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

Abstract

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.

Co-structure analysis and genetic associations reveal insights into pinworms (Trypanoxyuris) and primates (Alouatta palliata) microevolutionary dynamics

“…The patterns of genetic structure, differentiation and diversity are more similar between howler monkeys and its host species-specific pinworm Trypanoxyuris multilabiatus than with T. minutus , the host genus-specific. These findings support the tight evolutionary association previously suggested in a phylogenetic study where divergence in T. multilabiatus follows mantled howler monkey subspecies, while in T. minutus this pattern is absent [ 37 ].…”

“…This is evident in the haplotype genealogies where pinworms showed complex networks formed by many unique haplotypes differing by few mutational steps, compared to the simple and more structured haplotype network in the howler monkey. Even though cophylogenetic patterns between pinworms and their primate hosts have been documented at macroevolutionary scales [ 27 , 28 , 37 ], the intraspecific analyses we performed did not detect congruent divergence among pinworms and howlers, suggesting instead distinct diversification processes. Disparate rates of molecular evolution have been documented in a host-specific and coevolving host–parasite system (e.g.…”

The relationship between pinworm (Trypanoxyuris) infection and gut bacteria in wild black howler monkeys (Alouatta pigra)

“…For example, alterations in bacterial abundance have been observed in mammalian hosts that were infected with GI parasites that exert health costs such as diarrhea, abdominal pain, anorexia, or deficient nutrient absorption (Li et al, 2012). In contrast, our data revealed that the relationship volutionary relationships with their hosts (Brooks & Glen, 1982;Solórzano-García et al, 2019). Because of this, serious damage from…”

“…In contrast, our data revealed that the relationship between Trypanoxyuris infection in black howler monkeys and gut bacterial community composition was considerably weak relative to other factors. Trypanoxyuris parasites belong to the group of oxyurid nematodes, which are organisms that have developed strong coevolutionary relationships with their hosts (Brooks & Glen, 1982; Solórzano‐García et al, 2019). Because of this, serious damage from Trypanoxyuris to their host is uncommon, though a death related to Trypanoxyuris infection has been reported in a wild brown howler monkey (Amato et al, 2002).…”

Pinworms of the red howler monkey (Alouatta seniculus) in Colombia: Gathering the pieces of the pinworm-primate puzzle

“…Also, examinations of Trypanoxyuris from different red howler monkey populations across their distribution range are needed to account for morphological and molecular variation within these pinworm species and lineages. For example, it is possible that the moderate differences observed within linages will become more evident as different host subspecies are sampled, as has happened with other Trypanoxyuris species (Solórzano-García et al, 2019); or that the species assemblages occurring in each population vary across the host range. Another possible approach might require the use of next generation sequencing (NGS) methods, gathering large molecular datasets (e.g., complete mitochondrial genomes) that could result in a more robust species delimitation (Ahmad et al, 2019; Duan et al, 2015; Gao et al, 2014; Jaleta et al, 2018).…”