Skip to main content Accessibility help

Unveiling patterns of genetic variation in parasite–host associations: an example with pinworms and Neotropical primates

  • Brenda Solórzano García (a1) (a2), Amanda D. Melin (a3) (a4) (a5), Filippo Aureli (a6) (a7) and Gerardo Pérez Ponce de León (a1)

Patterns of genetic variation among populations can reveal the evolutionary history of species. Pinworm parasites are highly host specific and form strong co-evolutionary associations with their primate hosts. Here, we describe the genetic variation observed in four Trypanoxyuris species infecting different howler and spider monkey subspecies in Central America to determine if historical dispersal processes and speciation in the host could explain the genetic patterns observed in the parasites. Mitochondrial (cox1) and ribosomal (28S) DNA were analysed to assess genetic divergence and phylogenetic history of these parasites. Sequences of the 28S gene were identical within pinworms species regardless of host subspecies. However, phylogenetic analyses, haplotype relationships and genetic divergence with cox1 showed differentiation between pinworm populations according to host subspecies in three of the four Trypanoxyuris species analysed. Haplotype separation between host subspecies was not observed in Trypanoxyuris minutus, nor in Trypanoxyuris atelis from Ateles geoffoyi vellerosus and Ateles geoffoyi yucatanensis. Levels of genetic diversity and divergence in these parasites relate with such estimates reported for their hosts. This study shows how genetic patterns uncovered in parasitic organisms can reflect the host phylogenetic and biogeographic histories.

