Tempo and mode of allopatric divergence in the weakly electric fish Sternopygus dariensis in the Isthmus of Panama

Celestino Aguilar,Luis F De León,Rüdiger Krahe,Rigoberto González,Matthew J Miller,Jose R Loaiza

doi:10.1038/s41598-019-55336-y

Abstract

Spatial isolation is one of the main drivers of allopatric speciation, but the extent to which spatially-segregated populations accumulate genetic differences relevant to speciation is not always clear. We used data from ultraconserved elements (UCEs) and whole mitochondrial genomes (i.e., mitogenomes) to explore genetic variation among allopatric populations of the weakly electric fish Sternopygus dariensis across the Isthmus of Panama. We found strong genetic divergence between eastern and western populations of S. dariensis. Over 77% of the UCE loci examined were differentially fixed between populations, and these loci appear to be distributed across the species’ genome. Population divergence occurred within the last 1.1 million years, perhaps due to global glaciation oscillations during the Pleistocene. Our results are consistent with a pattern of genetic differentiation under strict geographic isolation, and suggest the presence of incipient allopatric species within S. dariensis. Genetic divergence in S. dariensis likely occurred in situ, long after the closure of the Isthmus of Panama. Our study highlights the contribution of spatial isolation and vicariance to promoting rapid diversification in Neotropical freshwater fishes. The study of spatially-segregated populations within the Isthmus of Panama could reveal how genetic differences accumulate as allopatric speciation proceeds.

Highlights

The closure of the Isthmus of Panama is one of the main drivers of Neotropical diversification
The extent to which spatially segregated populations show progress towards allopatric divergence is not always obvious. We explore this issue by using a panel of over 285 ultraconserved elements (UCEs), single nucleotide polymorphisms (SNPs) and complete mitogenome sequences in the weakly electric fish S. dariensis in the context of the biogeographic history of the Isthmus of Panama
Our analysis of population structure based on UCEs revealed two divergent clusters that corresponded to eastern (i.e., Chucunaque/Tuira) and western populations (Santa María, San Pablo and Tumaganti; Fig. 1B)

Summary

Introduction

The closure of the Isthmus of Panama is one of the main drivers of Neotropical diversification. Global events such as the Pleistocene glaciations[8] have facilitated the expansion and contraction of local populations via changes in sea level[9,10,11] Together, these events have defined the current spatial structure of the Isthmian populations[6,12,13,14], with implications for allopatric divergence across isolated populations. Divergence of seemingly isolated populations might be influenced by selective (i.e., local adaptation) and random processes (i.e., drift) that are difficult to disentangle if relying on low numbers of molecular markers[22] We explore these issues by quantifying genetic variation at both nuclear loci linked to ultraconserved elements.

Methods

Results

Conclusion