Gene flow, genomic homogenization and the timeline to speciation in Amazonian manakins.

Phylogeographical studies of the most species-rich region of the planet-the Amazon basin-have repeatedly uncovered genetically distinctive, allopatric lineages within currently named species, but understanding whether such lineages are reproductively isolated species is challenging. Here we harness the power of genome-wide data sets together with detailed phylogeographical sampling to both characterize the number of unique lineages and infer levels of reproductive isolation for three parapatric manakin species that make up the genus Pipra. The mitochondrial and nuclear genomes both support six distinctive lineages. The youngest lineages are now highly admixed with each other across major portions of their geographical ranges with one lineage now extinct in a genomically unadmixed state. In contrast, the oldest sets of lineages-dated to 1.4 million years-exhibit narrow hybrid zones. By fitting demographic models to parapatric lineage pairs we found that levels of gene flow and genomic homogenization decline with increasing evolutionary age. Only lineages descending from the basal node at 1.4 million years ago in the genus experience negligible gene flow, possess genomes resistant to homogenization and are separated by narrow hybrid zones. We conclude that a million years or more were required for Pipra manakins to become reproductively isolated. We suggest the six lineages be reclassified as two or three reproductively isolated species. Our unique approach to quantifying reproductive isolation in parapatric lineages could be applied broadly to other phylogeographical studies and would help determine species classification of the plethora of newly identified lineages in the Amazon basin and other regions.

Hybridization in headwater regions, and the role of rivers as drivers of speciation in Amazonian birds.

Many understory birds and other groups form genetically differentiated subspecies or closely related species on opposite sides of major rivers of Amazonia, but are proposed to come into geographic contact in headwater regions where narrower river widths may present less of a dispersal barrier. Whether such forms hybridize in headwater regions is generally unknown, but has important implications to our understanding of the role of rivers as drivers of speciation. We used a dataset of several thousand single nucleotide polymorphisms to show that seven taxon pairs that differentiate across a major Amazonian river come into geographic contact and hybridize in headwater regions. All taxon pairs possessed hybrids with low numbers of loci in which alleles were inherited from both parental species, suggesting they are backcrossed with parentals, and indicating gene flow between parental populations. Ongoing gene flow challenges rivers as the sole cause of in situ speciation, but is compatible with the view that the wide river courses in the heart of Amazonia may have driven interfluvial divergence during episodes of wet forest retraction away from headwater regions. Taxa as old as 4 Ma in our Amazonian dataset continue to hybridize at contact zones, suggesting reproductive isolation evolves at a slow pace.