Bayesian Divergence-Time Estimation with Genome-Wide Single-Nucleotide Polymorphism Data of Sea Catfishes (Ariidae) Supports Miocene Closure of the Panamanian Isthmus.

Michael Matschiner,Marcelo R Sánchez-Villagra,Matthew Hahn,Walter Salzburger,Madlen Stange

doi:10.1093/sysbio/syy006

Michael Matschiner, Marcelo R Sánchez-Villagra + Show 3 more

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https://doi.org/10.1093/sysbio/syy006

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Abstract

The closure of the Isthmus of Panama has long been considered to be one of the best defined biogeographic calibration points for molecular divergence-time estimation. However, geological and biological evidence has recently cast doubt on the presumed timing of the initial isthmus closure around 3 Ma but has instead suggested the existence of temporary land bridges as early as the Middle or Late Miocene. The biological evidence supporting these earlier land bridges was based either on only few molecular markers or on concatenation of genome-wide sequence data, an approach that is known to result in potentially misleading branch lengths and divergence times, which could compromise the reliability of this evidence. To allow divergence-time estimation with genomic data using the more appropriate multispecies coalescent (MSC) model, we here develop a new method combining the single-nucleotide polymorphism-based Bayesian species-tree inference of the software SNAPP with a molecular clock model that can be calibrated with fossil or biogeographic constraints. We validate our approach with simulations and use our method to reanalyze genomic data of Neotropical army ants (Dorylinae) that previously supported divergence times of Central and South American populations before the isthmus closure around 3 Ma. Our reanalysis with the MSC model shifts all of these divergence times to ages younger than 3 Ma, suggesting that the older estimates supporting the earlier existence of temporary land bridges were artifacts resulting at least partially from the use of concatenation. We then apply our method to a new restriction-site associated DNA-sequencing data set of Neotropical sea catfishes (Ariidae) and calibrate their species tree with extensive information from the fossil record. We identify a series of divergences between groups of Caribbean and Pacific sea catfishes around 10 Ma, indicating that processes related to the emergence of the isthmus led to vicariant speciation already in the Late Miocene, millions of years before the final isthmus closure.

Highlights

The closure of the Isthmus of Panama has long been considered to be one of the best defined biogeographic calibration points for molecular divergence-time estimation
We identify a series of divergences between groups of Caribbean and Pacific sea catfishes around 10 Ma, indicating that processes related to the emergence of the isthmus led to vicariant speciation already in the Late Miocene, millions of years before the final isthmus closure. (Keywords: Panamanian Isthmus; Central American Seaway; Bayesian inference; phylogeny; molecular clock; fossil record; single-nucleotide polymorphisms (SNPs); RAD sequencing; teleosts)
Our reanalysis of Neotropical army ant SNP data with the multi-species coalescent (MSC) resulted in a strongly supported phylogeny that recovered the topology proposed by Winston et al (2017) with the single exception that Eciton mexicanum appeared as the sister of E. lucanoides rather than diverging from the common ancestor of E. lucanoides, E. burchellii, E. drepanophorum, and E. hamatum (Supplementary Figure S5 and Supplementary Table S3)

Summary

Introduction

The closure of the Isthmus of Panama has long been considered to be one of the best defined biogeographic calibration points for molecular divergence-time estimation. Due to its presumed simultaneous impact on speciation events in numerous terrestrial and marine lineages, the closure of the Isthmus of Panama has been considered one of the best biogeographic calibration points for molecular divergence-time estimation and has been used in several hundreds of phylogenetic studies (Bermingham et al 1997; Lessios 2008; Bacon et al 2015a). While the Atrato strait represented the main connection between the Caribbean and the Pacific throughout most of the Miocene, other passageways existed in the Panama Canal basin (the Panama isthmian strait) and across Nicaragua (the San Carlos strait) (Savin and Douglas 1985) Both of these passageways were likely closed around 8 Ma (and possibly earlier) but reopened around 6 Ma with a depth greater than 200 m, according to evidence from fossil foraminifera (Collins et al 1996). The last connection between the Caribbean and the Pacific likely closed around 2.8 Ma (O’Dea et al 2016), but short-lived breachings induced by sea-level fluctuations as late as 2.45 Ma cannot be excluded and receive some support from molecular data (Groeneveld et al 2014; Hickerson et al 2006)

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