Evolution of mitochondrial relationships and biogeography of Palearctic green toads (Bufo viridis subgroup) with insights in their genomic plasticity

Abstract

Taxa involving three bisexually reproducing ploidy levels make green toads a unique amphibian system. We put a cytogenetic dataset from Central Asia in a molecular framework and apply phylogenetic and demographic methods to data from the entire Palearctic range. We study the mitochondrial relationships of diploids to infer their phylogeography and the maternal ancestry of polyploids. Control regions (and tRNAs between ND1 and ND2 in representatives) characterize a deeply branched assemblage of twelve haplotype groups, diverged since the Lower Miocene. Polyploidy has evolved several times: Central Asian tetraploids (B. oblongus, B. pewzowi) have at least two maternal origins. Intriguingly, the mitochondrial ancestor of morphologically distinctive, sexually reproducing triploid taxa (B. pseudoraddei) from Karakoram and Hindukush represents a different lineage. We report another potential case of bisexual triploid toads (B. zugmayeri). Identical d-loops in diploids and tetraploids from Iran and Turkmenistan, which differ in morphology, karyotypes and calls, suggest multiple origins and retained polymorphism and/or hybridization. A similar system involves diploids, triploids and tetraploids from Kyrgyzstan and Kazakhstan where green toads exemplify vertebrate genomic plasticity. A new form from Sicily and its African sister species (B. boulengeri) allow internal calibration and divergence time estimates for major clades. The subgroup may have originated in Eurasia rather than Africa since the earliest diverged lineages (B. latastii, B. surdus) and earliest fossils occur in Asia. We delineate ranges, contact and hybrid zones. Phylogeography, including one of the first non-avian datasets from Central Asian high mountains, reflects Quaternary climate and glaciation.

Origin and genome evolution of polyploid green toads in Central Asia: evidence from microsatellite markers

“…Clustering analyses based on our multi-locus genotype data, the vast majority of which represent newly established, cross-amplifying microsatellite loci, showed that the maternal ancestor of B. pewzowi (P m ) was closely related to B. turanensis, in accordance with previous suggestions that had been based on limited mtDNA and nuDNA sequence evidence (Stöck et al, 2006. The strong genetic similarity between these two genomes pointed to a very recent hybridization event: for all K values investigated in the STRUCTURE analyses, the P m and T genomes clustered together (Figure 2).…”

“…Natural polyploids are especially frequent in the latter class (Bogart, 1980;Schmid, 1980;Kawamura, 1984); they have evolved independently in multiple families (Mable et al, 2011), with 50 polyploid anuran species and six polyploid salamander species described (Evans et al, 2012). Palearctic green toads offer a particularly interesting system, forming a monophyletic radiation of at least 12 major mitochondrial DNA (mtDNA) haplotype groups (Stöck et al, 2006) with several cases of range overlap and interactions through hybridization and polyploidization (Colliard et al, 2010;Dufresnes et al, 2014). This radiation includes in particular bisexually reproducing species of three ploidy levels (2n, 3n and 4n; Stöck et al, 2010).…”

Simultaneous Mendelian and clonal genome transmission in a sexually reproducing, all-triploid vertebrate

“…This reproductive mode also raises questions regarding selective processes and evolutionary fate. Polyploid (3n, 4n) lineages of green toads, which evolved several times independently, are clearly associated with harsh habitats [50]. Batura toads, in particular, live in extreme conditions of altitude and xericity [52].…”

“…Batura toads, however, may have arisen too recently for such mutational meltdown or genomic conflict over sex determination to be detectable [25,50].…”

An overview of wetlands of Saudi Arabia: Values, threats, and perspectives

“…variabilis), Hyla savignyi, and Pelophylax ridibunda) (Balletto et al 1985). Many of these taxa are part of species complexes and, therefore, present a considerable taxonomic and biogeographic challenge (Stöck et al 2006;Portik and Papenfuss 2015).…”