Corresponding author
Author for correspondence: Brenda Solórzano García, E-mail:
Hide All
Bandelt, HJ, Forster, P and Röhl, A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 3748.
Barrett, LG, Thrall, PH, Burdon, JJ and Linde, CC (2008) Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends in Ecology & Evolution 23, 678685.
Blasco-Costa, I and Poulin, R (2013) Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology 140, 13161322.
Blouin, M (1998) Mitochondrial DNA diversity in nematodes. Journal of Helminthology 72, 285289.
Bradburd, GS, Ralph, PL and Coop, GM (2013) Disentangling the effects of geographic and ecological isolation on genetic differentiation. Evolution 67, 32583273.
Carmichael, LE, Krizan, J, Nagy, JA, Fuglei, E, Dumond, M, Johnson, D, Veitch, A, Berteaux, D and Strobeck, C (2007) Historical and ecological determinants of genetic structure in Arctic canids. Molecular Ecology 16, 34663483.
Collins, AC and Dubach, JM (2000) Phylogenetic relationships of spider monkeys (Ateles) based on mitochondrial DNA variation. International Journal of Primatology 21, 381420.
Conga, DF, Giese, EG, Serra-Freire, NM, Bowler, M and Mayor, P (2016) Morphology of the oxyurid nematodes Trypanoxyuris (t.) cacajao n. sp. and T. (T.) ucayalii n. sp. from the red uakari monkey Cacajao calvus ucayalii in the Peruvian Amazon. Journal of Helminthology 90, 483493.
Cortés-Ortiz, L, Bermingham, E, Rico, C, Rodriguez-Luna, E, Sampaio, I and Ruiz-Garcia, M (2003) Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Molecular Phylogenetics and Evolution 26, 6481.
Criscione, CD (2008) Parasite co-structure: broad and local scale approaches. Parasite 15, 439443.
Ellsworth, JA and Hoelzer, GA (2006) Genetic evidence on the historical biogeography of Central American howler monkeys. In Lehman, SM and Fleagle, LG (eds), Primate Biogeography, Progress and Prospects. New York: Springer, pp. 81103.
Ford, S (2006) The biogeographic history of Mesoamerican primates. In Estrada, A, Garber, P, Pavelka, M and Luecke, L (eds), New Perspectives in the Study of Mesoamerican Primates: Distribution, Ecology, Behavior, and Conservation. New York: Springer, pp. 81114.
Hasegawa, H (2009) Methods of collection and identification of minute nematodes from the feces of primates, with special application to coevolutionary study of pinworms. In Huffman, MA and Chapman, CA (eds), Primate Parasite Ecology. The Dynamics and Study of Host-Parasite Relationships. UK: Cambridge University Press, pp. 1946.
Hasegawa, H, Ikeda, Y, Dias-Aquino, JJ and Fukui, D (2004) Redescription of two pinworms from the black-handed spider monkey, Ateles geoffroyi, with reestablishment of Oxyuronema and Buckleyenterobius (nematoda: Oxyuroidea). Comparative Parasitology 71, 166174.
Hasegawa, H, Sato, H and Torii, H (2012) Redescription of Enterobius (enterobius) macaci yen, 1973 (Nematoda: Oxyuridae: Enterobiinae) based on material collected from wild Japanese macaque, Macaca fuscata (Primates: Cecopithecidae). Journal of Parasitology 98, 152159.
Hey, J and Machado, CA (2003) The study of structured populations-new hope for a difficult and divided science. Nature Reviews. Genetics 4, 535543.
Hugot, JP (1999) Primates and their pinworm parasites: the Cameron Hypothesis revisited. Systematic Biology 48, 523546.
Hugot, JP, Gardner, SL and Morand, S (1996) The Enterobiinae subfam. nov. (Nematoda, Oxyurida) pinworm parasites of primates and rodents. International Journal for Parasitology 26, 147159.
Huyse, T, Poulin, R and Théron, A (2005) Speciation in parasites: a population genetics approach. Trends in Parasitology 21, 469475.
Jasso-del Toro, C, Márquez-Valdelamar, L and Mondragón-Ceballos, R (2016) Diversidad genética en grupos de monos aulladores de manto (Alouatta palliata mexicana) en la Reserva de la Biosfera Los Tuxtlas (Veracruz, México). Revista Mexicana de Biodiversidad 87, 10691079.
Latch, EK, Reding, DM, Heffelfinger, JR, Alcalá-Galván, CH and Rhodes, OE (2014) Range-wide analysis of genetic structure in a widespread, highly mobile species (Odocoileus hemionus) reveals the importance of historical biogeography. Molecular Ecology 23, 31713190.
Miller, M, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop, New Orleans, pp. 18.
Morales-Jimenez, AL, Cortés-Ortiz, L and Di Fiore, A (2015) Phylogenetic relationships of Mesoamerican spider monkeys (Ateles geoffroyi): Molecular evidence suggests the need for a revised taxonomy. Molecular phylogenetics and evolution 82, 484494.
Nadler, S (1995) Microevolution and the genetic structure of parasite populations. Journal of Parasitology 81, 395403.
Nadler, SA and Pérez-Ponce de León, G (2011) Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138, 16881709.
Nakano, T, Okamoto, M, Ikeda, Y and Hasegawa, H (2006) Mitochondrial cytochrome c oxidase subunit 1 gene and nuclear rDNA regions of Enterobius vermicularis parasitic in captive chimpanzees with special reference to its relationship with pinworms in humans. Parasitology Research 100, 5157.
Ngeve, MN, Van der Stocken, T, Menemenlis, D, Koedam, N and Triest, L (2017) Hidden founders? Strong bottlenecks and fine-scale genetic structure in mangrove populations of the Cameroon Estuary complex. Hydrobiologia 803, 189207.
Nylander, JAA (2004) MrModeltest v2. Uppsala University: Evolutionary Biology Centre. Program distributed by the author.
Polzin, T and Dabeschmand, SV (2003) On Steiner trees and minimum spanning trees in hypergraphs. Operations Research Letters 31, 1220.
Ronquist, F and Huelsenbeck, JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 15721574.
Rozas, J, Sánchez-DelBarrio, JC, Messeguer, X and Rozas, R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics (Oxford, England) 19, 24962497.
Ruiz-García, M, Lichilín, N, Escobar-Armel, P, Rodríguez, G and Gutiérrez-Espeleta, G (2016) Historical genetic demography and some insights into the systematics of Ateles (Atelidae, Primates) by means of diverse mitochondrial genes. In Ruiz-García, M and Shostell, JM (eds), Phylogeny, Molecular Population Genetics, Evolutionary Biology and Conservation of the Neotropical Primates. New York, NY: Nova Sience Publisher Inc., pp. 143.
Ruiz-García, M, Cerón, Á, Sánchez-Castillo, S, Rueda-Zozaya, P, Pinedo-Castro, M, Gutierrez-Espeleta, G and Shostell, JM (2017) Phylogeography of the mantled howler monkey (Alouatta palliata; Atelidae, Primates) across its geographical range by means of mitochondrial genetic analyses and new insights about the phylogeny of Alouatta. Folia Primatologica 88, 421454.
Rylands, AB, Groves, CP, Mittermeier, RA, Cortes-Ortiz, L and Hines, J (2006) Taxonomy and distributions of Mesoamerican primates. In Estrada, A, Garber, PA, Pavelka, M and Luecke, L (eds), New Perspectives in the Study of Mesoamerican Primates: Distribution, Ecology, Behavior and Conservation. New York: Springer, pp. 2979.
Solórzano-García, B and Pérez-Ponce de León, G (2018) Parasites of Neotropical primates: a review. International Journal of Primatology 39, 155182.
Solórzano-García, B, Nadler, SA and Pérez Ponce de León, G (2015) Trypanoxyuris atelis and T. atelophora (Nematoda: Oxyuridae) in wild spider monkeys (Ateles geoffroyi) in tropical rain forest in Mexico: Morphological and molecular evidence. Parasitology International 64, 229235.
Solórzano-García, B, Nadler, SA and Pérez-Ponce de León, G (2016) Pinworm diversity in free-ranging howler monkeys (Alouatta spp.) in Mexico: Morphological and molecular evidence for two new Trypanoxyuris species (Nematoda: Oxyuridae). Parasitology International 65, 401411.
Solórzano-García, B, Gasca-Pineda, J, Poulin, R and Pérez-Ponce de León, G (2017) Lack of genetic structure in pinworm populations from New World primates in forest fragments. International Journal for Parasitology 47, 941950.
Stamatakis, A (2014) RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 13121313.
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biological Evolution 30, 27252729.
Whiteman, NK and Parker, PG (2005) Using parasites to infer host population history: a new rational for parasite conservation. Animal Conservation 8, 175181.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Type Description Title
Supplementary materials

Solórzano García et al. supplementary material
Figure S1

 Word (118 KB)
118 KB


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed