Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs

Subdivided Pleistocene glacial refugia, best known as “refugia within refugia”, provided opportunities for diverging populations to evolve into incipient species and/or to hybridize and merge following range shifts tracking the climatic fluctuations, potentially promoting extensive cytonuclear disco...

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Bibliographic Details
Published in:Molecular ecology 2020-03, Vol.29 (5), p.986-1000
Main Authors: Dufresnes, Christophe, Nicieza, Alfredo G., Litvinchuk, Spartak N., Rodrigues, Nicolas, Jeffries, Daniel L., Vences, Miguel, Perrin, Nicolas, Martínez‐Solano, Íñigo
Format: Article
Language:English
Subjects:
Amphibians
Animals
Biological evolution
Cell Nucleus - genetics
Divergence
DNA Barcoding, Taxonomic
DNA, Mitochondrial - genetics
Evolutionary genetics
Frogs
Genetic diversity
Genetic Speciation
Genetics, Population
Genomes
ghost lineage
glacial refugium
hybrid zone
Ice Cover
Mitochondria
Mitochondrial DNA
Mountains
Phylogeography
Pleistocene
Polymorphism, Single Nucleotide
Population genetics
Populations
RAD‐sequencing
Rana parvipalmata
Rana temporaria
Rana temporaria - genetics
Refugia
Refugium
Spain
Speciation
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Summary:Subdivided Pleistocene glacial refugia, best known as “refugia within refugia”, provided opportunities for diverging populations to evolve into incipient species and/or to hybridize and merge following range shifts tracking the climatic fluctuations, potentially promoting extensive cytonuclear discordances and “ghost” mtDNA lineages. Here, we tested which of these opposing evolutionary outcomes prevails in northern Iberian areas hosting multiple historical refugia of common frogs (Rana cf. temporaria), based on a genomic phylogeography approach (mtDNA barcoding and RAD‐sequencing). We found evidence for both incipient speciation events and massive cytonuclear discordances. On the one hand, populations from northwestern Spain (Galicia and Asturias, assigned to the regional endemic R. parvipalmata), are deeply‐diverged at mitochondrial and nuclear genomes (~4 My of independent evolution), and barely admix with northeastern populations (assigned to R. temporaria sensu stricto) across a narrow hybrid zone (~25 km) located in the Cantabrian Mountains, suggesting that they represent distinct species. On the other hand, the most divergent mtDNA clade, widespread in Cantabria and the Basque country, shares its nuclear genome with other R. temporaria s. s. lineages. Patterns of population expansions and isolation‐by‐distance among these populations are consistent with past mitochondrial capture and/or drift in generating and maintaining this ghost mitochondrial lineage. This remarkable case study emphasizes the complex evolutionary history that shaped the present genetic diversity of refugial populations, and stresses the need to revisit their phylogeography by genomic approaches, in order to make informed taxonomic inferences.
ISSN:0962-1083
1365-294X
DOI:10.1111/mec.15368