Tethyan Changes Shaped Aquatic Diversification: Aquatic

Biol. Rev. (2018), 93, pp. 874–896. 874 doi: 10.1111/brv.12376 Tethyan changes shaped aquatic diversiﬁcation

Zhonge Hou1 and Shuqiang Li1,2,∗ 1Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China 2Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences, Yezin, Nay Pyi Taw 05282, Myanmar

ABSTRACT

The Tethys Ocean existed between the continents of Gondwana and Laurasia from the Triassic to the Pliocene. Analyses of multiple biogeographic and phylogenetic histories reveal that the subsequent breakup of the Tethys greatly influenced the distributions of many species. The ancestral Tethyan realm broke into five biogeographic provinces, including the present-day East Pacific, West Atlantic, East Atlantic, Mediterranean Sea, and Indo-West Pacific. Palaeogeographic maps illustrate the Mesozoic Atlantic opening, the Cenozoic closure of the Tethys, the Messinian Salinity Crisis, the mid-Miocene closure of the Central American Seaway, and Quaternary geological changes. Further, we consider Cenozoic sea-level changes and the formation of freshwater habitats. These reconstructions allow assessment of patterns of aquatic diversification for marine and freshwater animals, and comparison of vicariance and dispersal processes. Estimated divergence times indicate that fragmentation of the Tethys was responsible for the vicariant speciation of aquatic animals because these dates are consistent with associated tectonic events. The opening of the Atlantic Ocean during the Cretaceous is responsible for the earliest isolation between the West and East Atlantic. The mid-Miocene closure of the Tethys, which blocked global equatorial currents, appears to have isolated the Atlantic/Mediterranean Sea and Indo-West Pacific. Finally, formation of the Isthmus of Panama isolated East Pacific and West Atlantic marine organisms. Dispersals related to the Messinian Salinity Crisis and Quaternary sea-level changes influenced population structuring. Tethyan changes affected marine habitats, created new freshwater habitats, inland caves and ancient lakes along the Alps and Himalayas, and influenced anchialine caves at the edge of the ancient sea. The extensive new habitats provided opportunities for colonisation and rapid diversification. Future work should focus on testing the biological impact of the series of Tethyan changes.

Key words: phylogenetics, biogeography, Tibetan uplift, climatic oscillations, vicariance, dispersal, habitat shift.

CONTENTS I. Introduction ...... 875 II. History of diversification study in the Tethyan region ...... 876 (1) Data selection and abbreviations ...... 876 (2) Geological advances promoted diversification studies ...... 876 (3) Vicariant versus dispersal hypotheses ...... 877 III. Geological reconstructions of the Tethys ...... 879 (1) Mesozoic Atlantic opening (110 to 65 Ma) ...... 879 (2) Cenozoic closure of the Tethys (50–12 Ma) ...... 879 (3) Messinian Salinity Crisis (5.96–5.33 Ma) ...... 880 (4) Middle Miocene to Pliocene closure of the Central American Seaway (15–3 Ma) ...... 880 (5) Quaternary geological changes (3 Ma to present) ...... 880 IV. Palaeoclimate reconstructions ...... 881 (1) Cenozoic sea-level changes and formation of freshwater habitats ...... 881 (2) Cave, anchialine habitat and lake formation ...... 881 V. Diversification patterns in the Tethyan region ...... 882

* Address for correspondence (Tel: +86 10 64807216; E-mail: [email protected])

(1) Open Tethys Ocean for marine species and Atlantic barrier ...... 882 (2) Tethyan closure drove vicariant speciation ...... 882 (3) Recolonisation of the Mediterranean Basin after the MSC ...... 883 (4) Contrasting patterns caused by the closure of the Central American Seaway ...... 885 (5) Species range expansion during the Quaternary climatic oscillations ...... 886 VI. Habitat shift from marine to freshwater ...... 886 (1) Marine extinction ...... 886 (2) Freshwater occupation ...... 887 (3) Radiations in caves, anchialine habitats and lakes ...... 887 VII. Vicariance and dispersal comparison ...... 889 VIII. Future directions ...... 890 IX. Conclusions ...... 890 X. Acknowledgements ...... 890 XI. References ...... 891 XII. Supporting Information ...... 896

I. INTRODUCTION & Piller, 2007). Today, such hotspots still occur in regions once covered by the ancient Tethys, including the Caribbean The Tethys Ocean of the equatorial region has a history islands, Mediterranean, eastern Himalayas, and Indo-West lasting 250 million years (Stow, 2010). It isolated Gondwana Pacific islands. Many groups of marine fish have their greatest and Laurasia and covered parts of the current Caribbean diversity in these areas (Huyse, Van Houdt & Volckaert, region, Atlantic Ocean, Mediterranean Sea, and the 2004; Kulbicki et al., 2013; Dornburg et al., 2015; Cowman Indo-West Pacific region (Fig. 1; Van Syoc et al., 2010). et al., 2017) and shallow marine margins around the ancient During the Cretaceous, the Atlantic Ocean opened as Tethys have a high diversity of benthic crustaceans and Gondwana and Laurasia broke up (Floeter et al., 2008; gastropods (Frey & Vermeij, 2008; Hou, Sket & Li, 2014). Greiner & Neugebauer, 2014). The Eocene collision of The diversity of fossils and extant species relates to the Eurasia and Africa/India drove the orogenesis of the Alps complex history of the Tethyan region. Recent syntheses of and Himalayas (Fig. 2). This led to the westward retreat of the fossil record and molecular evidence have identified the the Tethys from present-day Tibet and the Pamir Mountains role the Tethys played in the spatial and temporal dynamics (Bosboom et al., 2011, 2014; Carrapa et al., 2015). During of today’s biodiversity (Meynard et al., 2012; Cowman & the Miocene, the Arabian Plate pushed northward and Bellwood, 2013a,b; Dornburg et al., 2015). An understanding closed the Tethys Ocean between the Atlantic Ocean and of the drivers of this diversification may help to guide the Indo-West Pacific region (Adams, Gentry & Whybrow, conservation initiatives and facilitate forecasts on impacts 1983; Steininger & Rogl,¨ 1984; Rogl,¨ 1998). The Tethys-like of future climate changes. system vanished 5.5 Ma during the Messinian Salinity Crisis Fragmentation of the Tethys Ocean is the driver of due to uplifting of Gibraltar coupled with a drop in sea disjunct, endemic and relict distributions of Tethyan lineages level. By the Pliocene, the final closure of the Central (Ozawa et al., 2009; Hou et al., 2011). Considerably expanded American Seaway divided the ancient Tethys Ocean into five regions suggest that Tethyan evolution benefited organisms provinces (Fig. 1): East Pacific, West Atlantic, East Atlantic, such as amphipod crustaceans, whose distributions extend Mediterranean Sea, and Indo-West Pacific. The Tethys from ancient Tethys to the rivers of East Asia (Hou et al., Ocean experienced a succession of complex geodynamic 2011; Mamos et al., 2016). By contrast, the changes were events. This tectonic activity may be a major driving force deleterious for others, as relict distributions suggest, the on the origin, diversification, maintenance, and extinction of best-known case being the restriction of Remipedia to marine animals, including the shaping of modern patterns anchialine caves in the ancient Tethyan margin (Hoenemann of species richness in the former Tethyan region and the et al., 2013; Hou et al., 2014). Some marine fauna went modern Indo-West Pacific province (Stow, 2010; Hou et al., extinct, such as marine molluscs in the Paratethyan basin 2011; Cowman & Bellwood, 2013a,b; Mamos et al., 2016). following closure of the Tethys (Harzhauser & Piller, 2007), The Tethys Ocean once dominated the Earth and played the Mediterranean extinction crisis among fish during host to a large number of marine and continental freshwater the Messinian Salinity Crisis (Meynard et al., 2012) and species (Maisey, 2012). Fossils and extant reef fishes reveal Caribbean reef extinction after closure of the Central a shift in biodiversity from the western Tethyan region America Seaway (Budd, 2000; Leigh, O’Dea & Vermeij, (Mediterranean) to the Indo-West Pacific during the past 2014). 50 million years (Renema et al., 2008; Leprieur et al., 2016). Geological, fossil and molecular evidence has advanced For example, the diversity of fossil molluscs centred at the explorations into the evolution of Tethyan taxa. Herein, western Tethyan region during the Oligocene and then we offer a palaeogeographic reconstruction of the Tethyan moved to the Indo-West Pacific in the Miocene (Harzhauser region and discuss the impact of Tethyan evolution on

