Headwater Capture Evidenced by Paleo-Rivers Reconstruction and Population Genetic Structure of the Armored Catfish (Pareiorhaphis garbei) in the Serra do Mar Mountains of Southeastern Brazil

Abstract

Paleo-drainage connections and headwater stream-captures are two main historical processes shaping the distribution of strictly freshwater fishes. Recently, bathymetric-based methods of paleo-drainage reconstruction have opened new possibilities to investigate how these processes have shaped the genetic structure of freshwater organisms. In this context, the present study used paleo-drainage reconstructions and single-locus cluster delimitation analyses to examine genetic structure on the whole distribution of Pareiorhaphis garbei, a ‘near threatened’ armored catfish from the Fluminense freshwater ecoregion in Southeastern Brazil. Sequences of two mitochondrial genes (cytochrome b and cytochrome c oxidase subunit 1) were obtained from five sampling sites in four coastal drainages: Macaé (KAE), São João (SJO), Guapi-Macacu [sub-basins Guapiaçu (GAC) and Guapimirim (GMI)], and Santo Aleixo (SAL). Pronounced genetic structure was found, involving 10 haplotypes for cytB and 6 for coi, with no haplotypes shared between localities. Coalescent-based delineation methods as well as distance-based methods revealed genetic clusters corresponding to each sample site. Paleo-drainage reconstructions showed two putative paleo-rivers: an eastern one connecting KAE and SJO; and a western one merging in the Guanabara Bay (GAC, GMI, and SAL). A disagreement was uncovered between the inferred past riverine connections and current population genetic structure. Although KAE and SJO belong to the same paleo-river, the latter is more closely related to specimens from the Guanabara paleo-river. This discordance between paleo-drainage connections and phylogenetic structure may indicate an ancient stream-capture event in headwaters of this region. Furthermore, all analyses showed high divergence between KAE and the other lineages, suggesting at least one cryptic species in the latter, and that the nominal species should be restricted to the Macaé river basin, its type locality. In this drainage, impacts such as the invasive species and habitat loss can be especially threatening for such species with a narrow range. Our results also suggest that freshwater fishes from headwaters in the Serra do Mar mountains might have different biogeographical patterns than those from the lowlands, indicating a complex and dynamic climatic and geomorphological history.

Species delimitation in Neotropical fishes of the genus Characidium (Teleostei, Characiformes)

“…The remarkable occurrence of two genetically distinct species within the present concept of Characidium alipioi living in sympatry in the Rio Paraíba do Sul might be explained by an event of allopatric speciation followed by subsequent episodes of headwater river captures (Pucci et al, ), as extensively documented for Neotropical freshwater fishes in the southeastern Brazil (Albert & Reis, ; Camelier, Menezes, Costa‐Silva, & Oliveira, ; Lima et al, ; Ribeiro, ; Roxo et al, ) and including species of Characidium (Poveda‐Martínez et al, ; Pucci et al, ). A time‐calibrated hypothesis suggests a species‐level divergence between C. pterostictum and C. vidali from southeastern Brazil during the Pleistocene (~5.5 Myr) possibly due to allopatric speciation that resulted from events of marine incursions and/or headwater river captures (Poveda‐Martínez et al, ).…”

Common barriers, but temporal dissonance: Genomic tests suggest ecological and paleo‐landscape sieves structure a coastal riverine fish community

“…Shared haplotypes and patterns of relatedness between neighboring river basins has classically been used to infer biogeographic histories shaped by past connectivity (e.g., river capture; Lima et al, ; Swartz, Chakona, Skelton, & Bloomer, ), and has been extended to expectations of congruence among community members (Albert et al, ). However, our data shows that a community history shaped by a singular historical event is an oversimplification.…”

Flowing into the unknown: inferred paleodrainages for studying the ichthyofauna of Brazilian coastal rivers

“…For example, using a paleodrainage reconstruction for the southeastern coast of Brazil, it was demonstrated that paleodrainages and its properties account for most of the genetic variation and diversity observed for the characid genus Hollandichthys based on mitochondrial DNA (Thomaz et al, 2015) and next generation sequencing data (Thomaz et al, 2017). Likewise, analyses that took into consideration fluctuations on sea level suggests its role in structuring genetic divergence and demographic history of other members of the coastal ichthyofauna (Baggio et al, 2017;Hirschmann et al, 2017;Lima et al, 2017;Ramos-Fregonezi et al, 2017;Tschá et al, 2016Tschá et al, , 2017.…”

“…Consideration of species-specific effects is therefore an important biological component that needs to balance the abiotic factors that are often invoked for explaining divergence patterns (reviewed in Papadopoulou, Knowles, 2016). For example, it is possible that yet unknown river capture events might contribute to divergence patterns that do not exactly match expectations based on paleodrainage boundaries (i.e., "Pattern C" in Ribeiro, 2006;Lima et al, 2017) or when information about paleodrainages is lacking (Ramos--Fregonezi et al, 2017). Other potential explanations could underlie these incongruent patterns, ranging from misplaced interpretations of shared lineage (e.g., incomplete lineage sorting, instead of dispersal, could explain some geographic patterning of lineages, especially for Pleistocene; see Thomaz et al, 2015), to taxonomic differences that influence whether and when species might have dispersed across the past connections associated with paleodrainages (Hirschmann et al, 2015;Thomaz, Knowles, in prep.…”

“…Here we provide reconstructions of paleodrainages using GIS technologies for the eastern coast of Brazil, and for a few basins in the northeast and south. Together they represent a significant expansion over the information to date, which is limited to a local analysis of paleodrainages (Dias et al, 2014;Thomaz et al, 2015; and of proposed paleo-connections among a set of specific Brazilian river basins (Baggio et al, 2017;Lima et al, 2017). We also characterize general properties of the inferred paleodrainages, including the geographic area spanned by each paleodrainage and the number of contemporary river basins associated with individual paleodrainages.…”