Abstract

BackgroundIn parasitism arm race processes and red queen dynamics between host and parasites reciprocally mold many aspects of their genetics and evolution. We performed a parallel assessment of population genetics and demography of two species of pinworms with different degrees of host specificity (Trypanoxyuris multilabiatus, species-specific; and T. minutus, genus-specific) and their host, the mantled howler monkey (Alouatta palliata), based on mitochondrial DNA sequences and microsatellite loci (these only for the host). Given that pinworms and primates have a close co-evolutionary history, covariation in several genetic aspects of their populations is expected.ResultsMitochondrial DNA revealed two genetic clusters (West and East) in both pinworm species and howler monkeys, although population structure and genetic differentiation were stronger in the host, while genetic diversity was higher in pinworms than howler populations. Co-divergence tests showed no congruence between host and parasite phylogenies; nonetheless, a significant correlation was found between both pinworms and A. palliata genetic pairwise distances suggesting that the parasites’ gene flow is mediated by the host dispersal. Moreover, the parasite most infective and the host most susceptible haplotypes were also the most frequent, whereas the less divergent haplotypes tended to be either more infective (for pinworms) or more susceptible (for howlers). Finally, a positive correlation was found between pairwise p-distance of host haplotypes and that of their associated pinworm haplotypes.ConclusionThe genetic configuration of pinworm populations appears to be molded by their own demography and life history traits in conjunction with the biology and evolutionary history of their hosts, including host genetic variation, social interactions, dispersal and biogeography. Similarity in patterns of genetic structure, differentiation and diversity is higher between howler monkeys and T. multilabiatus in comparison with T. minutus, highlighting the role of host-specificity in coevolving processes. Trypanoxyuris minutus exhibits genetic specificity towards the most frequent host haplotype as well as geographic specificity. Results suggest signals of potential local adaptation in pinworms and further support the notion of correlated evolution between pinworms and their primate hosts.

Highlights

  • In parasitism arm race processes and red queen dynamics between host and parasites reciprocally mold many aspects of their genetics and evolution

  • Differentiation and diversity in host and parasites Structure results revealed two main genetic clusters corresponding to West and East sampling localities in both pinworm species and the howler monkey, the clustering is stronger in the host (Fig. 1)

  • Our mitochondrial DNA (mtDNA) findings show that pinworm gene flow is mediated by host dispersal, while at the same time no codivergence was observed between pinworms and their primate host

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Summary

Introduction

In parasitism arm race processes and red queen dynamics between host and parasites reciprocally mold many aspects of their genetics and evolution. Parasitism constitutes an intimate association in which arm race processes and red queen dynamics between host and parasites reciprocally mold many aspects of their genetics, physiology, morphology, behaviour, and life history traits [1,2,3]. Genetic studies about host–parasite systems have documented how the life cycle of the parasite and the degree of host specificity, jointly with host population size and dispersal capability, are key factors influencing the genetic structure of parasites and the potential to form coevolutionary associations [2, 4,5,6,7,8]. A cophylogenetic study evaluating the evolutionary histories of mammal hosts and helminth parasites showed that the host’s phylogenetic history is a key driver of host–parasite associations and parasite cross-species transmission potential [14]

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