Fig. 1. Present coastal regions once geologically linked as part of the ancient Tethys Ocean (modified from Van Syoc et al., 2010) and Paratethys basin (modified from Stow, 2010). The ancestral Tethyan realm broke into five present-day biogeographic provinces: East Pacific (EP), West Atlantic (WA), East Atlantic (EA), Mediterranean Sea (MS) and Indo-West Pacific (IWP). These provinces are defined by land bridges or deep and wide marine barriers following Cowman & Bellwood (2013b) and Dornburg et al. (2015): the Isthmus of Panama separating the EP from WA, the central Atlantic barrier separating the WA from EA, the Strait of Gibraltar separating the EA from MS, the Arabian plate separating the MS from IWP, and the central Pacific barrier separating the IWP from EP. patterns of diversification. Using case studies, we illustrate Indo-West Pacific. Abbreviations for temporal events include the effects of the opening and closure of the Tethys Ocean, the following: Ma, million years ago; MSC, Messinian of the Central American Seaway and of Quaternary climatic Salinity Crisis; TTE, Terminal Tethyan Event; LGM, Last oscillations on diversification across taxonomic scales ranging Glacial Maximum. from family to species. Moreover, we explore habitat shifts from marine to new niches, including freshwater, caves and (2) Geological advances promoted diversification anchialine habitats. Finally, we suggest future directions for studies testing hypotheses on the drivers of large-scale patterns, as well as for assessing species’ adaptations to environmental Austrian geologist Eduard Suess proposed that an inland changes. ocean once separated Laurasia and Gondwana, based on similar fossils occurring in Europe and Africa. He named the inland ocean ‘Tethys’ after a goddess in Greek mythology (Suess, 1893). Subsequently, plate tectonics provided the II. HISTORY OF DIVERSIFICATION STUDY IN THE TETHYAN REGION basis for the Tethys Ocean being a vanishing water body along sutures of the Pangean embayment (Sengor, 1992; Sorkhabi, 1995). (1) Data selection and abbreviations From the 1980s, a surge in interest on Tethyan geology led We conducted a literature search on ISI Web of Knowledge to the reconstruction of the region’s evolutionary history and database by entering key words ‘Teth*’ AND ‘diversifica- a set of palaeogeographic and palaeoenvironmental maps tion’. This search, which was performed on April 18, 2017, (Rogl,¨ 1998; Dercourt et al., 2000). These maps encompass a obtained 222 records. The reading of abstracts for these time span of 300 Ma and detailed explanatory notes accom- records for ‘marine’ or ‘freshwater’ narrowed the list to 108 panied each map. Several studies focused on restricted time articles. We then obtained full-text versions of these articles spans and local regions (Gaetani, 2003; Gaetani, Dercourt and expanded our search by tracing their citations. In total, & Vrielynck, 2003). Recently, geological research on the 246 papers were collected, from which we extracted infor- eastern Tethys and Tibetan Plateau resulted in more reliable mation on geology, palaeontology and evolutionary biology. and detailed tectonic models (Royden, Burchfiel & Van der The following abbreviations for geographic areas are Hilst, 2008; Bosboom et al., 2011; Favre et al., 2015). These used throughout the text: EP, East Pacific; WA, West geological advances provide methodological refinements Atlantic; EA, East Atlantic; MS, Mediterranean Sea; IWP, that explain the current patterns of biodiversity.

Fig. 2. Cenozoic reconstructions of land and sea indicating the changes to the Tethys Ocean. Maps modiﬁed from Popov et al. (2004) and Ron Blakey, NAU Geology (http://jan.ucc.nau.edu/∼rcb7/globaltext2.html). (A) ca.65Ma;(B)ca.50Ma;(C)ca.35Ma; (D) ca.20Ma;(E)ca. 5.7 Ma; and (F) Present.

Central to Darwin’s theory on the origin of species, et al., 2015). Global patterns of biodiversity have been biologists strive to explain global patterns of diversification identified over space and time, which require the integration (Rabosky, 2013). A large part of the biodiverse Tethys of macroecological and macroevolutionary perspectives included tropical marine environments (Cuttelod et al., 2008). (Meredith et al., 2011; Price et al., 2014; Heim et al., 2015). Before the 1990s, biodiversity research always related to local geography and focused on fossils associated with the ancestral Tethys and the descriptions of extant endemic species (3) Vicariant versus dispersal hypotheses (Tortonese, 1985; Geary, 1990). Subsequently, geological In comparison to continental environments, marine envi- advances have accelerated biodiversity research enormously, ronments appear to lack obvious barriers to gene flow; most including explorations into the relationships between geology marine species with high dispersal capabilities are expected and biology (Bellwood, Van Herwerden & Konow, 2004; to exist at a larger geographical scale (Zitari-Chatti et al., Ozawa et al., 2009). In the last decade, the explosive growth 2009). Nevertheless, broad-scale molecular surveys reveal of molecular data generated by next-generation sequencing geographically structured Tethyan lineages (Bauza-Ribot` has initiated a new wave of investigations (Malinsky et al., 2012; Botello et al., 2013; Leprieur et al., 2015). This

Fig. 3. Dated area cladograms outlining the vicariance hypothesis of Tethyan biogeography. EP, East Pacific; WA, West Atlantic; EA, East Atlantic; MS, Mediterranean Sea; IWP, Indo-West Pacific. (A) Extension of the Atlantic Ocean separated the EA from WA around 65 Ma; (B) Tethyan closure in the Middle Miocene drove the separation of Atlantic and IWP marine organisms; (C) closure of the Central American Seaway induced divergence between EP and WA species. Maps modified from Popov et al. (2004) and Ron Blakey, NAU Geology (http://jan.ucc.nau.edu/∼rcb7/globaltext2.html). Dashed line denotes the Atlantic deep-sea barrier to gene flow. Solid lines are land-bridge barriers. results in the formulation of two contrasting hypotheses et al., 2008), mainly in the present-day East Atlantic and that explain how species diversification might proceed Mediterranean basin. Therefore, the western Tethyan region across landmasses. The vicariant hypothesis states that (EA + MS) was recognised as a source region (Dornburg the progressive Tethyan fragmentation reduced genetic et al., 2015), and permitted bidirectional dispersals. Drowned connectivity, and resulted in allopatric diversification (Fig. 3). archipelagos and seamounts in the central Atlantic Ocean The opening of the Atlantic Ocean during the Cretaceous served as land bridges for east to west movement between the caused the earliest isolation between the EP + WA and MS and WA (Fig. 4A; Botello et al., 2013). After closure of EA + MS + IWP (Fig. 3A; Anger, 2013). The closure of the Tethys, dispersal between the Atlantic and Indo-Pacific the Tethys Ocean in the early to middle Miocene formed occurred via southern Africa during interglacial periods a significant vicariant event between the EA + MS and (Fig. 4C; Rocha et al., 2005; Bowen et al., 2006). South Pacific IWP (Fig. 3B; Bellwood et al., 2004). Finally, closure of archipelagos probably facilitated some migration between the Central American Seaway isolated the EP and WA the IWP and EP; they allowed IWP sharks to disperse east- (Fig. 3C; Leigh et al., 2014). This series of vicariant events ward and colonise remote oceanic islands (Fig. 4B; Duncan might not be contained in one phylogenetic history, but et al., 2006). However, ocean currents may also play a key sections of this pattern exist in subterranean crustaceans, role in the dispersal of some transpacific reef fishes that have which have low levels of dispersal (Neiber et al., 2011), and long-lived larvae (Lessios & Robertson, 2006; Cowman & shallow-water sharks bound to continental shelves (Schultz Bellwood, 2013b). et al., 2008). Contemporary patterns of biodiversity involve both An alternative hypothesis states that either taxa used vicariance and dispersal processes. Vicariance associates with archipelagos as stepping stones in their open-water dispersal Tethyan fragmentation, and dispersal after the closure of the to allow gene flow, or ocean currents moved their pelagic Tethys Ocean associates with recent lineages. Vicariance larvae (Fig. 4). During the Paleocene, the East Pacific and and dispersal are not mutually exclusive. Several studies Atlantic oceans were linked to the Indo-Pacific by dispersal have highlighted the synergy between these processes through the Tethys Ocean. Fossils reveal that Eocene global (Floeter et al., 2008; Burridge et al., 2012; Cowman & biodiversity peaked in the western Tethyan realm (Renema Bellwood, 2013b).

Fig. 4. Dispersal hypothesis and phylogenetic predictions associated with different dispersal routes. EP, East Pacific; WA, West Atlantic; EA, East Atlantic; MS, Mediterranean Sea; IWP, Indo-West Pacific. Marine biodiversity hotspots shifted from the western Tethyanregion(EA+ MS) to the modern IWP (Renema et al., 2008). Thus, the western Tethyan region was a source region. (A) Westward dispersal from the MS + EA through the Atlantic Ocean driven either by ocean currents or ancient drowned archipelagos as stepping stones (Bauza-Ribot` et al., 2012); (B) eastward dispersal from the EA + MS to IWP and even EP by currents or through archipelagos of the South Pacific as stepping stones (Duncan et al., 2006); (C) dispersal via southern Africa during the interglacial period includes active dispersal from the Atlantic to the IWP (Bourjea et al., 2007) and passive drift by currents from the IWP to the Atlantic (Rocha et al., 2005). Sizes of the ovals reflect haplotype frequencies. One phylogenetic history might not reflect the full series of dispersal events.

