Landscape dynamics and diversification of the megadiverse South American freshwater fish fauna

Landscape dynamics are widely thought to govern the tempo and mode of continental radiations, yet the effects of river network rearrangements on dispersal and lineage diversification remain poorly understood. We integrated an unprecedented occurrence dataset of 4,967 species with a newly compiled, time-calibrated phylogeny of South American freshwater fishes—the most species-rich continental vertebrate fauna on Earth—to track the evolutionary processes associated with hydrogeographic events over 100 Ma. Net lineage diversification was heterogeneous through time, across space, and among clades. Five abrupt shifts in net diversification rates occurred during the Paleogene and Miocene (between 30 and 7 Ma) in association with major landscape evolution events. Net diversification accelerated from the Miocene to the Recent (c. 20 to 0 Ma), with Western Amazonia having the highest rates of in situ diversification, which led to it being an important source of species dispersing to other regions. All regional biotic interchanges were associated with documented hydrogeographic events and the formation of biogeographic corridors, including the Early Miocene (c. 23 to 16 Ma) uplift of the Serra do Mar and Serra da Mantiqueira and the Late Miocene (c. 10 Ma) uplift of the Northern Andes and associated formation of the modern transcontinental Amazon River. The combination of high diversification rates and extensive biotic interchange associated with Western Amazonia yielded its extraordinary contemporary richness and phylogenetic endemism. Our results support the hypothesis that landscape dynamics, which shaped the history of drainage basin connections, strongly affected the assembly and diversification of basin-wide fish faunas.

Geological and climatic events are widely believed to shape the biodiversity of continental biotas (1–3), yet we are only beginning to understand the nuanced ways in which individual geological and climatic events have contributed to evolutionary diversification (speciation minus extinction) across large spatial scales (4–7). South America harbors the most diverse fauna of continental freshwater fishes in the world (~5,750 species), providing unique opportunities to study the effects of geological history and river dynamics on diversification in obligate aquatic taxa (8, 9). Hydrogeographic processes, operating over tens of millions of years, have caused predictable changes in the geometry of river drainage networks, by isolating and merging portions of adjacent river basins and their connections to the sea, and by altering the physiochemical characteristics of water discharge (10, 11). Here, we evaluate the influence of major geological events on diversity patterns of obligate freshwater fishes of South America over the past 100 Ma, the time period over which hydrogeographic events shaped the origins of modern fluvial systems (4, 5, 12). We conducted the most comprehensive assessment of diversification in this group to date, using an extensive dataset on species geographic occurrences and a newly compiled, species-dense phylogeny of South American freshwater fishes (13). This new synthesis afforded us the opportunity to link unique hydrogeographic events with the spatial and temporal diversification and dispersal of individual fish clades.The historical dynamics of South American river basins and aquatic biotas were strongly shaped by four prominent geophysical events (Fig. 1) (11, 14). The first was the final separation of South America from Africa during the Late Cretaceous (c. 100 Ma). Between the Late Cretaceous and Early Paleogene (c. 100 to 55 Ma), river drainage patterns of South America were controlled by the location of the preexisting continental uplands (cratons and shields), ongoing uplift of the Andean cordilleras, super greenhouse climatic conditions characterized by high temperatures and precipitation, and dramatically fluctuating eustatic sea levels. As a result, most low-elevation coastal plains and interior structural basins were covered by nearshore marine habitats, and upland freshwater riverine and riparian habitats were intermittently isolated and connected (4, 15). During the Paleogene (c. 55 to 33 Ma), the Proto-Amazon-Orinoco river basin (Proto-Amazon basin, hereafter) drained the Sub-Andean Foreland basin, including much of northern South America and the northern La Plata region (Fig. 1 A and B; 5, 16).Open in a separate windowFig. 1.Bioregions, principle current landforms and sub-basins, and approximate chronology and location of the principal landscape evolution events that shaped the current drainage basins of South America and influenced the diversification of freshwater fishes. (A) Current river basins and geological formations mentioned in the text and the six bioregions proposed (detailed in SI Appendix). (B–E) Between 100 and 55 Ma, aquatic systems in South America were intermittently connected by multiple marine transgressions and regressions.Thus drainages across the continent during this time were intermittently connected by epicontinental seaways. During this time, the Proto-Amazon basin was the main drainage of northern South America, flowing through the sub-Andean foreland. At the same time, the Paraná and Paraguay basins (La Plata bioregion) represented major aquatic systems in South America (4, 5, 10, 11). Additional information about principal landforms controlling basin connectivity at each time interval and for each bioregion delineation appears in SI Appendix, Table S1.Second, intraplate compression and tectonic subduction along the Pacific margin during the Oligocene (c. 33 to 23 Ma) drove tectonic uplift of the Altiplano and Michicola Arch (c. 30 Ma) associated with formation of the Bolivian Orocline (17). These orogenic deformations intermittently isolated and connected rivers among the Western Amazonian, Upper Madeira, and Upper Paraguay sedimentary basins of the Sub-Andean