Abstract
The evolutionary causes and consequences of allopolyploidization, an exceptional pathway to instant hybrid speciation, are poorly investigated in animals. In particular, when and why hybrid polyploids versus diploids are produced, and constraints on sources of paternal and maternal ancestors, remain underexplored. Using the Palearctic green toad radiation (including bisexually reproducing species of three ploidy levels) as model, we generate a range-wide multi-locus phylogeny of 15 taxa and present four new insights: (i) at least five (up to seven) distinct allotriploid and allotetraploid taxa have evolved in the Pleistocene; (ii) all maternal and paternal ancestors of hybrid polyploids stem from two deeply diverged nuclear clades (6 Mya, 3.1–9.6 Mya), with distinctly greater divergence than the parental species of diploid hybrids found at secondary contact zones; (iii) allotriploid taxa possess two conspecific genomes and a deeply diverged allospecific one, suggesting that genomic imbalance and divergence are causal for their partly clonal reproductive mode; (iv) maternal versus paternal genome contributions exhibit asymmetry, with the maternal nuclear (and mitochondrial) genome of polyploids always coming from the same clade, and the paternal genome from the other. We compare our findings with similar patterns in diploid/polyploid vertebrates, and suggest deep ancestral divergence as a precondition for successful allopolyploidization.
Highlights
How much hybridization and introgression events contribute to speciation and genome evolution is developing as an active research topic [1,2]
Our phylogenetic analysis highlighted at least five events of allopolyploidization that led to the evolution of two allotetraploids (B. pewzowi, B. oblongus) and three allotriploids (B. baturae, B. pseudoraddei, B. zugmayeri; figure 1c; electronic supplementary material, figure S2 (I –V) and text S5)
We document at least five hybridization events that resulted in the evolution of allopolyploid species
Summary
How much hybridization and introgression events contribute to speciation and genome evolution is developing as an active research topic [1,2]. We further hypothesize that the evolution of allopolyploid lineages may show similar asymmetric interactions To test these questions in amphibians, Palearctic green toads (Bufo viridis subgroup) present a highly suitable system to compare diploid and polyploid hybridization within one radiation. This group comprises different diploid lineages forming secondary contact zones, with levels of introgression that scale with divergence [22,34]. We use new multi-locus nuclear sequence data, supplemented by mitochondrial DNA, to (i) identify allopolyploidization events in the Palearctic green toad radiation, (ii) infer the paternal and maternal ancestries of polyploids,. All runs were performed on the CIPRES Science Gateway [50]
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