippines and Australia. This study is based on extensive field work in South-East Asia, comparative anatomy, and both mitochondrial (COI and 16S) and nuclear (ITS2 and 28S) DNA sequences. The two new species are found in the same habitat (mud surface in mangrove forests) and are externally cryptic but are distinct anatomically. Both species are also strongly supported by DNA sequences. Three cryptic, least-inclusive, reciprocally-monophyletic units within Laspionchis bourkei are regarded as subspecies: L. bourkei bourkei Dayrat & Goulding, ssp. nov., L. bourkei lateriensis Dayrat & Goulding, ssp. nov., and L. bourkei matangensis Dayrat & Goulding, ssp. nov. The present contribution shows again that species delineation is greatly enhanced by considering comparative anatomy and nuclear DNA sequences in addition to mitochondrial DNA sequences, and that thorough taxonomic revisions are the best and most efficient path to accurate biodiversity knowledge.
Many marine species are specialized to specific parts of a habitat. In a mangrove forest, for instance, species may be restricted to the mud surface, the roots and trunks of mangrove trees, or rotting logs, which can be regarded as distinct microhabitats. Shifts to new microhabitats may be an important driver of sympatric speciation. However, the evolutionary history of these shifts is still poorly understood in most groups of marine organisms, because it requires a well-supported phylogeny with relatively complete taxon sampling. Onchidiid slugs are an ideal case study for the evolutionary history of habitat and microhabitat shifts because onchidiid species are specialized to different tidal zones and microhabitats in mangrove forests and rocky shores, and the taxonomy of the family in the Indo-West Pacific has been recently revised in a series of monographs. Here, DNA sequences for onchidiid species from the North and East Pacific, the Caribbean, and the Atlantic are used to reconstruct phylogenetic relationships among Onchidella species, and are combined with new data for Indo-West Pacific species to reconstruct a global phylogeny of the family. The phylogenetic relationships of onchidiid slugs are reconstructed based on three mitochondrial markers (COI, 12S, 16S) and three nuclear markers (28S, ITS2, H3) and nearly complete taxon sampling (all 13 genera and 62 of the 67 species). The highly-supported phylogeny presented here suggests that ancestral onchidiids most likely lived in the rocky intertidal, and that a lineage restricted to the tropical Indo-West Pacific colonized new habitats, including mudflats, mangrove forests, and high-elevation rainforests. Many onchidiid species in the Indo-West Pacific diverged during the Miocene, around the same time that a high diversity of mangrove plants appears in the fossil record, while divergence among Onchidella species occurred earlier, likely beginning in the Eocene. It is demonstrated that ecological specialization to microhabitats underlies the divergence between onchidiid genera, as well as the diversification through sympatric speciation in the genera Wallaconchis and Platevindex. The geographic distributions of onchidiid species also indicate that allopatric speciation played a key role in the diversification of several genera, especially Onchidella and Peronia. The evolutionary history of several morphological traits (penial gland, rectal gland, dorsal eyes, intestinal loops) is examined in relation to habitat and microhabitat evolutionary transitions and suggests that the rectal gland of onchidiids is an adaptation to high intertidal and terrestrial habitats.
The genus Peronia Fleming, 1822 includes all the onchidiid slugs with dorsal gills. Its taxonomy is revised for the first time based on a large collection of fresh material from the entire Indo-West Pacific, from South Africa to Hawaii. Nine species are supported by mitochondrial (COI and 16S) and nuclear (ITS2 and 28S) sequences as well as comparative anatomy. All types available were examined and the nomenclatural status of each existing name in the genus is addressed. Of 31 Peronia species-group names available, 27 are regarded as invalid (twenty-one synonyms, sixteen of which are new, five nomina dubia, and one homonym), and four as valid: Peronia peronii (Cuvier, 1804), Peronia verruculata (Cuvier, 1830), Peronia platei (Hoffmann, 1928), and Peronia madagascariensis (Labbé, 1934a). Five new species names are created: P. griffithsi Dayrat & Goulding, sp. nov., P. okinawensis Dayrat & Goulding, sp. nov., P. setoensis Dayrat & Goulding, sp. nov., P. sydneyensis Dayrat & Goulding, sp. nov., and P. willani Dayrat & Goulding, sp. nov.Peronia species are cryptic externally but can be distinguished using internal characters, with the exception of P. platei and P. setoensis. The anatomy of most species is described in detail here for the first time. All the secondary literature is commented on and historical specimens from museum collections were also examined to better establish species distributions. The genus Peronia includes two species that are widespread across the Indo-West Pacific (P. verruculata and P. peronii) as well as endemic species: P. okinawensis and P. setoensis are endemic to Japan, and P. willani is endemic to Northern Territory, Australia. Many new geographical records are provided, as well as a key to the species using morphological traits.