Evolution of the Yangtze River and its biodiversity

Abstract

Documenting the origins of megadiverse (sub)tropical aquatic ecosystems is an important goal for studies of evolution and ecology. Nonetheless, the geological and ecological establishment of the modern Yangtze River remains poorly understood. Here, we reconstruct the geographic and ecological history of an endemic clade of East Asian fishes based on the mitochondrial phylogenomics analysis of Cyprinidae using 15 fossil calibrations. We estimate an ancestral condition of benthic spawning with demersal or adhesive eggs in southern East Asia before ∼23 Ma and a derived condition of riverine spawning with semibuoyant eggs in the Yangtze by ∼18 Ma. These results imply the formation of Yangtze riverine ecosystems around the Oligocene-Miocene boundary in response to plateau uplift and monsoon strengthening. Some of these cyprinids reverted to benthic spawning with adhesive eggs by ∼15 Ma, a time of rising to peak net diversification rates, indicating the formation of potamo-lacustrine ecosystems by the mid-Miocene during a strong East Asian summer monsoon. Our study provides increased spatiotemporal resolution for the co-evolutionary histories of the Yangtze River and its biodiversity and highlights biological evidence concerning the geomorphological dynamics of the Yangtze River.

Introduction

The origins of the modern Yangtze River and evolution of drainage systems in South and East Asia were linked to Neogene uplift of the Qinghai-Tibetan Plateau and onset of the modern Asian monsoon system.^1,2 The upper palaeo-Yangtze River (palaeo-Jinshajiang) originally flowed southward from sources in central Asia toward the South China Sea, but was diverted eastward in response to tectonically driven surface uplift to form the modern Yangtze River.^1,2 However, deriving an accurate understanding of the spatiotemporal evolution of the Yangtze River system has been challenging. Earlier geological studies argued for the initial diversion of the palaeo-Jinshajiang to the east at the First Bend and the incision of the Three Gorges dating from the Eocene to as recent as the Pleistocene, with estimates based on different sampling locations, dating methods, and proxies.

There is a growing scientific consensus that the geomorphological process of river capture contributes substantially to evolutionary diversification in freshwater fishes. In turn, reconstruction of the phylogeographic dynamics of freshwater fishes can help to constrain the spatiotemporal evolution of the river system. Previous studies have shown that an endemic clade of East Asian Cyprinidae evolved under the influence of a strong East Asian monsoon during the uplift of the Qinghai-Tibetan Plateau with adaptations to these unique climatic and hydrological conditions.³ In this endemic East Asian cyprinid clade, some fishes show benthic spawning with adhesive or demersal eggs, while others exhibit riverine spawning with semibuoyant eggs. Semibuoyant eggs are considered to be a key trait used by East Asian cyprinids to survive in large river environments with heavy seasonal precipitation, ie, a monsoonal climate.³ The earliest fossils of the endemic clade of East Asian Cyprinidae spawning semibuoyant eggs, ie, Ctenopharyngodon, Hypophthalmichthys, and Elopichthys, were found in the Lower Miocene strata of the Sihong Basin in the lower reaches of the Yangtze basin.⁴ The appearance of their ancestor can be used to indicate the establishment of the modern river ecological system and, logically, the formation of the Yangtze River close to its modern state. However, to date, the historical distribution and dispersal of endemic cyprinids across East Asia or the possible relationship between the spatiotemporal development of the Yangtze River and the evolution of egg types of endemic East Asian cyprinids has not been addressed.

From this perspective, we reconstruct the largest molecular phylogeny of the endemic clade of East Asian cyprinids based on the mitochondrial phylogenomics analysis of 118 Cyprinidae species, including all 9 subfamilies of Cyprinidae, 34 of the 44 valid genera (77%), and 71 of the 151 valid species (47%) of the endemic East Asian cyprinids (Figure 1A). We estimate the divergence times for Cyprinidae by using 15 fossil calibrations and infer the diversification dynamics, ancestral distribution and egg types of the endemic East Asian cyprinids based on the time-calibrated phylogeny. Combining all the evidence, we discuss the age at which the southward-flowing palaeo-Jinshajiang first connected with the middle reaches via the First Bend and formed the Yangtze River ecosystems, including the potamo-lacustrine ecosystems in the middle and lower reaches.

Figure 1.

Phylogeny of Cyprinidae and diversification history of endemic East Asian cyprinids

(A) Phylogeny of 118 Cyprinidae species and three Cobitidae species inferred from mitochondrial genomes based on Bayesian inference analysis.

(B) Egg type evolution (a) and schematic diagram of the historical distribution and dispersal (b–d) of the endemic East Asian clade of Cyprinidae under the development of the Yangtze River system in response to uplift of the Qinghai-Tibetan Plateau. Red dots indicate fossil sites.

(C) Diversification dynamics and macroevolutionary patterns of endemic East Asian cyprinids. (a) A single rate shift configuration with the maximum a posteriori probability represented as a phylorate plot of the endemic East Asian cyprinids showing variation in speciation rates. (b) The rate-through-time plot of the endemic East Asian cyprinids implemented by Bayesian Analysis of Macroevolutionary Mixtures. (c) Net diversification rate through time for the endemic East Asian cyprinids inferred from the relationship between the net diversification rate and East Asian monsoon in RPANDA. (d) The hematite/goethite proxy of ODP Site 1148 in the South China Sea as a function of time (modified from Clift et al.¹⁰).

Results and discussion

The palaeo-Jinshajiang flowing southward in the Oligocene

Relationships among major lineages of Cyprinidae are well supported by Bayesian inference analysis (Figure 1A). The main clades of the phylogenetic tree are compatible with those from previous studies.⁵ Our results show that the ancestors of the endemic East Asian cyprinid clade, which possesses benthic spawning with demersal or adhesive eggs, appeared before the late Oligocene (∼23 Ma; 95% CI: 20.2–25.3 Ma), including metzins, aphyocyprins, and opsariichthyins (Figure 1Ba). Combined with the fossils of †Ecocarpia ningmingensis in the Ningming Basin, Guangxi Province,⁶ and the distribution of extant species, we infer that their ancestors were most likely distributed within the palaeo-Pearl and palaeo-Red rivers before ∼23 Ma in southern East Asia (Figure 1Bb). This implies that the modern Yangtze River had not yet been formed and that the palaeo-Jinshajiang likely flowed toward the south, connecting with a stream similar to the modern Red River.

Other evidence suggests that the palaeo-Jinshajiang once flowed southward into the South China Sea. Studies using ⁴⁰Ar/³⁹Ar mica dating and zircon U-Pb dating methods coupled with statistical analysis suggest that a major Palaeogene river probably originated in the southeastern Qinghai-Tibetan Plateau and flowed through the Jianchuan Basin, extending to northern Vietnam during the late Eocene-Oligocene.⁷ This drainage had disappeared by the early Miocene. Furthermore, schizothoracine fishes commonly live on the Qinghai-Tibetan Plateau and surrounding areas at elevations of 1,250–4,750 m above sea level (a.s.l.).⁸ The time-calibrated phylogeny of Cyprinidae reveals that schizothoracine fish endemic to the Qinghai-Tibetan Plateau did not appear before ∼24 Ma. Combined with palaeontological evidence,⁹ we infer that the elevation of the central Qinghai-Tibetan Plateau was quite low in the Oligocene. Reorganization of rivers did not occur during the Eocene because the southeastern part of the plateau was not uplifted significantly until the Oligocene.⁷ These results indicate that the middle and lower reaches of the Yangtze River system had not yet been connected to the Jinshajiang, consistent with our new biological dating for the southern flow of the palaeo-Jinshajiang in the Oligocene.

The formation of the Yangtze River near the Oligocene-Miocene boundary

Fishes with semibuoyant eggs consisting of squaliobarbins and hypophthalmichthyins existed in the Yangtze River during the early Miocene (∼18 Ma; 95% CI: 16.2–19.6 Ma) (Figure 1Ba). The earliest fossils of Hypophthalmichthys, Ctenopharyngodon, and Elopichthys are found in the Lower Miocene strata of the Sihong Basin, Jiangsu Province.⁴ These results indicate that the endemic East Asian cyprinids dispersed to the position of the current Yangtze River and evolved into fishes laying semibuoyant eggs by ∼18 Ma (Figure 1Bc), suggesting that the Yangtze River had reversed its flow toward the east and formed the present drainage ecosystems before that time, close to the Oligocene-Miocene boundary (∼18–23 Ma). The hematite/goethite proxy from Ocean Drilling Program (ODP) Site 1148 in the South China Sea,¹⁰ which is positively correlated with the strength of East Asian monsoons, began to rise after 23 Ma and peaked at ∼18 Ma (Figure 1Cd). This indicates that the climate in East Asia became humid at that time. Abundant rainfall was conducive to the formation of a major Yangtze River system with high discharge.