Foreland, facilitating vicariance and biotic exchanges across their watershed divides (Fig. 1C; 4, 18–20). Third, tectonic reactivation and uplift of Serra do Mar and Serra da Mantiqueira ranges in southeastern Brazil during the Early Miocene (c. 23 to 16 Ma) re-routed some rivers from the La Plata basin directly to the Atlantic (Fig. 1D; 21, 22–24), isolating many terrestrial and aquatic species in the coastal basins of the Atlantic Forest. Also, at about this time (c. 23 to 10 Ma), the Pebas Megawetland extended over large areas of the modern Western Amazonia and Orinoco basins (Fig. 1D; 5, 7, 22–26). Fourth, the uplift of the Northern Andes during the Late Miocene and Pliocene (c. 10 to 4.5 Ma), which profoundly reorganized regional river drainage networks, isolated the modern Amazon, Orinoco, Magdalena, and Maracaibo river basins and connected the modern Western and Eastern Amazon basins, thereby forming the modern transcontinental Amazon River (Fig. 1E; 16, 27).Variation in connectivity and configuration of regional river networks resulting from these four major geological events strongly shaped diversity patterns of the Neotropical freshwater fish fauna (4, 12). In particular, river capture, in which a river drainage system is diverted from its historic bed to a neighboring bed, is a landscape evolution process that exerts a potent influence on diversification in obligate freshwater organisms, because it both severs existing and constructs new corridors of aquatic habitat among portions of adjacent drainage basins (18, 28). Because continental fishes are eco-physiologically restricted to freshwater habitats within drainage basins, watersheds represent natural dispersal barriers, as evidenced by the strong spatial concordance of geographic ranges in freshwater fish species with basin boundaries (28, 29). By isolating and connecting populations of aquatic taxa across watershed divides, river capture exerts complex effects on the diversity of freshwater organisms, for example by elevating extinction risk through geographic-range contraction, promoting speciation by genetic isolation and vicariance, and increasing biotic homogenization by dispersal and gene flow (16, 30–32).Although the role of geological events in shaping the evolution of rivers and freshwater diversity has long been recognized, the relative contributions of particular geological events remain poorly understood. Insights into their contributions can be gained only by studying diversity patterns at appropriate spatial, temporal, and taxonomic scales (28, 33–36). For instance, recent studies identified Western Amazonia as the center of Amazon fish diversity (high species richness, low phylogenetic diversity (PD), and high phylogenetic clustering, compared to Eastern Amazonia), with younger fish lineages dispersing progressively eastward across Amazonia after the formation of the modern transcontinental river c. 10 Ma (37–39). However, this interpretation did not consider the more ancient history of Neotropical fishes in the upland Brazilian and Guianas Shields, the formation of the modern lowland (< 250 m.a.s.l.) fauna in the Proto-Amazon basin, and the phenotypically and taxonomically modern composition of all the known Miocene paleo-ichthyofaunas (4, 40). Taking this deeper history into account, Pliocene and Pleistocene events may have served more as buffers against extinction than as drivers of speciation in the formation of Amazonian fish species diversity (Fig. 2; 15, 41). In fact, the most species-rich clades of Neotropical freshwater fishes are thought to have radiated during the Paleogene (c. 63 to 23 Ma) (4, 42, 43).Open in a separate windowFig. 2.Changes in the rates of net lineage diversification among South American freshwater fishes. Tips represent 2,523 fish species. (A) Branch colors indicate net lineage diversification rate estimated by BAMM, where red indicates highest and blue lowest diversification rates. Significant shifts in diversification rates are shown as pale green circles on the branches. Selected representative clades of Melanorivulus, Orestias, Ancistrini, Hypostomus, and Corydoras species are illustrated. The principal orders are represented by colored columns to the right of the tree tips. The timescale at the bottom is expressed in millions of years ago (Ma). Vertical dashed lines indicate timing of the main principal hydrogeographic events detailed in the inset legend on the left. (B) Rates-through-time plots based on BAMM estimations, considering all bioregions together (see Material and Methods for parametrization details). The shaded areas around the curves correspond to 95% CIs of the estimated rates. Dashed lines indicate the time period when most of shifts in diversification rates were estimated. (C) Rates-through-time plots considering the species present in each bioregion separately. Rates of diversification, speciation, and extinction were estimated mainly within crown taxa. The five photographs: Wikipedia Commons. *Ancistrini species of genera Hopliancistrus, Guyanancistrus, Pseudolithoxus, Lasiancistrus, Pseudancistrus, Panaque, and Pterygoplichthys.In the case of South American freshwater fishes, previous macroevolutionary studies have been hindered by the large number of species (~5,750), remote sampling localities, and logistical difficulties of gathering reliable data (8). Our new data on fish distributions, which we combine with a new, time-calibrated molecular phylogeny, offer powerful resources to study the role of geomorphological events and associated river captures in shaping fish diversity over longer time periods and larger spatial scales than has previously been attempted. In particular, we evaluate the prediction that the high diversity in Western Amazonia was influenced by biogeographical bridges formed across different aquatic systems and time periods, which led to both accelerated diversification rates and a role for Western Amazonia as a principal source of freshwater fish species for all of South America.