Fluviphylax, Whitley, 1965

Bragança, Pedro H. N. & Costa, Wilson J. E. M., 2018, Time-calibrated molecular phylogeny reveals a Miocene-Pliocene diversification in the Amazon miniature killifish genus Fluviphylax (Cyprinodontiformes: Cyprinodontoidei), Organisms Diversity & Evolution (New York, N. Y.) 18 (3), pp. 345-353 : 350-351

Fluviphylax diversification and paleogeographical evolution of northern South America during Miocene and Pliocene

Our time-calibrated analysis indicated that the ancestor of the Fluviphylax lineage diverged from its sister group, a clade comprising anablepids and poeciliids in the Eocene, at about 37 Mya ( Fig. 3 ). Considering that basal lineages of anablepids (e.g., genera Oxyzygonectes and Anableps ) and poeciliids (e.g., Tomeurus and Phalloptychus ) are uniquely found in estuarine brackish waters of tropical America ( Ghedotti 1998; Lucinda 2003), a common condition among new world cyprinodontoids (e.g., Rosen 1973), we assume that the ancestor of Fluviphylax lived in similar habitats. Although there are no available records for Fluviphylax species inhabiting brackish water, the distribution of F. palikur , the most basal species of the genus, along coastal river basins ( Fig. 1 ) may be an indicative of this past brackish water tolerance.

In contrast to F. palikur , the clade comprising all other species of Fluviphylax is distributed in the western-central Amazon River basin and in the Orinoco River basin ( Fig. 1 ). This distribution pattern is geographically partially concordant with the Miocene Pebas lake-wetland system (about 24–11 Mya), which was fed by Andean rivers in the west, small cratonic drainages in the east, and connected to the sea in the present Venezuela Caribbean coast (e.g., Wesselingh and Salo 2006; Wesselingh and Hoorn 2011). Based on paleontological pore and spore data, Hoorn (1993, 1994) has found evidence that the Pebas system was mostly a freshwater environment, affected by some episodically marine introgression events. More recently, Jaramillo et al. (2017) described two main introgression events in the Pebas system, one in the Early Miocene between 18.1 and 17.2 Mya and the other in the Middle Miocene between 16.1 and 12.4 Mya. Therefore, the divergence timing analysis indicating a split between F. palikur and the Amazon-Orinoco clade at about 16 Mya supports the hypothesis that the ancestor of the Amazon-Orinoco Fluviphylax clade colonized the Pebas system during a Middle Miocene marine introgression event.

According to our analysis, species diversification within the Amazon-Orinoco Fluviphylax clade took place between the Late Miocene (about 10 Mya) and Pleistocene (about 1 Mya). This timing is congruent with the establishment of the modern Amazon River basin configuration, as a consequence of continuing uplift of the Eastern Cordillera in the Late Miocene ( Hoorn et al. 1995; Dias de Gamero 1996). Andean-derived sediments reached the Amazon fan between 11.8 and 11.3 Mya, evidencing the breaching of the Purus arch and consequently the establishment of an east-flowing transcontinental Amazon River ( Figueiredo 2009, 2010; Wesselingh and Hoorn 2011). Around 10–8 Mya, Andean uplift in northern South America resulted in the rise of the Vaupés arch, leading to the capture of the Negro river drainage from the Orinoco River basin to the Amazon basin ( Dias de Gamero 1996; Winemiller and Willis 2011). The Vaupés arch represents the main divide between the Negro and the Orinoco river drainages and is considered to be responsible for some differentiation between the fish fauna of both river drainages ( Winemiller and Willis 2011). The split between Fluviphylax sp. A , endemic to Orinoco River basin and an adjacent area of the upper Negro river drainage ( Fig. 1 ), and the clade containing all other species of the Amazon-Orinoco Fluviphylax clade, estimated to have an age of about 10 Mya, is thus contemporary with the Vaupés arch uplift. The present common occurrence of Fluviphylax sp. A in both Orinoco and Negro drainages may be explained by a former isolation in the Orinoco basin just after the rise of the Vaupés arch, follow- ed by recent dispersal to the upper Negro drainage as a consequence of the present low topographic relief between the Orinoco and Negro watersheds, which have allowed ephemeral and year-round connections, thus enabling gene flow between fish populations from the Negro and Orinoco river drainages ( Winemiller et al. 2008; Winemiller and Willis 2011).

The capture of the upper Negro river drainage by the Amazon River allowed the subsequent dispersion of Fluviphylax over central Amazon River basin. The continuous Andean uplift led to a change in the amount of Andean sediments carried by the Amazon River, and around 7 Mya sedimentation rates in the Amazon fan increased ( Figueiredo 2009, 2010). Probably, Fluviphylax dispersed over the Amazon basin before the increase in sediment rate transport and between the series of periodic marine transgressions events that happened in the Late Miocene. According to our date estimates, the increase in the sediment load over the Amazon-Solimões River and the marine transgression events resulted in the initial diversification of the clade comprising species endemic to central Amazon around 9 Mya. Later, about 6.5 Mya, the increase in the sediments outflow in the Solimões and in the Madeira River basin resulted in the split between F. pygmaeus , endemic to the Madeira river drainage, and F. simplex , widespread along Solimões-Amazon floodplains. This disjunction may have been favored by the subsequent uplift of the Fitzcarrald ridge about 4 Mya, a major event in southwestern Amazon, responsible for compartmentalization of Solimões-Amazon and Madeira drainages ( Espurt et al. 2007; Espurt et al. 2010).

In the Pliocene, around 5–4 Mya, the Contigo and Uraricoera river drainages that formerly flowed northward to the Proto-Berbice river drainage were captured by the Branco river drainage, drastically changing the chemical composition of sediment inflow into the Negro River ( Ferreira et al. 2007; Lujan and Armbruster 2011; Lujan et al. 2014). The influence of the Branco River sediment discharges over the distribution of fishes in the Negro river drainage probably contributed to Fluviphylax diversification. Schneider et al. (2012) proposed that the Branco River acted as an ecological barrier between middle and lower Negro River populations of the characiform Carnegiella strigata . According to our dated analysis, around 9 Mya, Fluviphylax species occurring in the Negro river drainage, split in two distinct groups ( Fig. 3 ). One of these groups indicates a split of F. zonatus , from the Negro River drainage below Branco River mouth, and Fluviphylax sp. B , from the middle Negro drainage just above Branco River mouth ( Fig. 1 ) at about 1 Mya, which is here assumed to be a result of the continuous sediment inflow of the Branco River waters into the Negro River acting as a barrier to gene flow.

Figures

Fig. 3 Time-calibrated phylogeny of the Cyprinodontoidei and Fluviphylax obtained from the Bayesian dating analysis in Beast v.1.8. Bars represent maximum and minimum date estimates for each node, and the numbers are node divergence mean ages. Arrows indicate the nodes

Fig. 1 Distribution map of Fluviphylax: F. obscurus (white dot), F. palikur (orange dot), F. pygmaeus (yellow dot), F. simplex (blue dot), F. zonatus (red dot), Fluviphylax sp. A (green dot), Fluviphylax sp. B (brown dot), and Fluviphylax sp. C (purple dot)