III. GEOLOGICAL RECONSTRUCTIONS OF THE (Bortolotti & Principi, 2005). The gradual mid-Cretaceous TETHYS separation of North America from Laurasia and the breakup of Gondwana about 110–84 Ma opened the Atlantic Ocean, (1) Mesozoic Atlantic opening (110 to 65 Ma) the deep-water basin between Europe and the Americas (Floeter et al., 2008; Greiner & Neugebauer, 2014). The Knowledge of the geological history of the Tethys is essential spreading of the Atlantic constitutes an oceanic barrier due for understanding contemporary patterns of diversity. The to its great depth and width (Fig. 2A; Piovesan, Ballent & geography around the Tethys changed markedly during Fauth, 2012). the Cretaceous and Cenozoic. During the Cretaceous, the Tethys widened signiﬁcantly when high sea levels inundated nearly 40% of continental southern North America, southern (2) Cenozoic closure of the Tethys (50–12 Ma) Europe, southern Asia, northern South America and Major tectonic events began in the Eocene Epoch. In northern Africa (Harzhauser et al., 2007; Stow, 2010). the Early Eocene (about 50 Ma), India moved northward Cenozoic continental collisions caused the Tethys to shrink ∼2000 km from its original position, and collided with gradually and eventually close completely. Plate movements Asia (Fig. 2B). After this collision, in the Late Eocene formed the Alps and Himalayas (Rogl,¨ 1999; Meulenkamp & intracontinental convergence closed the Tethys north of the Sissingh, 2003). These geological events drove the formation Indian Plate and deformation continued with uplifting of the of biological hotspots (Renema et al., 2008). Tibetan Plateau (Royden et al., 2008; Van Hinsbergen et al., Change in the Tethys began with the Triassic break 2012). Also during this time, Africa converged with Europe up of supercontinent Pangea into Laurasia and Gondwana and formed an active alpine mountain belt along the southern

Biological Reviews 93 (2018) 874–896 © 2017 Cambridge Philosophical Society 880 Zhonge Hou and Shuqiang Li border of Eurasia (Rogl,¨ 1998). At the Eocene–Oligocene fauna (Neraudeau,´ 1994; Harzhauser et al., 2007), but boundary, the southern Mediterranean was created at brackish to freshwater lake ‘Lago-Mare’ and its confluents the western end of the Tethys and an intercontinental promoted some species to adapt to a freshwater environment Paratethys arose north of the tectonic belt (Fig. 2C). The (Penzo et al., 1998; Roveri et al., 2014). The MSC finished Paratethys once extended east to Tajikistan and covered when Atlantic waters refilled the Mediterranean, primarily the Tarim Basin (Sun & Jiang, 2013; Carrapa et al., 2015), driven by tectonic subsidence at the Gibraltar sill, flow connecting to the Arctic Ocean by the Turgai Strait and incision and sea-level rise (Garcia-Castellanos et al., 2009). linking to the North Sea via the Danish–Polish trough The opening of the Gibraltar Strait strongly influenced (Bosboom et al., 2011). During the Oligocene, the Tethys Mediterranean–Atlantic water exchange, forming marine retreated intensively and continentalisation increased in corridors for recolonisation of the Mediterranean by Atlantic central and western Europe, coinciding with the strong organisms (Perez-Portela,´ Almada & Turon, 2013). change in sea level (Popov et al., 2004; Miller et al., 2005). Concurrent with the MSC, Australia continued to move The connection between Indo-Pacific and Atlantic oceans north, leading to a complex of uplift, subsidence, contraction had been narrow throughout most of the Oligocene because and extension in Southeast Asia. As a result, nearly all of continentalisation, which reduced the exchange of deep present islands of the Indo-Australian Archipelago became and intermediate waters (Rogl,¨ 1999). subaerial and the Australian continental margin extended In the Early Miocene (24–20 Ma), the counter-clockwise (Lohman et al., 2011; Rix et al., 2015). The extensive creation rotation of the Africa-Arabian block drove the opening of new islands and shallow seas provided new opportunities of the Red Sea (DiBattista et al., 2013), and the collision for diversification in the IWP (Renema et al., 2008). between the Arabian Plate and Eurasia formed an elongated island chain (Fig. 2D; Rogl,¨ 1998). By the Middle Miocene (4) Middle Miocene to Pliocene closure of the (18–12 Ma), the Terminal Tethyan Event (TTE) gradually Central American Seaway (15–3 Ma) closed the Tethys Ocean between the Mediterranean and Indian Ocean, and a land bridge between Eurasia and Africa The rise of the Central American Isthmus began when came into existence (Adams et al., 1983; Steininger & Rogl,¨ the Central American arc collided with South America 1984). This closure caused a blockage of exchange between over 12 Ma, causing a mid-Miocene narrowing and shal- the Atlantic and Indian Ocean. Meanwhile, the Australian lowing of the seaway between the Americas (Leigh et al., Plate moved northward with Southeast Asia approximately 2014; Sepulchre et al., 2014). Extension of the Isthmus 23 Ma, which contributed to the emergence of islands along finally closed the Central American Seaway during the Wallace’s Line. This restricted the interchange between Late Pliocene (∼3.5 Ma) (Lessios, 2008; Leigh et al., 2014), the Pacific and Indian Ocean (Lohman et al., 2011). The separating the East Pacific and Atlantic (Fig. 2F). How- closure of the Tethys Ocean and the restriction of the ever, the timing of the actual closure remains controversial Indo-Pacific Seaway affected the global equatorial current (Farris et al., 2011; Montes et al., 2012b). A mid-Miocene and enhanced the disruption between the Atlantic and (15–13 Ma) closure was proposed based on geochronological IWP (Steeman et al., 2009). By contrast, the hydrological and geochemical data (Montes et al., 2015). Recent biological connections around the southern tips of Africa were probably evidence supported an early and complex closure during the too cold for dispersal (Bowen et al., 2006; Cowman & Oligocene–Miocene (Cowman & Bellwood, 2013b;Bacon Bellwood, 2013b), further isolating the tropical faunas of et al., 2015a). This led to questioning whether full closure took the Atlantic and IWP (Malaquias & Reid, 2009). These place at 3.5 Ma or much earlier (Bacon et al., 2015b; Lessios, tectonic events associated with the TTE, in turn, increased 2015; Marko, Eytan & Knowlton, 2015). The past homo- both the shallow-water area and extensive coral reef habitat geneous environment between the East Pacific and Atlantic in the IWP region, providing opportunities for radiation of oceans changed dramatically after the closure and this drove reef-associated organisms (Williams & Duda, 2008; Cowman biological divergence (Lessios, 2008). Formation of the land & Bellwood, 2011; Bellwood, Goatley & Bellwood, 2017). bridge represents a complete, relatively recent barrier for most transisthmian sister-species (Knowlton & Weigt, 1998). (3) Messinian Salinity Crisis (5.96–5.33 Ma) (5) Quaternary geological changes (3 Ma to present) In the Late Miocene (Fig. 2E), tectonic uplift of the Gibraltar arc and global sea-level changes controlled the inflow of Cyclic growth and decay of continental ice sheets typically water required to compensate for the hydrological deficit of define the Quaternary Period and climate and environmen- the Mediterranean (Duggen et al., 2003; Hernandez-Molina´ tal changes characterise it (Weigelt et al., 2016). Glacial cycles et al., 2014), causing the Messinian Salinity Crisis are responsible for the major transgressions and regressions (5.96–5.33 Ma). During the MSC, the Strait of Gibraltar was of the Black and Caspian seas in the ancient Paratethyan closed and the Mediterranean became progressively isolated region (Ryan et al., 2003; Sorokin, 2011). Initial separation of from the Atlantic, triggering widespread salt precipitation the Black and Caspian basins dates to about 3 Ma (Tudryn and a dramatic lowering of sea level due to evaporation et al., 2013). From that time, recurrent transgressions led (Krijgsman et al., 1999; Garcia-Castellanos & Villasenor,˜ to reconnections of the two basins (Hanfling¨ et al., 2009). 2011). The crisis extirpated most of the Mediterranean After the Last Glacial Maximum (LGM) approximately

