River capture or ancestral polymorphism: an empirical genetic test in a freshwater fish using approximate Bayesian computation

Mateus S Souza, Andréa T Thomaz, Nelson J R Fagundes

Abstract

A headwater or river capture is a phenomenon commonly invoked to explain the absence of reciprocal monophyly of genetic lineages among isolated hydrographic basins in freshwater fish. Under the assumption of river capture, a secondary contact between populations previously isolated in different basins explains the observed genetic pattern. However, the absence of reciprocal monophyly could also arise under population isolation through the retention of ancestral of polymorphisms. Here, we applied an approximate Bayesian computation (ABC) framework for estimating the relative probability of scenarios with and without secondary contact. We used Cnesterodon decemmaculatus as a study model because of the multiple possible cases of river capture and the demographic parameters estimated in a previous mitochondrial DNA study that are useful for simulating scenarios to test both hypotheses using the ABC framework. Our results showed that, in general, mitochondrial DNA is useful for distinguishing between these alternative demographic scenarios with reasonable confidence, but in extreme cases (e.g. recent divergence or large population size) there is no power to discriminate between scenarios. Testing hypotheses of drainage rearrangement under a statistically rigorous framework is fundamental for understanding the evolution of freshwater fish fauna as a complement to, or in the absence of, geological evidence.

Figure 1. A, sampling sites for Cnesterodon decemmaculatus. The inset shows the location of the study area (highlighted in a red square) in South America. Grey lines indicate country borders, and areas in different colours indicate different basins (blue, Southern; coral, Merín; green, Uruguay; grey, Negro). Haplotypes found in each sampling site (dots) are indicated. B, median-joining network for ND2 haplotypes. The size of the circles is proportional to haplotype frequency. Ticks on haplotype connections indicate the number of mutational steps. Original artwork based on the data from Ramos-Fregonezi et al. 2017.

Figure 2. Coalescent demographic scenarios. A, DIVISO (divergence and isolation). B, SECCON (secondary contact). C,
SECCONinv (secondary contact with inverted direction of gene flow). D, SECCONrgf (secondary contact with reciprocal gene flow). Abbreviations: Anc Pop, ancestral population; Mig1 and Mig2, migration parameters; Pop 1 and Pop 2, populations 1 and 2 (U-N: Pop 1, Uruguay and Pop 2, Negro; N-M: Pop 1, Merín and Pop 2, Negro; N-S: Pop 1, Negro and Pop 2, Southern; U-S: Pop 1, Southern and Pop 2, Uruguay); T0, present time; Td, time since divergence; Tsc, time since secondary contact. Migration parameters are represented backwards in time (e.g. Mig1 in scenario B represents the proportion of genetic lineages in Pop 1 that return to Pop 2 in Tsc).