Molecular insights versus morphological traits: rethinking identification of the closely related <i>Angiostrongylus cantonensis</i> and <i>Angiostrongylus malaysiensis</i>

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Abstract

Background

The closely related Angiostrongylus cantonensis and Angiostrongylus malaysiensis have been reported to coexist in Thailand and share similar hosts and life cycles. Recently, in an angiostrongyliasis outbreak in Thailand, both A. cantonensis and A. malaysiensis were found in the cerebrospinal fluid of affected patients. Morphological similarities, overlapping distribution, shared hosts and habitats, and the close genetics of the two Angiostrongylus species can complicate accurate species identification. Addressing these challenges, this study aims to evaluate whether a correlation between the morphological and genetic identities of A. cantonensis and A. malaysiensis can improve species identification accuracy.

Methods

Angiostrongylus spp. specimens from five zoogeographical regions in Thailand were subjected to morphological and molecular identification using the mitochondrial cytochrome b gene and the nuclear internal transcribed spacer 2 region (ITS2). The morphological characters for males and females were then validated using the species identity obtained from the nuclear ITS2 region.

Results

The results revealed that morphological misidentifications between these two closely related species are common due to overlapping morphological characters. Although certain male traits such as body length and width aided species differentiation, female traits were found to be less reliable. Furthermore, hybrid forms (8.2%) were revealed through the ITS2 results, which can further complicate morphological identification. Mito-nuclear discordance was also present in 1.9% of the Angiostrongylus specimens from Thailand, suggesting a complex historical interbreeding between the species.

Conclusions

Based on our findings, we suggest that nuclear ITS2 is a reliable marker for species identification of A. cantonensis and A. malaysiensis, especially in regions where both species coexist. Additionally, the scope and consequences of hybridization between the two closely related Angiostrongylus species should be further investigated in Thailand.

Graphical Abstract

Supplementary Information

The online version contains supplementary material available at 10.1186/s13071-024-06140-9.

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The biogeography of mitochondrial and nuclear discordance in animals.

David Toews, Alan Brelsford (2012)

Combining nuclear (nuDNA) and mitochondrial DNA (mtDNA) markers has improved the power of molecular data to test phylogenetic and phylogeographic hypotheses and has highlighted the limitations of studies using only mtDNA markers. In fact, in the past decade, many conflicting geographic patterns between mitochondrial and nuclear genetic markers have been identified (i.e. mito-nuclear discordance). Our goals in this synthesis are to: (i) review known cases of mito-nuclear discordance in animal systems, (ii) to summarize the biogeographic patterns in each instance and (iii) to identify common drivers of discordance in various groups. In total, we identified 126 cases in animal systems with strong evidence of discordance between the biogeographic patterns obtained from mitochondrial DNA and those observed in the nuclear genome. In most cases, these patterns are attributed to adaptive introgression of mtDNA, demographic disparities and sex-biased asymmetries, with some studies also implicating hybrid zone movement, human introductions and Wolbachia infection in insects. We also discuss situations where divergent mtDNA clades seem to have arisen in the absence of geographic isolation. For those cases where foreign mtDNA haplotypes are found deep within the range of a second taxon, data suggest that those mtDNA haplotypes are more likely to be at a high frequency and are commonly driven by sex-biased asymmetries and/or adaptive introgression. In addition, we discuss the problems with inferring the processes causing discordance from biogeographic patterns that are common in many studies. In many cases, authors presented more than one explanation for discordant patterns in a given system, which indicates that likely more data are required. Ideally, to resolve this issue, we see important future work shifting focus from documenting the prevalence of mito-nuclear discordance towards testing hypotheses regarding the drivers of discordance. Indeed, there is great potential for certain cases of mitochondrial introgression to become important natural systems within which to test the effect of different mitochondrial genotypes on whole-animal phenotypes. © 2012 Blackwell Publishing Ltd.

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Angiostrongylus cantonensis: a review of its distribution, molecular biology and clinical significance as a human pathogen.

Joel Barratt, Douglas Chan, Indy Sandaradura … (2016)

Angiostrongylus cantonensis is a metastrongyloid nematode found widely in the Asia-Pacific region, and the aetiological agent of angiostrongyliasis; a disease characterized by eosinophilic meningitis. Rattus rats are definitive hosts of A. cantonensis, while intermediate hosts include terrestrial and aquatic molluscs. Humans are dead-end hosts that usually become infected upon ingestion of infected molluscs. A presumptive diagnosis is often made based on clinical features, a history of mollusc consumption, eosinophilic pleocytosis in cerebral spinal fluid, and advanced imaging such as computed tomography. Serological tests are available for angiostrongyliasis, though many tests are still under development. While there is no treatment consensus, therapy often includes a combination of anthelmintics and corticosteroids. Angiostrongyliasis is relatively rare, but is often associated with morbidity and sometimes mortality. Recent reports suggest the parasites' range is increasing, leading to fatalities in regions previously considered Angiostrongylus-free, and sometimes, delayed diagnosis in newly invaded regions. Increased awareness of angiostrongyliasis would facilitate rapid diagnosis and improved clinical outcomes. This paper summarizes knowledge on the parasites' life cycle, clinical aspects and epidemiology. The molecular biology of Angiostrongylus spp. is also discussed. Attention is paid to the significance of angiostrongyliasis in Australia, given the recent severe cases reported from the Sydney region.

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Author and article information

Contributors

Urusa Thaenkham: urusa.tha@mahidol.edu

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 8 February 2024

Publication date PMC-release: 8 February 2024

Publication date Collection: 2024

Volume: 17

Electronic Location Identifier: 56

Affiliations

[1 ]Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, ( https://ror.org/01znkr924) Bangkok, Thailand

[2 ]Department of Molecular Tropical Medicine and Molecular Genetics, Faculty of Tropical Medicine, Mahidol University, ( https://ror.org/01znkr924) Bangkok, Thailand

[3 ]Department of Medical Entomology, Faculty of Tropical Medicine, Mahidol University, ( https://ror.org/01znkr924) Bangkok, Thailand

Article

Publisher ID: 6140

DOI: 10.1186/s13071-024-06140-9

PMC ID: 10851580

PubMed ID: 38326886

SO-VID: 20d26c7c-bad8-474c-a118-2f0e63db246d

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 28 August 2023

Date accepted : 17 January 2024

Funding

Funded by: Mahidol University

Open Access :

Open access funding provided by Mahidol University

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: angiostrongylus cantonensis,angiostrongylus malaysiensis,misidentification,morphological and molecular characters,hybrids

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ScienceOpen disciplines: Parasitology

Keywords: angiostrongylus cantonensis, angiostrongylus malaysiensis, misidentification, morphological and molecular characters, hybrids

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Molecular insights versus morphological traits: rethinking identification of the closely related Angiostrongylus cantonensis and Angiostrongylus malaysiensis

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Abstract

Background

Methods

Results

Conclusions

Graphical Abstract

Supplementary Information

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Malaria vaccine development

Most cited references 28

The biogeography of mitochondrial and nuclear discordance in animals.

Angiostrongylus cantonensis: a review of its distribution, molecular biology and clinical significance as a human pathogen.

RStudio: Integrated Development for R

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Cited by 2

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