20000 years ago, boreal glacial lakes drained south to the temperature and variations in sea-floor spreading, also may Caspian Sea through the Volga River. This caused an have produced sea-level fluctuations (Nores, 2004; Miller extensive transgression and the northern margin of the et al., 2005). The sea level rose 70–100 m above present in the Caspian Basin reached to the present middle Volga (Tudryn early Eocene (55–50 Ma), followed by a long-term decrease et al., 2013). Either the Caspian Sea overflowed to the Black of some 50–60 m owing to Eocene–Oligocene Antarctic Sea through the Kuma-Manych Strait (Dolukhanov, Chep- glaciations (Miller et al., 2005; Houben et al., 2012). From the alyga & Lavrentiev, 2010), or ice-marginal lakes provided late Pliocene to Holocene (2.5 Ma to Present), glaciations connections between the Caspian and the Arctic Ocean via induced sea-level changes of 60–120 m (Miller et al., 2005). the ancient Turgai Strait (Vain¨ ol¨ a,¨ Vainio & Palo, 2001). Tethyan regression and transgression linked to these The Black and Caspian seas experienced LGM sea-level global sea-level changes. The interplay between tectonic reductions associated with glacial expansion. These resulted plates and Tethyan retreat altered the extent of subaerial in the separation of the Black Sea from the Mediterranean. land, leading to Central Asian aridification (Rogl,¨ 1998; The Black Sea significantly reduced its size, and riverine Sun & Liu, 2006). During the Paleocene Epoch, the Tethys inflow during glacial retreat decreased its salinity (Ryan stretched west to east from across Southern Europe to Central et al., 2003; Wilson & Veraguth, 2010). The connection Asia (Meulenkamp & Sissingh, 2003). Along with Eocene between the Mediterranean and Black Sea was restored tectonic movements and Tethyan regression, the accretion with rising sea levels some 8000 years ago (Ca´ gatay˘ et al., of landmass formed a prominent new ecosystem ranging 2000; Fouache et al., 2012). The Mediterranean maintained from brackish to freshwater. Marine regression intensified in an unbroken connection with the Atlantic Ocean during the Miocene, resulting in an arid environment for the vast the Quaternary, which assured continuous faunal exchange interior of Asia (Popov et al., 2004; Sun & Liu, 2006; Sun & (Bouchet & Taviani, 1992; Maggs et al., 2008). Pleistocene Jiang, 2013). Shrinkage of the ocean led to the extinction of glaciations modified global drainage systems dramatically. In Tethyan marine assemblages (Vasiliev et al., 2010; Lukeneder turn, this substantially impacted species population structure et al., 2011), and yet the increase in freshwater area afforded (Burridge, Craw & Waters, 2006; Daniels et al., 2015). new niches for biota to occupy (Geary, 1990; Hou et al., 2014). During the Quaternary in the IWP region, repeated global Quaternary sea-level changes repeatedly connected or cooling and the lowering of sea levels produced a number of isolated islands in the Mediterranean Sea, such as Corsica land bridges that isolated aquatic systems, such as closing the and Sardinia (Provan & Bennett, 2008; Salvo et al., 2010). Sunda and Malacca straits between the Indian and Pacific During episodes of connection, island bridges gave complete oceans. These restrictions formed allopatric distributions, access for terrestrial and limnic species to all the newly which promoted regional diversification (Crandall et al., exposed terrain (Jesse et al., 2011). High sea levels disrupted 2008). The climatic and sea-level fluctuations drove the these ephemeral land bridges and isolated insular populations retraction of coral reef habitats with a rapid loss of marine (Ali & Aitchison, 2014). Quaternary climatic oscillations biodiversity. However, stable coral reef habitats acted as might not have produced species, yet they played an refugia for species of reef fishes (Pellissier et al., 2014; Leprieur important role in shaping geographic distribution and genetic et al., 2015). In contrast to extensive coral reef refugia in the structure of modern species (Shi et al., 2013; Pellissier et al., IWP region, more than 60% of coral species disappeared 2014). in the Caribbean region, and only the northern coast of Venezuela and the mainland coast of Brazil served as refugia (2) Cave, anchialine habitat and lake formation (Leigh et al., 2014; Marko et al., 2015). Climatic conditions, rock-properties, and tectonic settings determine the formation and development of caves (Hao et al., 2012). The principal features of caves around the IV. PALAEOCLIMATE RECONSTRUCTIONS Mediterranean probably relate to the MSC (Morvan et al., 2013). Pliocene sea-level fluctuations caused Messinian surface erosion on the continental shelf (Audra et al., 2004). (1) Cenozoic sea-level changes and formation of freshwater habitats Further, downcutting of Mediterranean tributary rivers enhanced inland karst systems, such as the Ardeche karst in Sea-level fluctuations have important implications for the France that the Rhone River incised (Mocochain, Clauzon organic productivity of oceans and the distribution patterns & Bigot, 2006). Similar features occur in Balkan karst of sediment along continental margins and in interior basins regions (Sket, 1999). Quaternary glacial cycling heavily (Haq, Hardenbol & Vall, 1987; Leite et al., 2016). Sea-level influenced the surface habitat, while the cave or hypogean changes are also thought to control hydrographic–climatic habitats experienced modest climatic shifts and in doing so patterns and, indirectly, biotic distribution patterns (Hallam, supplied shelters for surface fauna. This isolation drove rapid 1984). Eustasy is often reconstructed through marine speciation (Curcic & Jovanovic, 2004). foraminiferan sediments and oxygen and carbon isotopes Compared with freshwater caves, anchialine caves occur in (Zachos et al., 2001). coastal regions. They were affected by both inland freshwater Glaciation was the main driver of late Cenozoic sea-level input and tidal exchanges with oceanic waters via subsurface changes, but other factors, such as changes in seawater channels and cracks (Neiber et al., 2011). Extensive anchialine

Biological Reviews 93 (2018) 874–896 © 2017 Cambridge Philosophical Society 882 Zhonge Hou and Shuqiang Li caves occur in ancient Tethyan margins, such as the both temporal (molecular dating) and spatial (biogeographic) Caribbean and Mediterranean seas. Sea-level fluctuations scales (Huyse et al., 2004; Sola` et al., 2013). Some studies link during the LGM greatly influenced this underground setting the timing of diversification and environmental conditions (Mylroie & Mylroie, 2011). Falling sea level dried out (Williams, 2007; Hou et al., 2014). Increasing evidence aquatic habitats, interrupted continuous passages of water from geologic, palaeoclimatic and species richness data will and caused fragmentation of species ranges. This might provide a solid framework for hypothesis testing on patterns have subsequently driven evolutionary divergence. Sea-level of aquatic diversification. The chronology of the impacts of rises had equally important effects by reconnecting formerly several geological events illustrates patterns of diversification separated habitats and taxa. The anchialine cave ecosystem for different taxonomic levels ranging from family, genus, with its local physico-chemical gradients shelters a unique and species to population. and novel fauna, which salinity-stratified water layers often separate. For example, many atyid shrimps and amphipods (1) Open Tethys Ocean for marine species and occur only in meteoric waters above the halocline, while Atlantic barrier remipedes are restricted to the underlying marine component of anchialine systems (Moritsch, Pakes & Lindberg, 2014). Before the end of the Eocene, the Tethys Ocean provided From the Pliocene, geological movements, sea-level a potential migration route between the developing Atlantic fluctuations and climatic changes initiated cave and lake and the IWP (Malaquias & Reid, 2009; Van Syoc et al., systems. The most outstanding European example is 2010). A considerable degree of overlap in fossils reflects oligotrophic and karstic Lake Ohrid, including its sister Lake this connectivity (Neraudeau´ & Mathey, 2000; Bellwood & Prespa. They formed as a result of the Dinaric subduction Wainwright, 2002; Zanata & Vari, 2005; Keller, Punekar & during 5–2 Ma (Albrecht & Wilke, 2008). Endemism in Mateo, 2016). Studies at higher taxonomic levels, including Lake Ohrid occurs at different spatial and taxonomic scales genera or families, associate with the opening of the Tethys because of its isolation. Large alpine lakes also occur in Ocean. For example, research on marine fish deposits from the Alps, Tian Shan and the Tibetan Plateau. These Monte Bolca in Italy identified similar familial compositions serve as important indicators of climatic change (Li et al., in the Atlantic and Indo-Pacific (Bellwood & Wainwright, 2011). Few have been studied to determine their ages, but 2002). Almost all modern families of reef fishes were most of them have been isolated from each other since widespread in the Eocene (Cowman & Bellwood, 2013a). about 5000–4000 years ago (Mathis et al., 2014). Freshwater Gastropods exhibit a similar pattern in that the MS and IWP fish and crustaceans occupy these alpine lakes, which share fossils (Harzhauser, 2004; Merle et al., 2014). The chain are characterised by cold and oligo-mesotrophic habitats of localities starts in the French Adour Basin, and includes (Catalan et al., 2009; Ventura et al., 2014). the Veneto region and the Turin Mountains of northern Italy, the Greek Mesohellenic Trough and the Turkish Sivas Basin down to the central Iranian basin and Pakistan in the east (Harzhauser, 2004, 2007). Marine squamates also had a V. DIVERSIFICATION PATTERNS IN THE worldwide distribution through the Tethys Ocean and diver- TETHYAN REGION sified into three major groups by the Late Cretaceous (Bardet et al., 2008). Benthic rudist bivalves and ostracod fossils found Over space and time, geological and climatic dynamics can in the Tibet and Tarim Basin correspond with the Tethys impact significantly the patterns of biodiversity seen today. Ocean extending to the Far East during the Late Cretaceous The spatial and temporal scales of the biotic assemblages and Paleogene (Scott et al., 2010; Foreal et al., 2011). can show if these processes promoted or constrained Although the Tethys Ocean served mainly as an open species diversification (Gillespie & Roderick, 2014). Because seaway during the Cretaceous, the expanse of the Atlantic Tethyan fragmentation spans over 100 million years, its Ocean likely formed a formidable barrier for benthic impact on patterns of aquatic biodiversity is significant. organisms (Fig. 3A). For example, the spatangoid echinoids How did Tethyan changes affect diversification globally and benthonic ostracod Majungaella had disjunct distributions or within regional scales on different timescales? Since in South America and Africa, which is consistent with the the mid-Cretaceous, the gradual separation of North opening of the Atlantic in the Late Cretaceous (Villier & America from Eurasia and the breakup of Gondwana Navarro, 2004; Piovesan et al., 2012). Similarly, the relictual increasingly fragmented the Tethys Ocean. These geological distribution in amphi-Atlantic interstitial groundwater processes drove speciation and shared patterns of biodiversity suggests that living thermosbaenacean crustaceans are among animals (Anger, 2013). The evolutionary histories of ancient Tethyan lineages and the opening of the Atlantic co-distributed taxa can be compared spatially and temporally Ocean around 120–95 Ma drove their diversification to assess general patterns by mapping their phylogenetic (Jaume, 2008). histories onto geological reconstructions. Research on the ancient Tethyan region initially relied on (2) Tethyan closure drove vicariant speciation fossil distributions (Newton, 1988; Fraaye, 1996). However, recent studies have used genetic data to test the hypothesis The Tethys Ocean closed in the Middle Miocene that Tethyan changes triggered evolutionary radiations on (18–12 Ma) starting with the northward tectonic movement

