Haemosporidian parasites on latitudinal gradients: molecular epidemiology, reproductive output, and immunogenetics in the Thorn-tailed Rayadito (Aphrastura spinicauda)

Título traducido de la tesis: Parásitos hemosporidios en gradientes latitudinales: epidemiología molecular, rendimiento reproductivo e inmunogenética en el Rayadito (Aphrastura spinicauda)

Tesis doctoral


Host-parasite interactions represent an important selective force in free-living organisms, developing a co-evolutionary arms race with strategies for survival of their respective species. Biogeographic patterns such as the latitudinal gradients help to understand how these systems are co-evolve over different environments. Avian haemosporidian parasites and their bird hosts represent an excellent model to assess the follow ecological and evolutionary question: Is there a latitudinal gradient in the host-parasite interactions of haemosporidian parasites and the Thorn-tailed Rayadito?.
By using an integrative approach that include, epidemiology, mixed effects models, molecular techniques such as next generation sequencing, evolutionary models, and the monitoring of the reproductive biology of a Neotropical passerine in a long-term scenario. In this thesis, we analyzed the biogeographic patterns underlying distribution of the haemosporidian parasites, their associations with the reproductive output, and explore pathogen-mediated selection in the Toll-like receptors (TLR) genes of the innate immunity in the Thorn-tailed Rayadito (Aphrastura spinicauda) across of their latitudinal distribution (~ 3,000 km).
In Chapter I, we assessed the prevalence, diversity, and drivers of haemosporidian parasites (Leucocytozoon spp., Plasmodium spp., and Haemoproteus spp.) along a latitudinal gradient (30°–56° S), that encompass the total distribution (~3,000 km) of the Thorn-tailed Rayadito (Aphrastura spinicauda) in the South American temperate forests from Chile. We analyzed 516 individuals from 18 localities between 2010 and 2017 and observed an overall prevalence of 28.3% for haemosporidian parasites. Leucocytozoon spp. was the most prevalent parasite (25.8%). We recorded 19 distinct lineages (13 for Leucocytozoon spp., five for Plasmodium spp., and one for Haemoproteus spp.). Differences in haemosporidian prevalence and diversity by genus and type of habitat were observed in the latitudinal gradient. Further, we support the existence of a latitudinal associate distribution of Leucocytozoids in South America, where prevalence and diversity increase toward higher latitudes. Distribution of Leucocytozoon spp. was associated with sub-antarctic habitat (higher latitude) and explained by cold temperature and high precipitation. On the other hand, we lacked to find a latitudinal associate pattern for Plasmodium spp. and Haemoproteus spp., however low prevalence and high diversity were recorded in areas considered as a hotspot of biodiversity in Central Chile. Our findings confirmed the importance of habitat and climatic variables explaining prevalence, diversity, and distribution of haemosporidian parasites in a large latitudinal gradient, belonging the distribution of the Thorn-tailed Rayadito in the world's southernmost forests ecosystems.
In Chapter II, we compared several variables describing reproductive output (laying date, clutch size, incubation period, brood size, nestling body condition and early-life telomere length) of infected and non-infected parents (individually and as breeding pairs). We found that infected-females and breeding pairs with both parents infected showed significantly shorter incubation periods than un-infected Thorn-tailed Rayaditos. Furthermore, breeding pairs with both parents infected raised nestlings with higher body condition than nestlings for which infection was present in only one or in none of the parents. Our results suggest that the higher the parental investment, the higher the risk of relapse of chronic infection by Leucocytozoon spp. Thorn-tailed Rayaditos that decrease their incubation period pay the cost of infection to take advantage of early breeding through a greater more availability of resources, producing nestlings with higher body condition.
In Chapter III, we explored the genetic variation of five TLR genes (TLR2A, TLR2B, TLR3, TLR4, TLR7) for evidence of pathogen-mediated selection in the evolution of these genes in large geographical scale, belonging to the total distribution of Thorn-tailed Rayaditos. By using an integrative approach using next-generation sequencing and combining neutrality tests, codon selection models, and statistical associations with Leucocytozoon spp. infection, we provided evidence of diversifying and purifying selection acting on the TLRs under study. Furthermore, we observed that the most-frequent alleles (one to three) in the five TLRs confer susceptibility to Leucocytozoon spp. This study provides insights for the mechanisms underlying the host-parasite coevolutionary interactions between TLRs and Leucocytozoon spp., which suggest pathogen-mediated selection in a Red Queen scenario. In the arms race, Leucocytozoon spp. parasites have been adapted to the most frequent alleles and Rayadito TLRs are subject to diversifying selection.
Integrating all the results, our findings confirm the importance of habitat and climatic variables to explain the distribution of haemosporidian parasites on latitudinal gradients. The interactions between Thorn-tailed Rayaditos and the haemosporidian (Leucocytozoon spp.) parasites support an inverse latitudinal gradient of diversity. Parasite-mediated selection has been acting, developing a co-evolutionary arms race (the Red Queen hypothesis) with strategies for survival of both, hosts and parasites. In this co-evolutionary arms race, Leucocytozoon spp. have adapted to the most frequent alleles and the TLRs of the Rayadito are subject to diversifying selection.
Fecha de adjudicación16 feb 2021
Idioma originalInglés

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