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| Onchidella (Hoffmannola) hansi (Ev. Marcus and Er. Marcus, 1967), Sinaloa, Mexico, photo by Q. Y. Abadia-Chanona and O. H. Avila-Poveda; Peronina tenera (Stoliczka, 1869), Pulau Burung, Malaysia; Onchidium typhae Buchannan, 1800, Andaman Islands, India; Marmaronchis vaigiensis (Quoy & Gaimard, 1825), Gilimanuk, Bali, Indonesia; Platevindex coriaceus (Semper, 1880), Mabini, Bohol, Philippines; Semperoncis cf. montana (Plate, 1893), Mt. Palali, Luzon, Philippines, at around 1400 m altitude, photo by R. Lücking; Laspionchis boucheti Dayrat & Goulding, 2019, 39 mm long, Can Gio, Vietnam; Paromoionchis tumidus (Semper, 1880), Calatagan, Batangas, Philippines; Wallaconchis sinanui Goulding & Dayrat, 2018, Lateri, Ambon, Indonesia; Melayonchis eloisae Dayrat, 2017, Pasir Park, Singapore; Alionchis jailoloensis Goulding & Dayrat 2018, Kao, Halmahera, Indonesia; Peronia peronii (Cuvier, 1804), Mahebourg waterfront, Mauritius. in Goulding, Khalil, Tan, et al., 2022. |
Highlights:
• A global molecular phylogeny of onchidiid slugs is reconstructed.
• The common ancestor of onchidiid slugs likely lived in the rocky intertidal.
• Onchidiids transitioned into new habitats in mangrove forests during the Miocene.
• Diversification is the result of allopatric and sympatric (ecological) speciation.
Abstract
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 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 provides the first evidence that the rectal gland of onchidiids is an adaptation to high intertidal and terrestrial habitats.
Keywords: Biogeography, divergence time, ecological speciation, habitat transition, mangroves, rocky intertidal
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| Photos from top to bottom are Onchidella nigricans (Quoy and Gaimard, 1832), 15 mm long, New South Wales, Australia; Onchidella (Hoffmannola) hansi (Ev. Marcus and Er. Marcus, 1967), 40 mm long, Sinaloa, Mexico, photo by Quetzalli Yasu Abadia-Chanona and Omar Hernando Avila-Poveda; France; Peronina tenera (Stoliczka, 1869), 36 mm long, Pulau Burung, Malaysia; Onchidium typhae Buchannan, 1800, 40 mm long, Andaman Islands, India; Melayonchis eloisae Dayrat, 2017, 15 mm long, Pasir Park, Singapore; Marmaronchis vaigiensis (Quoy & Gaimard, 1825), 23 mm long, Gilimanuk, Bali, Indonesia; Platevindex coriaceus (Semper, 1880), 37 mm long, Mabini, Bohol, Philippines; Semperoncis cf. montana (Plate, 1893), Mt. Palali, Luzon, Philippines, at around 1400 m altitude, photo by Robert Lücking; Onchidina australis (Semper, 1880), 45 mm long, Blackman Park, New South Wales, Australia; Laspionchis boucheti Dayrat & Goulding, 2019, 39 mm long, Can Gio, Vietnam; Paromoionchis tumidus (Semper, 1880), 31 mm long, Calatagan, Batangas, Philippines; Wallaconchis sinanui Goulding & Dayrat, 2018, 9 mm long, Lateri, Ambon, Indonesia; Alionchis jailoloensis Goulding & Dayrat 2018, 48 mm long, Kao, Halmahera, Indonesia; Peronia peronii (Cuvier, 1804), 110 mm long, Mahebourg waterfront, Mauritius. |
Tricia C. Goulding, Munawar Khalil, Shau Hwai Tan, Rebecca A. Cumming and Benoît Dayrat. 2022. Global Diversification and Evolutionary History of Onchidiid Slugs (Gastropoda, Pulmonata). Molecular Phylogenetics and Evolution. In Press, 107360. DOI: 10.1016/j.ympev.2021.107360