Biological Reviews 93 (2018) 874–896 © 2017 Cambridge Philosophical Society Aquatic diversification in the Tethyan region 883 of Africa and India, and subsequent convergence of the Closure of the Tethys not only imposed a separation African–Arabian and Eurasian plates. This has been between the Atlantic and IWP marine groups, but also termed the Terminal Tethyan Event (TTE; Adams et al., promoted rapid speciation in the IWP region such as for gas- 1983; Rogl,¨ 1998). The TTE erected physical barriers to tropods of the genera Conus, Nerita and Turbo (Vallejo, 2005; the exchange of marine populations between the Atlantic Williams, 2007; Frey & Vermeij, 2008) and ostracods of and Indo-Pacific, which drove diversifications (Bellwood the genus Neocytheromorpha (Yamaguchi, Mashiba & Kamiya, et al., 2004; Steeman et al., 2009; Cowman & Bellwood, 2012). This time span coincides with the tectonic collision 2013b; Cowman, 2014; Schiffer & Herbig, 2016). Fossil between Australia and Southeast Asia, which formed the deposits, such as the significant decrease in similarity IWP island arc (Lohman et al., 2011). A proliferation of between the Mediterranean and Pakistan gastropod faunas reef-building corals occurred concurrently (Williams, 2007; during the Early Miocene, witness the vicariant pattern Bellwood et al., 2017). Thus, increases in diversification of (Harzhauser, Piller & Steininger, 2002; Harzhauser et al., reef-associated IWP lineages were responses to both the 2007). Extant biotic assemblages clearly reflect the closure availability of new shallow-water habitats and increased of the Tethys Ocean (Banford, Bermingham & Collette, carbonate platforms originating from the diversification of 2004; Cowman & Bellwood, 2013a; Eilertsen & Malaquias, coral reefs (Cowman & Bellwood, 2011, 2013a,b;Priceet al., 2015); deep phylogenetic splits occur in some aquatic groups 2011; Dornburg et al., 2015; Bellwood et al., 2017). The between the Atlantic/Mediterranean and the Indo-Pacific centre of global marine biodiversity appears to have shifted (Fig. 3B). from the western Tethyan realm to the present IWP in the Concordant patterns of vicariance between lineages from early Miocene. This links to tectonic events and final closure the tropical Atlantic/Mediterranean and IWP mark the of the Tethys Ocean (Harzhauser et al., 2007; Renema et al., TTE around 18–12 Ma (see online Table S1, Fig. 5). For 2008; Leprieur et al., 2016). example, studies of deep-sea gastropod genus Scaphander indicate that the IWP became isolated from the Atlantic by (3) Recolonisation of the Mediterranean Basin after closure of the Tethys Ocean in the early Miocene, which the MSC corresponds well with the final closure of the Tethys (Eilertsen The MSC, which lasted from 5.96 to 5.33 Ma, led to & Malaquias, 2015). Some reef-associated fishes exhibit the formation of a lake system termed as ‘Lago-Mare’ the same pattern (Cowman & Bellwood, 2013b; Dornburg (Orszag-Sperber, 2006; Roveri et al., 2014). The progressive et al., 2015). However, several divergences pre-date the evaporation of Mediterranean waters and the consequent separation between the Atlantic and IWP (Aoyama, Nishida disappearance of marine habitats might have driven extinc- & Tsukamoto, 2001; Stelbrink et al., 2010; Swart et al., 2015). tion of most of the marine fauna (Meynard et al., 2012). Fossil For example, killifishes of the genus Aphanius have two bryozoans reveal an imbalance between the speciose IWP major clades that correspond to the Oligocene splitting and the species-depauperate Mediterranean (Harzhauser of the former western (the Mediterranean basin) and eastern et al., 2007). This suggests that the marine fauna suffered Tethys (Arabian basin) (ca. 37 Ma; Hrbek & Meyer, 2003). strong impoverishment after the TTE, and nearly disap- The division existed 20–10 million years before the closing peared by the MSC and Pliocene glaciation (Harzhauser of the Tethys. Thus, barriers to gene flow must have et al., 2007). The reduction of planktonic productivity pre-dated the Eocene tectonic collisions. Evidence from and coral habitat further confirms MSC extinction, which estuarine gastropods of the genus Bulla supports this pre-TTE included reef-associated bivalves, gastropods and fishes (Lan- scenario; it diverged into IWP and Atlantic groups ca.46Ma dini & Sorbini, 2005; Meynard et al., 2012; Vermeij, 2012). (Malaquias & Reid, 2009), preceding the final closure of the The opening of the Strait of Gibraltar at the end of the MSC Tethys by about 20 Ma as predicted from other molluscs allowed marine species to recolonise the Mediterranean from (Williams & Reid, 2004; Reid, Dyal & Williams, 2010; the Atlantic Ocean. Because of free exchange, little genetic Uribe et al., 2017). Further, most molecular estimates of variation exists between Mediterranean and Atlantic popula- Tethyan divergences in coral reef fishes pre-date the TTE tions (Duran, Pascual & Turon, 2004; Patarnello, Volckaert by falling in the range 35–20 Ma (Bellwood et al., 2004; & Castilho, 2007), and fewer marine endemic species exist Barber & Bellwood, 2005; Cowman & Bellwood, 2013b); in the Mediterranean after the MSC than before (Meynard this is similar to crustaceans (Page, Humphreys & Hughes, et al., 2012). 2008) and bryozoans (Nikulina, Hanel & Schafer,¨ 2007). The MSC drove marine fauna to extinction in the Thus, it appears that ecological changes induced by a Mediterranean, but the MSC formed the freshwater series of tectonic events from the Eocene to Miocene have ‘Lago-Mare’ stage and connected the European mainland continuously affected diversification on both sides of the with Mediterranean islands. During the MSC, some marine Tethys Ocean. Notwithstanding, the discrepancy between species adapted to the freshwater environment (Roveri biotic divergence time estimations and Tethyan closure et al., 2014). Following reflooding of the Mediterranean could indicate earlier vicariant events, as well as selective basins from the Atlantic Ocean, these species retained extinction or errors of calibration (Williams & Reid, 2004; their freshwater habits and, thus, remained isolated from Williams, 2007; Cowman & Bellwood, 2013b). Therefore, euryhaline Ponto-Caspian species (Fig. 6A). This probably biogeographic explanations require careful consideration. gave rise to the freshwater endemism that exists today

Fig. 5. The ranges of splits between Atlantic/Mediterranean and Indo-West Pacific clades in fishes (green), molluscs (yellow), crustaceans (purple), and bryozoans (blue). The estimated divergence times and 95% confidence intervals were taken from published literature (see online Table S1). The x-axis indicates the geological time in million years and geological events related to the closure of the Tethys Ocean (maps taken from Fig. 2). The grey area represents the period of Tethyan closure. About 10 groups match the geological time of Tethyan closure, while 22 groups pre-date the Tethyan closure. These differences reflect that tectonic events from the Eocene to Miocene have continuously affected splitting between Atlantic/Mediterranean and Indo-West Pacific clades. in the Mediterranean region (Penzo et al., 1998). The environments, and subsequent reflooding triggered specia- molecular phylogeny of sand goby fishes of the genera tion and radiation on the Salentina Peninsula (Wilke, 2003). Pomatoschistus, Gobiusculus, Knipowitschia and Economidichthys The MSC led to contact between previously isolated records the influence of the MSC (Huyse et al., 2004). landmasses and ancient river drainage systems, which The sand goby ancestor occupied the EA and MS, yet functioned as an important corridor for faunal dispersal several species survived and adapted to freshwater habitats from the Eurasian mainland to Mediterranean islands during the MSC. After recolonisation, species radiated in (Bianco, 1990; Sola` et al., 2013). Freshwater animals marine and brackish habitats and isolated freshwater gobies experienced rapid speciation upon return of the basin to became endemic species (Huyse et al., 2004). A similar marine conditions (Fig. 6B). Splits between taxa endemic pattern exists for snails of the genus Salenthydrobia (Wilke, to Mediterranean islands and the Eurasian mainland have 2003). The disappearance of marine habitats during the been reported, such as for planarians (Dugesia) on islands of MSC drove a Salenthydrobia taxon to adapt to freshwater the Aegean Sea (Sola` et al., 2013), freshwater crabs (Potamon)

