Hepatozoon en Chile y las Américas: diversidad genética y relaciones filogenéticas
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Date
2025
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Universidad de Concepción
Abstract
Hepatozoon (Apicomplexa: Adeleorina) es un género de hemoparásitos que infecta leucocitos y eritrocitos de vertebrados, cuya transmisión ocurre principalmente mediante la ingestión de artrópodos hematófagos (AH) infectados con ooquistes. Otras rutas de infección incluyen la transmisión vertical (transplacentaria) y la depredación. En la fauna silvestre, estos parásitos se mantienen en ciclos complejos que involucran múltiples hospedadores y vectores, lo que dificulta su caracterización desde una perspectiva ecológica y sistemática. En América, el conocimiento sobre la diversidad genética, distribución y vectores naturales de Hepatozoon continúa siendo limitado y fragmentario, particularmente en ecosistemas del Cono Sur de América, donde convergen distintas regiones biogeográficas.
El objetivo de este trabajo fue examinar el estado del conocimiento sobre el género Hepatozoon en mamíferos silvestres de las Américas, y analizar la diversidad genética y las relaciones filogenéticas del género en hospedadores silvestres y artrópodos hematófagos en Chile. Asimismo, se compararon los linajes locales con patrones filogenéticos previamente descritos en las Américas. Para ello, se empleó un enfoque multidimensional que incluyó: (1) una revisión sistemática de la literatura científica siguiendo el protocolo PRISMA; (2) análisis filogenéticos de secuencias del gen 18S ARNr obtenidas de GenBank, incluyendo secuencias correspondientes a mamíferos silvestres de las Américas, así como otras secuencias de Hepatozoon recuperadas de aves, pequeños mamíferos, carnívoros, anfibios y reptiles de distintas regiones del mundo; y (3) estudios moleculares basados en muestras recolectadas en terreno en diferentes localidades de Chile.
Se obtuvieron y analizaron muestras de sangre de roedores cricétidos capturados en siete localidades del norte de Chile, así como de ectoparásitos (garrapatas, pulgas, ácaros, piojos y triatominos) recolectados en 23 localidades a lo largo del país. La detección del ADN de Hepatozoon en muestras de roedores silvestres se realizó mediante PCR convencional dirigida al gen de la subunidad ribosomal menor (18S ARNr). Paralelamente, se empleó secuenciación de alto rendimiento mediante la plataforma Oxford Nanopore para la obtención de secuenciadas del mismo gen a partir de ADN extraído de AH. Las secuencias obtenidas mediante ambos métodos fueron analizadas utilizando enfoques de sistemática molecular para evaluar su diversidad genética, estructura poblacional y relaciones evolutivas con linajes previamente descritos.
Los resultados revelaron la presencia de múltiples linajes de Hepatozoon en roedores silvestres de los géneros Phyllotis, Abrothrix y Oligoryzomys, algunos relacionados con secuencias previamente detectadas en garrapatas del género Ixodes. Asimismo, se identificaron nuevos linajes en ácaros y triatominos, constituyendo el primer registro molecular de Hepatozoon en estos artrópodos a escala global. Además, el análisis de varianza molecular (AMOVA) mostró que la identidad del hospedador, y no la geografía, puede impulsar la diferenciación genética del parásito en Chile.
Este estudio proporciona evidencia de la presencia de ADN de Hepatozoon en vertebrados y artrópodos no reportados previamente, y destaca su elevada diversidad genética, la cual podría estar influenciada por la identidad de sus hospederos vertebrados. Además, pone de relieve a Hepatozoon como un potencial agente patógeno en mamíferos silvestres amenazados y el papel de los cánidos silvestres como propagadores de infecciones por Hepatozoon en las Américas. Finalmente, refuerza la importancia de integrar enfoques moleculares y ecológicos para una mejor comprensión de los ciclos de transmisión de parásitos emergentes en ecosistemas poco estudiados.
