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Black-spotted pond frog Pelophylax nigromaculatus as a new host for the renal coccidian genus Hyaloklossia (Alveolata: Apicomplexa).

ABSTRACT: Hyaloklossia Labbé, 1896 (Apicomplexa: Sarcocystidae) is a renal coccidium that infects anuran species. The genus consists of two species: H. lieberkuehni, recorded from Pelophylax kl. esculentus, Pelophylax ridibundus, and Rana temporaria in Europe; and H. kasumiensis, recorded from Pelophylax porosus porosus in Japan. However, there have been no reports of Hyaloklossia in the other anurans in Japan. On June 2021, we examined a total of 58 adult frogs comprising 2 P. p. porosus, 23 Pelophylax nigromaculatus, 8 Rana japonica, 3 Glandirana rugosa (Ranidae), 13 Fejervarya kawamurai (Dicroglossidae), and 9 Buergeria buergeri (Rhacophoridae) for infection by Hyaloklossia. Microscopic examination of kidney tissues revealed a high infection incidence of 47.8% (11/23) in P. nigromaculatus, but the other frog species were negative for Hyaloklossia. Morphological and molecular analyses using nuclear ribosomal and mitochondrial genes confirmed the infective species as H. kasumiensis. This is a new host record for H. kasumiensis.

SUBMITTER: Tokiwa T

PROVIDER: S-EPMC8844192 | biostudies-literature | 2022 Apr

REPOSITORIES: biostudies-literature

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Black-spotted pond frog Pelophylax nigromaculatus as a new host for the renal coccidian genus Hyaloklossia (Alveolata: Apicomplexa).

Tokiwa Toshihiro T Chou Shyun S Morizane Riona R Yoshikawa Natsuhiko N

International journal for parasitology. Parasites and wildlife 20220204

Hyaloklossia Labbé, 1896 (Apicomplexa: Sarcocystidae) is a renal coccidium that infects anuran species. The genus consists of two species: H. lieberkuehni, recorded from Pelophylax kl. esculentus, Pelophylax ridibundus, and Rana temporaria in Europe; and H. kasumiensis, recorded from Pelophylax porosus porosus in Japan. However, there have been no reports of Hyaloklossia in the other anurans in Japan. On June 2021, we examined a total of 58 ...[more]

PMID: 35198372

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Project description:BackgroundMitochondrial introgression may result in the mitochondrial genome of one species being replaced by that of another species without leaving any trace of past hybridization in its nuclear genome. Such introgression can confuse the species genealogy estimates and lead to absurd inferences of species history. We used a phylogenetic approach to explore the potential mitochondrial genome introgression event(s) between two closely related green pond frog species, Pelophylax nigromaculatus and P. plancyi.ResultsDNA sequence data of one mitochondrial and two nuclear genes from an extensive sampling of the two species were collected, and the genealogies of the three genes were constructed and compared. While the two nuclear genes congruently showed mutual reciprocal monophyly of both species, the mitochondrial phylogeny separated a Korean P. nigromaculatus clade, a paraphyletic central China P. plancyi assemblage, and a large well-supported introgression clade. Within the introgression clade, the mitochondrial haplotypes of the two species were mixed together. This reticulated pattern can be most parsimoniously explained by an ancient mitochondrial introgression event from P. plancyi to P. nigromaculatus that occurred at least 1.36 MYA, followed by multiple recent introgression events from P. nigromaculatus back to P. plancyi within the last 0.63 MY. The re-constitution of previously co-adapted genomes in P. plancyi may be responsible for the recent rampant introgression events. The Korean P. nigromaculatus clade likely represents the only surviving "true" mitochondrial lineage of P. nigromaculatus, and the central China P. plancyi assemblage likely represents the "original" P. plancyi mitochondrial lineage. Refugia in the Korean Peninsula and central China may have played a significant role in preserving these ancient lineages.ConclusionsThe majority of individuals in the two species have either introgressed (P. nigromaculatus) or reclaimed (P. plancyi) mitochondrial genomes while no trace of past hybridization in their nuclear genomes was detected. Asymmetrical reproductive ability of hybrids and continuous backcrossing are likely responsible for the observed mitochondrial introgression. This case is unique in that it includes an ancient "forward" introgression and many recent "backward" introgressions, which re-constitutes the original nuclear and mitochondrial genomes of P. plancyi. This hybrid system provides an excellent opportunity to study cyto-nuclear interaction and co-adaptation.

Project description:BackgroundPleistocene glaciations had considerable impact on phylogeographic patterns within and among closely related species of many vertebrates. Compared to Europe and North America, research on the phylogeography of vertebrates in East Asia, particularly in China, remains limited. The black-spotted frog (Pelophylax nigromaculata) is a widespread species in East Asia. The wide distribution of this species in China makes it an ideal model for the study of palaeoclimatic effects on vertebrates in East Asia. Our previous studies of P. nigromaculata revealed significant subdivisions between the northeast China populations and populations in other regions of the mainland. In the present study, we aim to see whether the deepest splits among lineages and perhaps subsequent genealogical divisions are temporally consistent with a Pleistocene origin and whether clade geographic distributions, with insight into expansion patterns, are similarly spatially consistent with this model.ResultsUsing 1143 nucleotides of the mitochondrial cytochrome b gene from 262 individuals sampled from 28 localities, two main clades (clade A and clade B) differing by c. 7.72% sequence divergence were defined from parsimony analyses. The corresponding timing of lineage divergence, 0.92 Mya, indicates a most likely Pleistocene split. The A clade is further subdivided into two sub-clades, A1 and A2 with 1.22% sequence divergence. Nested clade phylogeographical and population demographic analyses suggested that the current distribution of this frog species was the result of range expansion from two independent refugia during the last interglacial period. We discovered a population within which haplotype lineages A and B of P. nigromaculata coexist in the Dongliao area of China by nucleotide sequences, PCR-RFLP and ISSR (inter simple sequence repeat) patterns. The ISSR result in particular supported divergence between the mitochondrial clades A and B and implied introgressive gene flow between the two divergent lineages.ConclusionNested clade phylogeographical and population demographic analyses indicate that the current distribution of P. nigromaculata is the result of range expansion from two independent refugia during the last interglacial period in late Pleistocene. One refugium was in east China and the lower elevations of south-western plateau. The distribution of the other mitochondrial clade is consistent with the presence of a refugium in the Korean Peninsula. The gene flow as detected by ISSR markers suggests a range expansion of the two refugia and a secondary contact between the two highly divergent lineages in the Dongliao (DL) area of northeast China.

Dataset Information

Black-spotted pond frog Pelophylax nigromaculatus as a new host for the renal coccidian genus Hyaloklossia (Alveolata: Apicomplexa).

Publications

Black-spotted pond frog <i>Pelophylax nigromaculatus</i> as a new host for the renal coccidian genus <i>Hyaloklossia</i> (Alveolata: Apicomplexa).

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