Fig. 6. Hypothesized colonisation routes into the Mediterranean Basin during the Messinian Salinity Crisis (MSC) and example cladograms. (A) Marine species recolonised the Mediterranean Sea (MS) from the Atlantic Ocean, while isolated freshwater survivors during the MSC speciated. Examples include sand gobies (Pomatoschistus, Gobiusculus, Knipowitschia and Economidichthys;Huyseet al., 2004) and snails (Salenthydrobia; Wilke, 2003). (B) Freshwater animals dispersed from mainland to islands and radiated in the Mediterranean Basin during the MSC. Examples include planarians (Dugesia;Sola` et al., 2013) and crabs (Potamon; Jesse et al., 2011). from Asia Minor across the mid-Aegean trench to the et al., 2015a). Sister-species on both sides of the isthmus Mediterranean basin (Jesse et al., 2011), and water frogs were likely isolated at different time intervals, depending (Pelophylax) of Cyprus isolated from Asia Minor (Akin et al., on habitat preference (Cowman & Bellwood, 2013b;Leigh 2010). Moreover, patterns of diversification of the fish genera et al., 2014). Sister pairs restricted to deep-water habitats Chondrostoma and Telestes showed concomitant short intern- typically differentiated earlier than those found along the odes with a polytomy, which was attributed to the cessation mainland or shallow waters, such as for benthic mollusc pairs of contact between landmasses due to rapid reflooding of the (Lessios, 2008; Montes et al., 2012a). Among crustaceans, Mediterranean after the MSC (Durand et al., 2003; Ketmaier mangrove-associated groups showed the smallest divergence, et al., 2004). Thus, it appears that a number of lineages orig- as expected due to being separated later by the rising inated virtually simultaneously around the Mediterranean isthmus (Knowlton & Weigt, 1998). Both molecular and fossil hydrographical system by vicariance after the MSC. The analyses have demonstrated an early separation of marine MSC event thus triggered the diversification and endemism organisms in the Atlantic and Pacific oceans regardless of of the European freshwater fauna (Beerli et al., 1994; Reyjol dispersal ability and habitat preference (Bacon et al., 2015a). et al., 2007). Thus, closure of the Central American Seaway promoted diversification on the Pacific and Atlantic sides, yet the time (4) Contrasting patterns caused by the closure of estimate of final closure remains under debate (Bacon et al., the Central American Seaway 2015b; Lessios, 2015; Marko et al., 2015). The closure of the Central American Seaway caused The tectonic events coupled with climatic and ocean extensive changes in ocean circulation and climate (Montes current changes that accompanied the closure of the Central et al., 2015). It was an influential vicariant event that drove American Seaway propelled environmental transformations aquatic biotic diversifications on both sides of the Isthmus in both the WA and EP. These resulted in extinction, (Fig. 3C). Molecular analyses document well the evolutionary especially among reef-forming corals and reef-associated consequences via extant transisthmian sister-species of fishes, faunas (Leigh et al., 2014; Schwartz, Budd & Carlon, 2012; crustaceans, echinoids and molluscs (Lessios, 2008; Bacon Marko et al., 2015). The final closure induced contrasting

Biological Reviews 93 (2018) 874–896 © 2017 Cambridge Philosophical Society 886 Zhonge Hou and Shuqiang Li environments. The WA had lower productivity, less salinity, largely unaffected (Wilson & Veraguth, 2010). Similar higher surface temperature, narrower tidal range and more patterns have been identified in a sprat fish (Sprattus; corals than the EP side (Lessios, 2008; Schwartz et al., 2012). Debes, Zachos & Hanel, 2008) and a marine demersal fish These differences affected modern species compositions. (Pomatoschistus; Larmuseau et al., 2009), possibly reflecting the Reef-associated molluscs and fishes, which tend to occur on general role played by the LGM. deep, hard sea floors, are more diverse in the WA than in Quaternary sea-level fluctuations connected the Mediter- the EP. Intertidal inhabitants such as Littorinidae snails and ranean islands with the mainland temporarily and enabled sand dwellers of semelid bivalves are more diverse in the EP exchange between islands and the mainland. Freshwater than WA (Leigh et al., 2014). crabs sampled from the Aegean Archipelago share the same Closure of the Central American Seaway fully fragmented species without insular endemics, suggesting that the low the ancestral Tethys Ocean into the EP, WA, EA, MS and sea levels possibly promoted dispersal to these islands, but IWP (Fig. 3). The IWP was isolated from the EA and MS by subsequent rises in sea level did not cause speciation (Jesse the closure of the Tethys Ocean about 18–12 Ma, becoming et al., 2011). Insular diving beetles (Agabus brunneus) from the a biodiversity hotspot. EA and MS organisms exchanged via Balearic Islands, Corsica and Sardinia did not differentiate the Gibraltar Seaway, while the Central American Isthmus in either genetics or ecology, reflecting the palaeodrainage isolated the EP and WA. connectivity between islands and mainland during the LGM (Hidalgo-Galiana et al., 2014). (5) Species range expansion during the Quaternary Colder temperatures and lower sea levels during the climatic oscillations Quaternary in the IWP broadened the continental area and restricted seaways between the Indian and Pacific basins Quaternary climatic cycling and associated geomorpholog- (Hewitt, 2000). This separation promoted diversification. ical and hydrographic conditions repeatedly altered the Clades correspond to the Indian and Pacific basins albeit geographical distributions of species (Hewitt, 2000; Hanfling¨ with a little secondary contact and gene flow (Crandall et al., 2009; Qu et al., 2014; Weigelt et al., 2016). Glaciation et al., 2008). This pattern occurs in scad mackerel (Decapterus restricted species to more or less severe ranges and frag- russelli; Rohfritsch & Borsa, 2005), the gastropods Nerita mentations in refugia (Noonan & Gaucher, 2006; Pellissier albicilla (Crandall et al., 2008) and Lunella cinerea (Williams et al., 2014). Interglacial conditions were more favourable, et al., 2011), and the mud crab (Scylla serrata; Fratini, and modified river systems provided new opportunities for Ragionieri & Cannicci, 2010). Although divergence ranges dispersal. The principal refugia for European freshwater ani- from the Late Miocene to Pleistocene, these studies point mals localise on the Mediterranean margins (Verovnik, Sket to vicariance owing to glacial cycling. The Quaternary & Trontelj, 2005; Audzijonyte et al., 2015). The Black and climatic oscillations drove species to move, adapt, and go Caspian sea basins connected at the beginning of the Pleis- extinct. Coral habitats were compressed and maintained tocene (2–1 Ma), and fishes of the genus Vimba expanded in some refugia, but isolated from each other by deep from its refugium in the margins of the Black Sea towards the sea barriers or land bridges (Kool et al., 2011). Coral reef Baltic basin when melting ice filled the Baltic basin with fresh fragmentation promoted vicariance events in reef-associated water (Hanfling¨ et al., 2009). By contrast, the Arctic marine fishes (Cowman & Bellwood, 2013b; Leprieur et al., 2015). crustacean Gammaracanthus colonised the Caspian Sea during However, stable reef habitat preserved marine biodiversity times of high sea level through the Turgai Strait (about 1 Ma), during times of glaciation (Pellissier et al., 2014). The and the following glaciation isolated this population (Vain¨ ol¨ a¨ Quaternary thus greatly affected species distributions and et al., 2001). These discoveries confirm that Quaternary cli- contributed to species richness in the IWP hotspot. matic oscillations connected or isolated the Paratethys basin from the Baltic/Arctic basins and in so doing shaped the current population structures of aquatic organisms. VI. HABITAT SHIFT FROM MARINE TO Quaternary glaciation, particularly the LGM, greatly FRESHWATER affected the distributions and population sizes of temperate marine species. Their ranges retreated towards the equator (1) Marine extinction to escape ice sheets (Crandall et al., 2008). Traditional genetic models predict low genetic diversity in formerly The tectonic activity associated with the Cenozoic Tethyan glaciated areas and high diversity in glacial refugia (Hewitt, closure and climatic upheaval shifted the hotspot to the 2000; Maggs et al., 2008). During the Quaternary, sea-level IWP. At the same time, it led to stepwise extinction in the reductions led to the separation of the Black Sea from the ancient Tethyan region due to the disappearance of marine Mediterranean, but the Mediterranean remained connected habitats (Harzhauser & Kowalke, 2002; Stow, 2010). During to the Atlantic Ocean and it potentially offered refugia. For the Oligocene the Paratethys, a northern part of the Tethys, example, analysis of the marine pipefish (Syngnathus) yields extended from central Europe to inner Asia (Popov et al., a strong signal of postglacial recolonisation of the northern 2004; Sun & Jiang, 2013). It gradually shrank into relictual Atlantic coast and Black Sea with reduced genetic diversity, Caspian and Black seas due to the continental collision that while the coastal Mediterranean populations exhibited high shaped the Alpine-Himalayan orogenic belt (Rogl,¨ 1998). genetic variation, indicating that the LGM left this region The marine habitat in the Paratethys completely vanished

