A relative of the Ganges and Indus river dolphins from Miocene deposits of the Amazonian basin: multiple toothed whale invasions of freshwater environments?

During their transition to the marine environment, in addition to numerous morphological changes, early cetaceans had to evolve physiologically to face the excess of salt due to the ingestion of seawater. But evolution is complex, far from being a process with one way. After this critical Eocene step of their evolutionary history, followed by several phases of diversification of fully marine cetaceans (leading to the two extant suborders, Mysticeti, the baleen whales, and Odontoceti, the toothed whales), members of several odontocete clades independently recolonized freshwater environments. Nowadays, four species in the genera Inia, Lipotes (possibly recently extinct), and Platanista (two species), exclusively occupy river and lake habitats, respectively in the Amazon-Orinoco, Yangtse, and Ganges-Indus river basins. Based on morphological and molecular data, as well as on paleontological information on their fossil relatives, it has been demonstrated that Inia, Lipotes, and Platanista are relict members of ancient lineages with distantly related marine ancestors. Among them, the endangered Platanista is interesting for several reasons. In addition to its unusual cranial morphology, this nearly blind dolphin is the sole survivor of the superfamily Platanistoidea, much diversified from the late Oligocene up to the middle Miocene. Among platanistoids, the fossil record of Platanistidae is dominated by members of the extinct subfamily Pomatodelphininae, most of them discovered in marine to estuarine Miocene layers. Only one fragmentary mandible, from marine deposits of the early Miocene of Oregon, has been tentatively referred to the subfamily Platanistinae, the clade typified by the extant Platanista. We report on the discovery of an isolated platanistid periotic (ear bone, one of the most diagnostic elements in crown cetaceans) found in late middle Miocene sediments of the Fitzcarrald Arch area, Peruvian Amazonia. This periotic is identified as belonging to a platanistine, based on several derived characters shared with Platanista. Even if fragmentary, this is likely the most significant fossil record of a platanistine, partly filling the temporal gap between the emergence of the subfamily and the Recent Platanista. Interestingly, this specimen was found in a geographic area now occupied by Inia. Sedimentology and associated fauna indicate that this middle Miocene depositional area corresponds to an inland tidally-influenced freshwater/oligohaline basin. Although a marine origin cannot be discarded for this new fossil platanistine record, it is tempting to hypothesize that it illustrates an early step of the colonization of a freshwater habitat, in a region very far from the area of Platanista. If confirmed, this interpretation would further support the scenario of multiple Miocene freshwater invasions by members of several odontocete clades. Reasons for such drastic ecological changes are not yet clear, and several factors, both biological (competition with diversifying pelagic delphinoids, flight from oceanic predators, migration of prey in freshwater regions) and physical (sea level changes and temperature fluctuation), might have played a role. Species of three strictly freshwater odontocete genera survived until the Holocene, and one of them probably went extinct at the dawn of a twenty-first century that will be decisive for the fate of the remaining others.