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

Abstract

Background: In 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.

Results: Mitochondrial 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.

Conclusion: The 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.

Keywords: Coevolution; Ecological interactions; Gene flow; Host-specificity; Host–parasite associations; Parasitism.

Fig. 1

Study site and population genetic structure of Alouatta palliata and its pinworms Trypanoxyuris minutus and T. multilabiatus. A Maps showing sampling localities for host and the two parasite species; pie charts depict average per cluster assignment values in each population. B Barplots of ancestry proportions (Structure results), based on mitochondrial cytochrome b (cyt-b) and microsatellites loci (Mst) for the host and on mitochondrial cytochrome oxidase subunit 1 gene (COI) for the parasites, in the six studied regions: TUX = Los Tuxtlas (1. Montepio), SMT = Santa Marta (2. Playa, 3. Mirador Pilapa, 4. La Valentina), AGA = Agaltepec island (5), UXP = Uxpanapa (6. Plan de Arroyo, 7. Murillo Vidal), CML = Comalcalco (8. Hacienda la Luz, 9. Archaeological Site), PCH = Pichucalco (10); numbers correspond to locations in figure A

Fig. 2

Interpolation maps showing the distribution of genetic diversity in the host and the two pinworm species across their range in Mexico. A Alouatta palliata expected heterozygosity from microsatellite data; B A. palliata haplotype diversity (Hd) from cyt-b sequences; C Trypanoxyuris minutus and D T. multilabiatus haplotype diversity (Hd) from COI sequence data. Black dots represent sampling localities

Fig. 3

Haplotype genealogical relationships and demographic history of A Alouatta palliata, B Trypanoxyuris minutus and C T. multilabiatus. Top: median-joining haplotype networks, colours correspond to sampled geographic regions in southeast Mexico. Bottom: Bayesian skyline plots based on mtDNA showing changes in median female effective population sizes (Nef) through time. A Gradual population growth in howler monkeys until ca. 8000 years ago, decreasing afterwards until reaching a most recent Nef of 60,000. B Continuous population growth in T. minutus until ca. 250 years ago when the increase rate slowed down to a relatively constant trend (Nef from 1,303,500 to 1,347,000. C dynamic trend in T. multilabiatus population growth, remaining constant until ca. 2000 years ago and then fluctuating by decreasing from 32,250 to 24,700, followed by a rapid increase around 800 years ago up to 88,400, to a final decrease with a most recent Nef of 86,000

Fig. 4

Host/parasite haplotype associations between howler monkeys (Alouatta palliata) and pinworms (Trypanoxyuris minutus). Bars represent haplotype frequency and lines indicate the associations among haplotypes. Colours correspond to geographic regions. Black lines depict associations occurring in different regions. Top inset: Spearman correlation between T. minutus haplotype frequency and haplotype infectivity (number of different host haplotypes associated to each pinworm haplotype). Bottom inset: Spearman correlation between A. palliata haplotype frequency and vulnerability (number of different pinworm haplotypes co-occurring within each host haplotype)

Fig. 5

Mean genetic distance between haplotypes sharing host/parasite and those associated to different host/parasite haplotypes. A Line graphs showing the mean p-distance values between sharing (red) and differing host (light blue) for each Trypanoxyuris minutus haplotype. B Boxplot showing the differences on p-distance between pinworm haplotypes sharing and differing host haplotypes. C Line graphs showing the mean p-distance values between sharing and differing parasites for each Alouatta palliata haplotype. D Boxplot of the differences on p-distance between host haplotypes sharing and differing pinworm haplotypes. P values derived from Wilcoxon–Mann Whitney test