Biological Reviews 93 (2018) 874–896 © 2017 Cambridge Philosophical Society Aquatic diversification in the Tethyan region 887 around 11.6 Ma (Geary et al., 1989; Harzhauser & Mandic, is consistent with the collision of the Asian and Indian 2008) after Tethyan closure from the Indo-Pacific and subcontinents, which promoted the cohesive zone shift from a strong restriction of connections to the Mediterranean shallow marine waters to freshwater habitats (Yamanoue (Harzhauser & Piller, 2007; Studencka & Jasionowski, et al., 2011). Pulmonate snails (Holznagel et al., 2010) and 2011). The change from marine to brackish and freshwater copepods (Adamowicz et al., 2010) colonised freshwater only ecosystems resulted in the extinction of corals, foraminiferans once leading to major radiations. This suggests that they and molluscs in the Paratethys (Harzhauser & Piller, 2007; infrequently shift habitats. The colonisation of islands by Studencka & Jasionowski, 2011). It also drove the sudden marine species constitutes another form of habitat shift. evolution of endemic brackish and freshwater molluscs This has been reported in crabs during the Late Tertiary (Geary, 1990; Müller, Geary & Magyar, 1999; Lukeneder emergence of Jamaica, along with rapid radiation (Schubart et al., 2011). Different faunal compositions in fossils reflect the et al., 1998). In the Mediterranean islands, marine-derived Paratethyan shift from marine to freshwater habitat about species moved into freshwater habitat during the MSC and 12 Ma. This time-point was considered as being the origin diversified locally (Huyse et al., 2004). Tectonic events and of extant Ponto-Caspian molluscs (Albrecht et al., 2007; Sket, sea-level fluctuations in the ancient Tethyan region resulted 2011; Bilandˇzija et al., 2013) and crustaceans (Cristescu & in the emergence of new freshwater habitats. A habitat shift Hebert, 2005; Audzijonyte et al., 2008; Hou & Sket, 2016). from marine to freshwater provided ecological opportunities with unoccupied niches for exploitation by marine ancestors, (2) Freshwater occupation leading to a rapid diversification and range expansion in freshwater environments (Hou et al., 2011). Continental plate movements uplifted marginal mountain Some fishes have colonised freshwater habitats multiple ranges, e.g. the Alps and the Himalayas, and Tethyan times such as diadromous species that migrate between regression resulted in the emergence of new freshwater marine and freshwater habitats. Ariid catfishes appear habitats (Tsigenopoulos & Berrebi, 2000; Mamos et al., to have colonised freshwater habitats more than 10× 2016). The changing environment drove the transition of independently in all major geographical ranges (Betancur-R, many marine-derived organisms to other habitats (Schubart, 2009, 2010; Betancur-R et al., 2012). Except for the rela- Diesel & Hedges, 1998; Seehausen & Wagner, 2014). Molec- tively large diversity of freshwater ariids in Australia–New ular phylogenies indicate the frequency and age of historical Guinea, biodiversity in tropical America, Africa, and marine–freshwater transitions of crustaceans (Adamowicz Southeast Asia are comparable (Fig. 7B). Moreover, their et al., 2010; Hou et al., 2011), fishes (Lovejoy, Bermingham & freshwater distributions are not far from the sea, suggesting Martin, 1998; Yamanoue et al., 2011) and snails (Holznagel, colonisation via river systems that drain into estuaries and Colgan & Lydeard, 2010). Most studies indicate a clear coastal margins. Among globally distributed marine fishes, separation between marine and freshwater lineages. This anchovies, drums and needlefishes also appear to have suggests that diversification in the new environment followed entered freshwater habitats multiple times (Lovejoy et al., a single freshwater colonisation event (Fig. 7A). However, 2006). In the Mediterranean, gobies exhibit multiple inde- research also shows that closely related marine and freshwa- pendent colonisations of freshwater (Penzo et al., 1998). This ter species occur intercalated across lineages, indicating that colonisation is attributed to the influence of the MSC and the marine–freshwater transitions occurred repeatedly (Fig. 7B). production of progressively desalinized habitats and episodic A single transition from marine to freshwater habitat usu- aquatic connections between freshwater and marine realms ally associates with a major geological event. For example, (Penzo et al., 1998). Despite the increase in studies of habitat Hou et al. (2011) found that widely distributed, Eurasian transitions, few have investigated diversification rates to freshwater crustaceans (Gammarus) clustered together compare differences between marine and freshwater habitats phylogenetically and underwent rapid diversification in or between geographical regions (Betancur-R et al., 2012; the Late Eocene. By contrast, Tethyan marine Gammarus Bloom et al., 2013). Further research is needed to understand maintained a constant rate of diversification (Fig. 7A). The the factors generating marine–freshwater habitat shifting, as marine–freshwater habitat shift corresponds well with the well as those promoting habitat-specific diversification and collisions between the Eurasian and Africa/Indian plates adaptation. and subsequent retreat of the Tethys. This suggests that an ancient colonisation of freshwater habitat and subsequent (3) Radiations in caves, anchialine habitats and speciation was linked to geographical range expansions (Hou lakes et al., 2014; Mamos et al., 2016). Fishes, snails and other crustaceans show similar patterns. South American stingrays Late Miocene active ground-water incising initiated cave (Lovejoy et al., 1998; Lovejoy, Albert & Crampton, 2006) and systems along the Mediterranean margins (Zaksek,ˇ Sket & African herring (Wilson, Teugels & Meyer, 2008) present Trontelj, 2007; Franjevic´ et al., 2010). A variety of subter- a clear distinction between marine and freshwater groups. ranean faunas occupy these caves (Sket, 1999). Speciation in Fishes invaded freshwater habitats due to marine incursions this system is due primarily to spatial isolation and restricted and subsequently spread across continents. Pufferfishes dispersal (Juan et al., 2010). During the MSC, the formation may have occupied freshwater habitats in Southeast Asia of large limestone beds and underground karst provided suit- during the Eocene (Yamanoue et al., 2011). This scenario able conditions for the colonisation of subterranean habitats

Fig. 7. Alternative hypotheses for marine–freshwater habitat-shifting represented by phylogenetic trees. Branch colours correspond to ecological habitats of marine (black) and freshwater (red). Dotted area denotes present coast regions once linked to the ancient Tethys Ocean and red arrows indicate colonisations of freshwater habitats. (A) A single colonisation of a freshwater habitat followed by rapid diversification and range expansion (Gammarus crustaceans; Hou et al., 2011). (B) Independent colonisations of euryhaline and freshwater habitats (ariid catfishes; Betancur-R, 2010; Betancur-R et al., 2012). by surface freshwater ancestors (Sket, 1999). A widespread, plate tectonic vicariant events that subdivided them along common ancestor or multiple surface ancestors invaded cave the margins of Tethys (Sket, 1996). Well-known examples systems. Subsequently, vicariance associated with progres- include crustaceans, such as Remipedia, Thermosbaenacea, sive karstification fragmented populations. Isolation and low Atyidae (shrimps) and Metacrangonyctidae (amphipods). dispersal abilities facilitated speciation, which led to a high Their disjunct global distributional patterns match precisely regional biodiversity (Trontelj et al., 2009). The Dinaric karst the area covered by the ancient Tethys Ocean or its region of the Balkan Peninsula hosts a considerable subter- coastlines (Jaume, 2008; Neiber et al., 2011). The Tethyan ranean faunal diversity, which offers great potential for phy- vicariance hypothesis was tested in the family Metacran- logeographic analyses (Sket, 2011). For instance, cave shrimp gonyctidae. Results suggested that major diversifications along the edge of the Mediterranean have different origins. occurred between 96 and 83 Ma, coincident with vicariance France–Iberian Peninsula Gallocaris has an old epigean fresh- driven by ancient plate tectonics (Bauza-Ribot` et al., 2012). water common ancestor while Dinaric–Caucasian Troglocaris Biogeographic analyses of cave shrimps (Typhlatya) indicated has a different freshwater ancestor (Sket & Zaksek,ˇ 2009). that the split of Caribbean and Mediterranean subclades Diversification of Dinaric Troglocaris dates to 5.3–3.7 Ma, post-dates the establishment of deep water between the which corresponds to the beginning of local karstification Atlantic shores; this supports the marine dispersal hypothesis (Zaksekˇ et al., 2007). This pattern also occurs in other crus- (Botello et al., 2013). Caribbean Typhlatya originated from an taceans, including isopods (Asellus; Verovnik et al., 2005) and ancestral marine population before the formation of anchia- amphipods (Niphargus; Trontelj, Blejec & Fiser,ˇ 2012). line cave habitat at the Pliocene/Pleistocene boundary, and Insular cave species are descendants of freshwater subsequently migrated to caves once they formed (Hunter ancestors, while anchialine species seem to have originated et al., 2008). Future molecular analyses can investigate the directly from the sea, although their non-cavenicolous influence of Tethyan fragmentation on other anchialine marine relatives are either extinct or inhabit deep sea (Juan taxa that have a presumed Tethyan distribution, including et al., 2010). The extremely disjunct global distributions of species of Remipedia and Thermosbaenacea (Canovas´ many circumtropical anchialine groups likely result from et al., 2016).

