Biogeography, habitat transitions and hybridization in a radiation of South American silverside fishes revealed by mitochondrial and genomic RAD data

Abstract

Rivers and lake systems in the southern cone of South America have been widely influenced by historical glaciations, carrying important implications for the evolution of aquatic organisms, including prompting transitions between marine and freshwater habitats and by triggering hybridization among incipient species via waterway connectivity and stream capture events. Silverside fishes (Odontesthes) in the region comprise a radiation of 19 marine and freshwater species that have been hypothesized on the basis of morphological or mitochondrial DNA data to have either transitioned repeatedly into continental waters from the sea or colonized marine habitats following freshwater diversification. New double digest restriction‐site associated DNA data presented here provide a robust framework to investigate the biogeographical history of and habitat transitions in Odontesthes. We show that Odontesthes silversides originally diversified in the Pacific but independently colonized the Atlantic three times, producing three independent marine‐to‐freshwater transitions. Our results also indicate recent introgression of marine mitochondrial haplotypes into two freshwater clades, with more recurring instances of hybridization among Atlantic‐ versus Pacific‐slope species. In Pacific freshwater drainages, hybridization with a marine species appears to be geographically isolated and may be related to glaciation events. Substantial structural differences of estuarine gradients between these two geographical areas may have influenced the frequency, intensity and evolutionary effects of hybridization events.

Comparing diversification rates in lakes, rivers, and the sea

“…This is intuitive, as lakes are fed by rivers and do not usually interface directly with the ocean (but see Schluter and McPhail 1992 and Hughes et al. 2020 for counterexamples). The most common path to entering lakes is by first entering rivers, then occurring in both rivers and lakes, then finally becoming endemic to lakes (Fig.…”

“…In the best-fitting model, direct transitions from the ocean into lakes were constrained to be rarer than marine-riverine transitions (Table 2). This is intuitive, as lakes are fed by rivers and do not usually interface directly with the ocean (but see McPhail 1992 andHughes et al 2020 for counterexamples). The most common path to entering lakes is by first entering rivers, then occurring in both rivers and lakes, then finally becoming endemic to lakes (Fig.…”

Multiple drainage reversal episodes and glacial refugia in a Patagonian fish revealed by sequenced microsatellites

“…The processes usually described as the two most important factors in South America are the uplift of the Andes, which began approximately 23 Ma [28], and the glacial cycles of the Quaternary (2.5 Ma-10 000 BP). Their combined influence has affected phylogeographic patterns for many species, including the number and location of glacial refugia and the rates and directions of late and post-Pleistocene gene flow [12,24,29,30]. Some species survived the last glacial maximum (LGM) in glacial refugia east of the Andes, on the largely unglaciated Patagonian steppe [10,12,17,22,31].…”

“…post-Pleistocene gene flow [12,24,29,30]. Some species survived the last glacial maximum (LGM) in glacial refugia east of the Andes, on the largely unglaciated Patagonian steppe [10,12,17,22,31].…”

Genome-wide sequence data show no evidence of admixture and introgression among pollinator wasps associated with a community of Panamanian strangler figs

“…Although additional approaches are often used to test for hybridization and introgression, they were not applicable for our data set. For example, D-statistics (Green et al, 2010;Durand et al, 2011), often referred to as ABBA/BABA tests, have been widely used to infer a signal of introgression among numerous clades across the tree of life (e.g., Eaton and Ree, 2013;Streicher et al, 2014;Meier et al, 2017;Hughes et al, 2020;Pulido-Santacruz et al, 2020). D-statistics, however, can not estimate gene flow between sister species, and our biologically informed hypotheses do not lend themselves well to the strict phylogenetic pattern (((P1,P2),P3),OG) typically required for testing if one species (P3) has hybridized with another (either species P1 or species P2).…”