Geological studies constrain the age of formation of the present Yangtze River system to 23.0–36.5 Ma based on ⁴⁰Ar/³⁹Ar dating of basalts and U-Pb dating of zircon sand grains from the lower reaches of the Yangtze River, as well as the appearance of evaporites and lacustrine sedimentation in the Jianghan Basin.² This result is close to the date of Yangtze River formation we estimate from the timing of divergence of the semibuoyant egg group. In addition, specialized schizothoracine fishes mostly live in the Qinghai-Tibetan Plateau at an elevation of >2,750 m a.s.l.⁸ Based on the results of the time-calibrated phylogeny of schizothoracine fishes, the timing of divergence between primitive and specialized grades was likely ∼18 Ma, indicating that the central and SE plateau had reached a high elevation by the early Miocene. The surface of the SE Qinghai-Tibetan Plateau was uplifted when the ductile lower crust beneath the central plateau flowed toward the plateau margin starting from the late Oligocene to the early Miocene. At the same time, large-scale strike-slip faults linked to the eastward extrusion of rigid crustal blocks away from the point of collision with the Indian block resulted in the reversal or capture of river systems.^1,2 As a result, we argue that the Yangtze River diverted its flow from being toward the south to eastward and through the Three Gorges to form the modern river system at that time.

Formation of the middle Miocene potamo-lacustrine Yangtze River ecosystems

Based on the diversification dynamics from the Bayesian Analysis of Macroevolutionary Mixtures and RPANDA analyses (Figures 1Ca–1Cc), the net diversification rate of the endemic East Asian cyprinids rose to a peak at ∼15 Ma, together with a significant rate shift configuration in the maximum a posteriori probability. These results imply that the drainage network in the Yangtze River basin provided a large number of niches, facilitating rapid radiation and dispersal of fishes. In the middle Miocene (∼15 Ma; 95% CI: 13.9–16.9 Ma), fish laying adhesive eggs arose again, including xenocyprins and cultrins (Figure 1Ba). This finding indicates that, to adapt to the lake environment, endemic East Asian cyprinids evolved into fishes spawning adhesive eggs that attached to aquatic plants to develop. This implies that the potamo-lacustrine ecosystems of the Yangtze River had appeared by the middle Miocene (Figure 1Bd). Coincidentally, the sedimentary hematite/goethite proxy rapidly rose to a peak at ∼15 Ma at ODP Site 1148 in the South China Sea (Figure 1Cd).¹⁰ This indicates that the climate in East Asia was humid and associated with a strong summer monsoon season at that time. The strong precipitation could have sustained a potamo-lacustrine ecosystem in the Yangtze River, greatly increasing species diversification.

Taken together, our results indicate that, before the formation of the Yangtze River, the ancestors of endemic East Asian cyprinids were confined to southern East Asia between the palaeo-Pearl and palaeo-Red Rivers during the Oligocene. At that time, the palaeo-Jinshajiang flowed southward to the South China Sea roughly along the course of the modern Red River. Endemic East Asian cyprinids dispersed into the Yangtze River basin and evolved into fishes laying semibuoyant eggs by ∼18 Ma, which suggests that a modern Yangtze riverine ecosystem had formed around the Oligocene-Miocene boundary (∼18–23 Ma) in response to regional surface uplift and large strike-slip tectonics and climatic changes. Notably, the endemic clade of East Asian cyprinids evolved into fishes spawning adhesive eggs again by ∼15 Ma, coinciding with an increase to a peak in the net diversification rate of this endemic clade and a high intensity of the East Asian summer monsoon. This indicates that the Yangtze River system probably had developed into a potamo-lacustrine ecosystem with high productivity by the middle Miocene. Our studies constrain the ages of important events in the geological and ecological evolution of the Yangtze River from a biological perspective, helping us to understand the evolutionary history of the Yangtze River system and providing a new paradigm for the reconstruction of river-lake ecosystems.

Published Online: March 21, 2023