Geological events and Pleistocene deglaciation formed can persist at sea for up to several months and disperse ancient lakes, which served as evolutionary reservoirs by 1000 km (Cowen & Sponaugle, 2009; Burridge et al., 2012), preserving ancient lineages and providing relatively stable which promotes genetic exchange over a large area. Comber environments for intralacustrine speciation. For example, fish (Serranus cabrilla) may have dispersed frequently from intralacustrine radiations of Gammarus balcanicus in Lake west to east over the Almeria–Oran Front by ocean cur- Ohrid in the Balkan Peninsula that occurred at 3–2 Ma rent, facilitating gene flow (Schunter et al., 2011). Similarly, and less than 1 Ma associate with the origin of the lake and European eels (Anguilla anguilla) show that westward ocean Pleistocene water-level fluctuations (Wysocka et al., 2013, currents drive transatlantic dispersal and enhance gene flow 2014). Further, freshwater crustaceans, such as Gammarus (Baltazar-Soares et al., 2014). Within the IWP, the absence of lacustris (Meyran & Taberlet, 1998; Vainio & Vain¨ ol¨ a,¨ 2003; hard barriers allows coral reef fishes to maintain widespread Altermatt et al., 2014) and Daphnia longispina (Ventura et al., geographic ranges that span from the east coast of Africa to 2014) occupy recent glacial alpine lakes along the Alps islands in the Central Pacific (Cowman & Bellwood, 2013a). and Himalayas. Scant evidence suggests that certain alpine However, sometimes genetic connectivity is based on a organisms can colonise available habitats with advancing stepping stone model, where dispersion occurs in a sequen- deglaciation. Alpine Gammarus lacustris colonised glacial lakes tial manner in time and space via suitable stepping stones, of northern Europe from southern Europe and little genetic ultimately leading to genetic homogeneity among geograph- divergence exists between northern and southern popula- ically distant sites. The scalloped hammerhead shark (Sphyrna tions (Meyran & Taberlet, 1998; Vainio & Vain¨ ol¨ a,¨ 2003). lewini) originated in the IWP and radiated during the late Contrary to circumpolar Gammarus lacustris, its sister-species Pleistocene into the central Pacific and EP using South Pacific G. alpinus experienced a Pliocene range expansion across the archipelagos (Fig. 4B; Duncan et al., 2006). The stepping Alps lakes and vicariance due to climatic warming following stone model also explains the distribution of anchialine crus- the Quaternary glaciation (Alther, Fiserˇ & Altermatt, taceans (Metacrangonyx), which dispersed from the Tethyan 2017). Comparable temporal data are available for Daphnia Mediterranean to the Caribbean Sea using ancient, drowned longispina that live in alpine lakes in the Pyrenees. A single archipelagos (about 60 Ma) in the central Atlantic along with colonisation event following gradual deglaciation of the east-to-west warm circumequatorial marine currents in the Pyrenees after the LGM best explains its genetic structure ancient Tethys (Fig. 4A; Bauza-Ribot` et al., 2012). (Ventura et al., 2014). In addition, the island-like nature of Closure of the Tethys Ocean in the Middle Miocene alpine lake habitats is expected to create opportunities for strongly restricted exchanges of tropical fauna between the local adaptation (Ventura et al., 2014). A more extensive Atlantic and IWP (Cowman & Bellwood, 2013a). The survey of Alps–Himalaya alpine lakes could uncover the remaining gateway around the South Africa formed a mechanism of speciation to address this hypothesis. cold-water barrier between the Atlantic and IWP in the early Pleistocene (Rocha et al., 2005). However, during interglacial times, some fishes and turtles crossed the Cape of Good Hope VII. VICARIANCE AND DISPERSAL to radiate bidirectionally (Fig. 4C). Hammerhead sharks COMPARISON (Sphyrna lewini; Duncan et al., 2006), Parablennius fishes (Levy et al., 2013) and green sea turtles (Chelonia mydas;Bourjeaet al., Vicariance is the process of separating organisms by a 2007) radiated from the Atlantic Ocean into the IWP by this physical barrier. This lends itself to rigorous hypothesis route. Most marine dispersals occur from the IWP to the testing by using distinct distribution patterns. Vicariance Atlantic Ocean via passive larval transport in the ocean cur- often occurs following large-scale geological events such as rent (Bourjea et al., 2007). Phylogeographic studies confirmed orogenesis and the separation of continents. The Tethyan that some coral reef fish (Gnatholepis) invaded the Atlantic realm experienced three major vicariant events (Fig. 3): (i) Ocean during the interglacial period about 145000 years ago the Atlantic barrier, an expansion of ocean that separated (Rocha et al., 2005), as did pygmy angelfish (Centropyge; Bowen the EA from WA (Fig. 3A); (ii) closure of the Tethys Ocean, et al., 2006), coral fish (Scarus; Cowman & Bellwood, 2013b) which cut off the dispersal between the Atlantic and IWP and ridley sea turtles (Lepidochelys olivacea; Bowen et al., 1998). (Fig. 3B); and (iii) closure of the Central American Seaway, In the Tethyan region, the vicariance hypothesis is less which resulted in the evolution of species pairs on the controversial than dispersal at higher taxonomic levels and Atlantic and Pacific sides (Fig. 3C). Molecular phylogenies of large geographic scales. Vicariance is the clear driver of globally distributed marine groups can detect the signature speciation in deeper lineages. Divergence-time estimations of Tethyan vicariance, as noted above. play key roles in differentiating between vicariance and Dispersal contrasts with vicariance as an explanation for dispersal. Estimated dates that are older than or consistent widespread distributional patterns (Fig. 4). Therefore, knowl- with geological splits support the vicariance hypothesis that edge of processes affecting dispersal of marine organisms is the common ancestor of sister-groups had a contiguous crucial to understanding their evolutionary history. Popu- range and subsequently separated into distinct groups driven lations of coastal species with a planktonic larval stage are by geological events. By contrast, estimated dates that are usually assumed to be demographically open and highly younger than the formation of physical barriers point to connected (Becker et al., 2007). Larvae of some marine taxa dispersal. In this case, animals arose in one biogeographic

Biological Reviews 93 (2018) 874–896 © 2017 Cambridge Philosophical Society 890 Zhonge Hou and Shuqiang Li region and subsequently experienced long-distance dispersal Central American Seaway. Ultimately, the ancient Tethys to establish new populations. Dispersal followed by split into the EP, WA, EA, MS and IWP (Fig. 1). Quaternary vicariance has been found in galaxiid fishes (Burridge et al., sea-level changes resulted in the connection and separation 2012) and cave shrimps (Botello et al., 2013). The dispersal of the MS, Black and Caspian seas. This restricted exchange hypothesis predominates for biota on islands that have never between the Indian and Pacific oceans. The geological been connected to continental shelves, such as volcanic changes undergone by the Tethys reshaped marine habitats, islands (Gillespie et al., 2012; Botello et al., 2013) and recent and created new freshwater, inland cave and anchialine exchanges between continents and islands (Burridge et al., habitats. 2013). Diversity in the Tethyan region results from long-term (2) The ancient Tethys provided an open seaway evolution. Vicariant or dispersal processes can work in between the developing Atlantic and Pacific oceans before concert to explain contemporary patterns of diversification. the Cenozoic, but subsequent expansion of the Atlantic Vicariance best explains ancient biogeographic patterns, Ocean was a barrier to benthic organisms between the while dispersal best explains patterns within biogeographic EA and WA. Explicit, phylogeny-based studies document regions. that the mid-Miocene Tethyan closure separated Atlantic and IWP marine organisms, and the Central American Isthmus induced the split between EP and WA species pairs. The vicariance hypothesis best explains these VIII. FUTURE DIRECTIONS diversification patterns. Population genetics shows that MSC and Quaternary climatic oscillations provided dispersal The ancient Tethyan region experienced drastic geological routes for freshwater faunas between the European mainland changes. It provides an excellent setting for testing evolu- and Mediterranean islands, thus causing range expansion. tionary and ecological hypotheses. Future research should The tectonic events associated with Tethyan closure centre on four key problems. (i) Geological and biodiversity are responsible for the shift in the biodiversity hotspot data are accumulating rapidly for taxa on the north side of to the IWP. the Tethys, but comparable information for the southern (3) The vanishing Tethys reduced the extent of marine region is limited. Dated geological reconstructions and habitats and led to their extinction. New freshwater, cave biodiversity surveys in the southern Tethys will facilitate and anchialine habitats provided new unoccupied niches a far better understanding of the influence of Tethyan for marine-originated animals and triggered their rapid changes on aquatic diversification. (ii) Many previous diversification. Some marine-derived organisms colonised studies have hypothesised that Tethyan changes triggered freshwater habitats once and then expanded far inland, while aquatic diversification. However, few have provided a full others invaded continental habitats multiple times along set of complementary analyses involving molecular dating, continental margins. Relictual lineages inhabit anchialine biogeography and assessments of diversification rate. Such caves around Tethyan margins. analyses can merge geological events and biotic interactions (4) Vicariance and dispersal drove diversity at different into a single integrative framework of evolutionary history. spatial and temporal scales. Vicariance is responsible (iii) Habitat shifts from marine to freshwater and insular or for diversifications between biogeographic regions, while anchialine caves occur in various aquatic animals. However, dispersal dominates population structuring. Divergence-time the mechanisms of adaptation remain poorly understood. estimations can differentiate between the vicariant or Future genomic, transcriptiomic and proteomic analyses dispersal hypotheses. will contribute an understanding of adaptation to different (5) Although many well-sampled phylogenies provide a salinities. (iv) Palaeogeologic and palaeoclimatic changes framework for aquatic biota diversification, the driver(s) define patterns of diversification. It remains unknown how of biodiversity in the Tethyan region remain an enigma. current climatic change influences local biodiversity, and Comparisons of various organisms and applications of new how animals respond to environmental change. genomic and statistic methods could uncover a general pattern. Such information may allow forecasts of the impact of future climatic change on biodiversity, which could help IX. CONCLUSIONS to preserve biodiversity.

(1) The Tethys Ocean was the most geologically changed region across the tropical marine environment. Its complex X. ACKNOWLEDGEMENTS topography ranges from marine to Alpine–Himalayan mountain ranges and this provided various habitats for The manuscript benefitted greatly from comments by aquatic biota diversification. The development of tectonic editors Sara Lees and Alison Cooper. We thank Robert W. theory has clarified the geological history of the Tethys Murphy, Peter Cowman, Boris Sket and two anonymous Ocean. The ancient Tethys passed through the Atlantic reviewers for their valuable comments on an earlier version opening, and its closure resulted from convergence of the of this manuscript. This study was supported by the Strategic Arabian block with Eurasia, the MSC, and loss of the Priority Research Program, Chinese Academy of Sciences

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(Received 12 July 2016; revised 12 September 2017; accepted 13 September 2017; published online 12 October 2017)