Topology testing and demographic modeling illuminate a novel speciation pathway in the Greater Caribbean Sea following the formation of the Isthmus of Panama

Recent genomic analyses have highlighted the prevalence of speciation with
gene flow in many taxa and have underscored the importance of accounting
for these reticulate evolutionary processes when constructing species
trees and generating parameter estimates. This is especially important for
deepening our understanding of speciation in the sea where fast-moving
ocean currents, expanses of deep water, and periodic episodes of sea level
rise and fall act as soft and temporary allopatric barriers that
facilitate both divergence and secondary contact. Under these conditions,
gene flow is not expected to cease completely while contemporary
distributions are expected to differ from historical ones. Here we conduct
range-wide sampling for Pederson’s cleaner shrimp (Ancylomenes pedersoni),
a species complex from the Greater Caribbean that contains three clearly
delimited mitochondrial lineages with both allopatric and sympatric
distributions. Using mtDNA barcodes and a genomic ddRADseq approach, we
combine classic phylogenetic analyses with extensive topology testing and
demographic modeling (10 site frequency replicates x 45 evolutionary
models x 50 model simulations/replicate = 22,500 simulations) to test
species boundaries and reconstruct the evolutionary history of what was
expected to be a simple case study. Instead, our results indicate a
history of allopatric divergence, secondary contact, introgression, and
endemic hybrid speciation that we hypothesize was driven by the final
closure of the Isthmus of Panama and the strengthening of the Gulf Stream
Current ~3.5 million years ago. The history of this species complex
recovered by model-based methods that allow reticulation differs from that
recovered by standard phylogenetic analyses and is unexpected given
contemporary distributions. The geologically and biologically meaningful
insights gained by our model selection analyses illuminate what is likely
a novel pathway of species formation not previously documented that
resulted from one of the most biogeographically significant events in
Earth’s history.