Phylogeography of the Chocó Endemic Rainbow Characin (Teleostei: Rhoadsia)
South America's Chocó, part of the North Andean Pacific Slopes–Rio Atrato ecoregion, is a biodiversity hotspot with many disjunct rivers, yet phylogeographic and population genetic studies of the Chocó's aquatic species are scarce. Rhoadsia is a Chocó endemic freshwater fish genus with two recognized species: R. minor from the upper Esmeraldas River drainage and R. altipinna from the lower Guayas River drainage, Ecuador. Little is known about the evolutionary history of Rhoadsia, and due to morphological similarities, the validity of the two nominal species has been questioned. We conducted a phylogeographic study using two mitochondrial genes and 12 microsatellite markers to examine the evolutionary history of Rhoadsia and the validity of its two species. Samples collected in drainages throughout western Ecuador from sea level to 1260 m.a.s.l. were included, as were samples of species in the closely related genera Parastremma and Carlana from Colombia and Central America. Phylogenetic analysis of the mtDNA markers confirmed the reciprocal monophyly of a northern and southern clade, and the presence of mitochondrial haplotypes of both clades in the northern Guayas basin. Structure analysis with the microsatellite markers pointed to introgression at the border between the species ranges as the likely cause of the mixing of mitochondrial haplotypes in the northern Guayas. Bayesian analysis of the microsatellite data revealed the existence of ten populations throughout western Ecuador, divided into three main geographically segregated groups. Group I coincided with the northern distribution of R. minor, while groups II and III seemed to represent geographic subgroups of R. altipinna in the Guayas and southern coastal drainages. Patterns of genetic divergence and diversity support the recognition of multiple evolutionarily significant units within both species and allowed reevaluation of previously reported freshwater biogeographic zones in the Ecuadorian Chocó. This study provides a baseline for future studies examining freshwater biogeographical patterns throughout the Ecuadorian Chocó, as well as a phylogeographic framework to examine the genetic basis of adaptation of morphologically divergent populations of Rhoadsia inhabiting Andean mountain streams in the region.
Live photos of Rhoadsia spp. (A) Male Rhoadsia minor, ROM 93672, from the Silanchi River, Esmeraldas River drainage; (B) female Rhoadsia minor, ROM 93696, from the Leilia River, Esmeraldas River drainage; and (C) male Rhoadsia altipinna, ROM 93791, from the Santa Rosa River. All scale bars = 1 cm.
Map of Ecuador showing the sites and drainages in western Ecuador sampled for this study. The drainages are colored in gray and labeled in bold. The sites are represented with different symbols referring to their respective drainage. Streams related to the sites sampled are highlighted. Meaning of site codes can be seen in Table 1. Scale of map, 1:390000.
Frequency of cytochrome b haplotypes (Cyt-b, left) and cytochrome oxidase I (COI, right) per site. Haplotypes colored in white correspond to private haplotypes (PH; i.e., haplotypes that are unique to a particular site). The bottom left corner graphs (a and b) present the haplotype frequency showing the number of individuals sampled in each drainage. Su-At (Sua and Atacames combined), Esm (Esmeraldas), Gua-Ta (Guayas and Taura combined), SP (San Pablo), Jub (Jubones), and SR (Santa Rosa).
Haplotype network for the mitochondrial genes cytochrome b (Cyt-b, top) and cytochrome oxidase I (COI, bottom) color coded by site. The size of the circles is proportional to the haplotype frequency. The number of mutations between the haplotypes are represented by hatch marks. The populations within drainages are represented by different color shades (see legend). Haplotypes fall into two groups: the northern (N, enclosed by blue dashed line) and the southern group (S, enclosed by red dashed line).
Bayesian phylogenetic trees based on the mitochondrial genes cytochrome b (Cyt-b, left) and cytochrome oxidase I (COI, right). Nodes supported by posterior probabilities greater than 0.7 are displayed with black dots unless specified (arrow). Clade I (blue) comprised populations from the northern region, while Clade II (red) is represented by populations from the southern region. The format for the label of the ingroup is: Site code_Drainage code_Haplotype number_Year_(number of individuals with identical haplotype). For the outgroup, it is: Species code_Country code_Sample ID_(Number of individuals with identical haplotype).
Structure analysis of populations of Rhoadsia in Ecuador based on 12 microsatellites. Neighbor-joining of clusters (K = 10) inferred in STRUCTURE (top left). Proportion of membership of each cluster per site (top right). Proportion of membership of each cluster assigned to each individual (bottom). Clusters fell into three main groups (I, II, and III) based on the distance matrix generated in STRUCTURE. We tentatively recommend recognition of the ten clusters from the STRUCTURE analysis as evolutionarily significant units (ESUs).
Contributor Notes
Associate Editor: M. P. Davis.