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Molecular and statistical approaches to the delimitation of Eimeriidae species: a case of extreme polymorphism in eimerian oocysts from the plumbeous pigeon Patagioenas plumbea (Vieillot, 1818) (Columbiformes) in South America

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Abstract

The current work aimed to analyze, morphologically, statistically, and molecularly, oocysts shed from plumbeous pigeons, Patagioenas plumbea (Vieillot, 1818), from a locality at 2197 m of altitude near the Agulhas Negras peak, the highest point of the State of Rio de Janeiro, southeastern Brazil. The oocysts were extremely polymorphic, being subspheroidal, ovoidal, or ellipsoidal, in addition to having the random presence/absence of characteristic features associated with the oocyst wall, such as micropyle, micropyle cap, lateral micropyle, and outer veil/rough wall. Linear regression confirmed the extreme polymorphism of oocysts, showing that if all combinations of taxonomic characters in oocysts (morphotypes) were overestimated, 19 different species could be identified/described. In contrast, the means comparison analysis between oocysts with the presence/absence of characteristic features and the histograms showed equivalences and regularity in the distribution in the classes of measures, which indicate the presence of a single species in the measured oocysts. Molecular analyses were performed from the isolation of individual oocysts of different morphotypes, which had their genetic material extracted, amplified, and sequenced in 4 non-overlapping loci in the cox1 and cox3 genes and fragments of the small and large subunit rDNA of mitochondrial DNA. The sequences were 100% identical between the morphotypes, with the exception of a very small divergence observed at the locus that partially covers the cox3 gene. The phylogenetic analysis was inconclusive for the locus within the cox1 gene traditionally used for eimeriid coccidians; however, the other loci should have a promising future for phylogenetic studies when more sequences for the same genic regions are deposited in GenBank. Finally, the multifactorial analysis of the current work supported that the polymorphic oocysts shed from P. plumbea are a single species, which was named Eimeria patagioenasae, making this the twenty-second eimerian description from Columbiformes.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We are thankful to the staff at the Parque Nacional do Itatiaia, mainly to the research coordinators Dr Léo Nascimento (previous) and Marcelo Souza Motta (current), who allowed us to access and use some facilities during the expeditions.

Funding

This study was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ). CNO-F and LASA have scholarships from CAPES (Grant/Award Number: 001). MSO has a postdoctoral scholarship from FAPERJ (Grant/Award Number: E-26/204.228/2021). VML has a fellowship from FAPERJ (Grant/Award Number: E-27/211.566/2021). BPB has a fellowship from CNPq (Grant/Award Number: 302345/2022–1) and from FAPERJ (Grant/Award Number: E-26/200.565/2023).

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Authors and Affiliations

  1. Programa de Pós-Graduação em Biologia Animal, Instituto de Ciências Biológicas e da Saúde (ICBS), Universidade Federal Rural do Rio de Janeiro (UFRRJ), BR-465 Km 7, Seropédica, RJ, 23897-000, Brazil

    Carlos Nei Ortúzar-Ferreira, Mariana S. Oliveira & Lucas de Assis S. Andrade

  2. Programa de Pós-Graduação em Ciências Veterinárias, Instituto de Veterinária, UFRRJ, BR-465 Km 7, Seropédica, RJ, 23897-000, Brazil

    Ericson R. de Mello

  3. Departamento de Biologia Animal, ICBS, UFRRJ, BR-465 Km 7, Seropédica, RJ, 23897-000, Brazil

    Viviane M. Lima & Bruno P. Berto

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  1. Carlos Nei Ortúzar-Ferreira
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  2. Mariana S. Oliveira
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  3. Lucas de Assis S. Andrade
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  4. Ericson R. de Mello
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Contributions

The study was designed by MSO, VML and BPB. Field work was performed by CNO-F, LASA and BPB. Laboratory procedures for maintenance, recovery, measurements, photomicrographs and isolation of oocysts were performed by CNO-F and LASA. Primers for amplification of new loci were designed by MSO and VML. DNA extraction, amplification and sequencing were performed by MSO, ERM and VML. New sequences were deposited in GenBank by VML. Morphometric statistical and phylogenetic analyses, figure editing and line drawings were performed by BPB. The manuscript was written by CNO-F, MSO and BPB and subsequently revised by all other authors. All authors read and approved the final manuscript.

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Correspondence to Mariana S. Oliveira or Bruno P. Berto.

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Field-collecting permits were issued by the Chico Mendes Institute for Biodiversity Conservation (Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio)), through the Biodiversity Authorization and Information System (Sistema de Autorização e Informação em Biodiversidade (SISBIO)) under license number 70132, and the Animal Ethics Committee (Comitê de Ética no Uso de Animais (CEUA)) of the University of Grande Rio (Universidade do Grande Rio (UNIGRANRIO)) under protocol number 021/2019. Banding permits and metal rings were issued by CEMAVE/ICMBio (Senior Ringer: BPB, registration 5967850). All applicable institutional, national, and international guidelines for the care and use of animals were followed.

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Ortúzar-Ferreira, C.N., Oliveira, M.S., Andrade, L.d.A.S. et al. Molecular and statistical approaches to the delimitation of Eimeriidae species: a case of extreme polymorphism in eimerian oocysts from the plumbeous pigeon Patagioenas plumbea (Vieillot, 1818) (Columbiformes) in South America. Parasitol Res 123, 42 (2024). https://doi.org/10.1007/s00436-023-08045-5

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