Cytonuclear discordance and historical demography of two brown frogs, Rana tagoi and R. sakuraii (Amphibia: Ranidae)

Abstract

Prior studies of mitochondrial genomic variation reveal that the Japanese brown frog Rana tagoi comprises a complex of cryptic species lineages, and that R. sakuraii arose from within this complex. Neither species forms a monophyletic group on the mitochondrial haplotype tree, precluding a simple explanation for the evolutionary origins of R. sakuraii. We present a more complete sampling of mitochondrial haplotypic variation (from the ND1 and 16S genes) plus DNA sequence variation for five nuclear loci (from the genes encoding NCX1, NFIA, POMC, SLC8A3, and TYR) to resolve the evolutionary histories of these species. We test hypotheses of population assignment (STRUCTURE) and isolation-with-migration (IM) using the more slowly evolving nuclear markers. These demographic analyses of nuclear genetic variation confirm species-level distinctness and integrity of R. sakuraii despite its apparent polyphyly on the mitochondrial haplotype tree. Divergence-time estimates from both the mitochondrial haplotypes and nuclear genomic markers suggest that R. sakuraii originated approximately one million years ago, and that incomplete sorting of mitochondrial haplotype lineages best explains non-monophyly of R. sakuraii mitochondrial haplotypes. Cytonuclear discordance elsewhere in R. tagoi reveals a case of mitochondrial introgression between two species lineages on Honshu. The earliest phylogenetic divergence within this species group occurred approximately four million years ago, followed by cladogenetic events in the Pliocene and early Pleistocene yielding 10-13 extant species lineages, including R. sakuraii as one of the youngest.

Evolution of Sex Chromosome Heteromorphy in Geographic Populations of the Japanese Tago’s Brown Frog Complex

“…As for the mechanism of non-monophyly of R. sakuraii mitochondrial haplotypes, Eto and Matsui [2014] postulated incomplete sorting, but not interspecies hybridization, based on mitochondrial and nuclear DNA data. To prove Y chromosome introgression into the R. sakuraii genome by interspecies hybridization, molecular data analysis of autosomal and sex-linked loci is required.…”

Deciphering the origin of mito‐nuclear discordance in two sibling caddisfly species

“…For instance, disagreements between mitochondrial and nuclear gene data, called mito‐nuclear discordances, are mainly caused by two different processes (Toews & Brelsford, ): incomplete lineage sorting (ILS) and introgression. If ILS, i.e., the presence of the same ancestral variants in several lineages, underlies mito‐nuclear discordances, it indicates that the time since the onset of speciation was insufficient for genetic drift to result in fixation of all variants between lineages (Ballard & Whitlock, ; Eto & Matsui, ; McKay & Zink, ). If introgression resulting from hybridization between sister species is the driver of mito‐nuclear discordances, it indicates the presence of historical or ongoing gene flow (Toews & Brelsford, ).…”

Assessing the ecological and evolutionary processes underlyingcytonuclear interactions

“…例如, 黑鼠内(Rattus rattus)复合体种间因不完全分选(incomplete lineage sorting)或杂交产生核质不同的遗传系统 树 [69] ; 类似的报道还有镖鲈亚属粗背杜父鱼(Etheostoma subgenus: Catonotus) [70] , 林蛙属内种间(Rana tagoi 和R. sakuraii) [71] 等; 非洲象因发生不对称数量的亲本 回交在杂交带产生核质扩散不同 [72] ; 蝾螈(Salamandra salamandra)和蟒蛇(Python)种间因核质基因流差异产 生不同系统树 [73,74] . 类似地, 动物种内不同群体间, 核 质基因不同程度地扩散可导致其空间分布不一致.…”