Haemosporidian parasites on latitudinal gradients : molecular epidemiology, reproductive output, and immunogenetics in the Thorn-tailed Rayadito (Aphrastura spinicauda)
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2020
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es
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Universidad Andrés Bello
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Resumen
Las interacciones parásito-hospedero son fuerzas selectivas importantes en la naturaleza, han
desarrollado una carrera armamentista co-evolutiva con estrategias que permiten la
supervivencia de las especies implicadas. Patrones biogeográficos, tales como los gradientes
latitudinales ayudan a comprender la coevolución de estos sistemas en diferentes ambientes.
Los hemosporidios aviares y sus hospederos representan un excelente modelo para evaluar la
siguiente pregunta ecológica y evolutiva:
¿Existe un gradiente latitudinal en las interacciones parásito-hospedero entre el Rayadito y
los parásitos hemosporidios?
Esta tesis utiliza un abordaje que incluye epidemiología, modelos mixtos, técnicas
moleculares de secuenciación masiva, modelos evolutivos y datos de la biología reproductiva a
largo plazo en un paseriforme Neotropical, este enfoque integrador nos permitió analizar los
patrones biogeográficos de los parásitos hemosporidios, sus asociaciones sobre la inversión
reproductiva y explorar la selección mediada por patógenos en los genes Toll-like receptors
(TLRs) de la inmunidad innata en el Rayadito (Aphrastura spinicauda) a través de su rango de
distribución latitudinal (~ 3000 km).
En el Capítulo I, evaluamos la prevalencia, la diversidad y los factores que influencian
a los parásitos hemosporidios (Leucocytozoon spp., Plasmodium spp. y Haemoproteus spp.) a
través de un gradiente latitudinal (30° -56° S) en los bosques templados de Chile. Analizamos
516 individuos en 18 localidades entre 2010-2017. Observamos una prevalencia general de
28,3% para los tres géneros agrupados, siendo Leucocytozoon spp. el más prevalente (25,8%).
Registramos 19 linajes distintos (13 para Leucocytozoon spp., cinco para Plasmodium spp. y
uno para Haemoproteus spp.). Se observaron diferencias en la prevalencia y diversidad por
género y tipo de hábitat en el gradiente latitudinal. Interesantemente, nuestros resultados
evidenciaron la existencia de un gradiente latitudinal inverso para los leucocitozoides en
América del Sur, donde la prevalencia y la diversidad aumentan hacia latitudes más altas. La
distribución de Leucocytozoon spp. se asoció al hábitat subantártico (latitudes altas) y explicado
por la temperatura más fría y las altas precipitaciones lo que estaría favoreciendo las
interacciones parásito-hospedero. Por otro lado, no observamos un patrón latitudinal asociado a
la distribución de Plasmodium spp. y Haemoproteus spp., sin embargo, se registró una baja
prevalencia y alta diversidad en áreas consideradas como un hotspot de biodiversidad en Chile
central. Nuestros hallazgos confirmaron la importancia del hábitat y las variables climáticas para
explicar la prevalencia, diversidad y la distribución de los parásitos hemosporidios en un
gradiente latitudinal extenso, correspondiente al rango de distribución del Rayadito en los
bosques templados más australes del mundo.
En el Capítulo II, comparamos múltiples variables de la inversión parental (fecha de
puesta, tamaño de la nidada, período de incubación, número de pichones, condición corporal y
la longitud de los telómeros en los pichones) entre padres infectados y no infectados con
Leucocytozoon spp. (individualmente y como parejas reproductoras) en la población de Isla de
Navarino (55°-40° S). Evaluamos 104 parejas reproductoras y 487 polluelos durante cinco
temporadas reproductivas (2010-2014). Observamos que las hembras infectadas y las parejas
con ambos Rayaditos infectados presentaron un período de incubación significativamente más
corto que los Rayaditos no infectados. Además, esas parejas reproductoras (ambas infectadas)
criaron pichones con una condición corporal más alta que los pichones de solo hembras, machos
o ambos padres no infectados. Nuestros resultados sugieren que, a una mayor inversión parental,
los reproductores presentan mayor es el riesgo de recaída de la infección crónica por
Leucocytozoon spp. Los Rayaditos probablemente disminuyen su periodo de incubación por las
ventajas que ofrece el inicio de la época reproductiva (mayor disponibilidad de recursos), los
Rayaditos pagan el costo de la infección por los beneficios para su descendencia, es decir, una
mayor condición corporal en los pichones.
En el Capítulo III, exploramos la variación genética en cinco genes TLR (TLR2A,
TLR2B, TLR3, TLR4, TLR7) y su asociación con la infección con Leucocytozoon spp.
(selección mediada por patógenos) en seis poblaciones a lo largo de la distribución del Rayadito.
Analizamos 184 individuos (100 no infectados y 84 infectados con Leucocytozoon spp.).
Mediante un enfoque integrador de genes candidatos, técnicas de secuenciación masiva y
combinando pruebas de neutralidad, modelos de selección de codones y sus asociaciones
estadísticas con la infección por Leucocytozoon spp., evidenciamos selección diversificadora y
purificadora actuando en los genes TLRs. Además, observamos que los alelos más frecuentes
(entre uno a tres) en los cinco genes TLRs confieren susceptibilidad a Leucocytozoon spp. Este
estudio proporciona evidencia sobre los mecanismos subyacentes a las interacciones coevolutivas entre Leucocytozoon spp. y los genes TLR, lo que sugiere que selección mediada por
patógenos en un escenario de “Reina Roja”. En esta carrera armamentista co-evolutiva,
Leucocytozoon spp. se han adaptado a los alelos más frecuentes y los TLRs del Rayadito están
sujetos a una selección diversificadora.
Integrando los resultados de esta tesis, nuestras observaciones confirman la importancia
del hábitat y las variables climáticas para explicar la distribución de los parásitos hemosporidios
en gradientes latitudinales. Las interacciones co-evolutivas entre los Rayaditos y los parásitos
hemosporidios (Leucocytozoon spp.) evidencian un gradiente latitudinal de distribución inverso.
La selección mediada por parásitos ha estado actuando, desarrollando una carrera armamentista
co-evolutiva (hipótesis de la reina roja) con estrategias de supervivencia tanto para los
hospederos como para los parásitos. En esta carrera armamentista co-evolutiva, Leucocytozoon
spp. se han adaptado a los alelos más frecuentes y los TLRs del Rayadito están sujetos a una
selección diversificadora.
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.
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.
Notas
Tesis (Doctor en Medicina de la Conservación)
Palabras clave
Thorn-Tailed Rayadito, Investigaciones, Parásitos., Aves, /insectos, peces, etc