Hepatozoon (Apicomaplexa: Adeleorina) is a genus of blood-dwelling protozoa that invade vertebrate white and red blood cells. Most infections arise when vertebrates eat blood-sucking arthropods (BSA) already packed with infective oocysts, though other infections routes include vertical (transplacental) transmission and predation. In wildlife populations these parasites circulate through intricate, multi-host, multi-vector networks, making complicated efforts to pin down their ecology and systematics. In the Americas, knowledge about the genetic diversity, distribution, and natural vectors of Hepatozoon remains limited and fragmentary, particularly in ecosystems in the Southern Cone of South America, where different biogeographic regions converge. This study first examined the current state of knowledge about the genus Hepatozoon on wild mammals of the Americas. Then, it aimed to analyze the genetic diversity and phylogenetic relationships of the genus in wild hosts and hematophagous arthropods in Chile. Local lineages were compared with previously described phylogenetic patterns in the Americas. A multidimensional approach was used to achieve this objective. First, a systematic review of the scientific literature was conducted according to the PRISMA protocol. Second, phylogenetic analyses were performed on the minor ribosomal subunit (18S rRNA) gene sequences obtained from GenBank —these sequences included those from wild mammals in the Americas, as well as other Hepatozoon sequences from birds, small mammals, carnivores, amphibians, and reptiles in various regions worldwide— and third, molecular studies were conducted on samples collected in different locations in Chile. Blood samples were obtained from cricetid rodents captured in seven locations in northern Chile and analyzed. Additionally, ectoparasites (ticks, fleas, mites, lice, and triatomines) were collected in 23 locations throughout the country and analyzed. Hepatozoon DNA was detected in the wild rodent samples using conventional PCR targeting the 18S rRNA. Concurrently, high-throughput sequencing was performed on the Oxford Nanopore platform to obtain sequences of the same gene from DNA extracted from BSAs. We analyzed the sequences obtained by both methods using molecular systematic approaches to assess their genetic diversity, population structure, and evolutionary relationships with previously described lineages. The results revealed multiple Hepatozoon lineages in wild rodents of the genera Phyllotis, Abrothrix, and Oligoryzomys. Some of these lineages were related to sequences previously detected in Ixodes ticks. New lineages were also identified in mites and triatomines, marking the first molecular record of Hepatozoon in these arthropods worldwide. Additionally, molecular variance analysis (AMOVA) showed that host identity, rather than geography, may drive genetic differentiation of the parasite in Chile. This study provides evidence of Hepatozoon DNA in vertebrates and BSAs that have not been reported previously. It also highlights the parasite’s high genetic diversity, which may be influenced by the identity of its vertebrate hosts. Additionally, the study identifies Hepatozoon as a potential pathogen in endangered wild mammals and emphasizes the role of wild canids in spreading Hepatozoon infections in the Americas. Finally, the study emphasizes the importance of integrating molecular and ecological approaches to better understand the transmission cycles of emerging parasites in poorly studied ecosystems.
Hepatozoon (Apicomaplexa: Adeleorina) is a genus of blood-dwelling protozoa that invade vertebrate white and red blood cells. Most infections arise when vertebrates eat blood-sucking arthropods (BSA) already packed with infective oocysts, though other infections routes include vertical (transplacental) transmission and predation. In wildlife populations these parasites circulate through intricate, multi-host, multi-vector networks, making complicated efforts to pin down their ecology and systematics. In the Americas, knowledge about the genetic diversity, distribution, and natural vectors of Hepatozoon remains limited and fragmentary, particularly in ecosystems in the Southern Cone of South America, where different biogeographic regions converge. This study first examined the current state of knowledge about the genus Hepatozoon on wild mammals of the Americas. Then, it aimed to analyze the genetic diversity and phylogenetic relationships of the genus in wild hosts and hematophagous arthropods in Chile. Local lineages were compared with previously described phylogenetic patterns in the Americas. A multidimensional approach was used to achieve this objective. First, a systematic review of the scientific literature was conducted according to the PRISMA protocol. Second, phylogenetic analyses were performed on the minor ribosomal subunit (18S rRNA) gene sequences obtained from GenBank —these sequences included those from wild mammals in the Americas, as well as other Hepatozoon sequences from birds, small mammals, carnivores, amphibians, and reptiles in various regions worldwide— and third, molecular studies were conducted on samples collected in different locations in Chile. Blood samples were obtained from cricetid rodents captured in seven locations in northern Chile and analyzed. Additionally, ectoparasites (ticks, fleas, mites, lice, and triatomines) were collected in 23 locations throughout the country and analyzed. Hepatozoon DNA was detected in the wild rodent samples using conventional PCR targeting the 18S rRNA. Concurrently, high-throughput sequencing was performed on the Oxford Nanopore platform to obtain sequences of the same gene from DNA extracted from BSAs. We analyzed the sequences obtained by both methods using molecular systematic approaches to assess their genetic diversity, population structure, and evolutionary relationships with previously described lineages. The results revealed multiple Hepatozoon lineages in wild rodents of the genera Phyllotis, Abrothrix, and Oligoryzomys. Some of these lineages were related to sequences previously detected in Ixodes ticks. New lineages were also identified in mites and triatomines, marking the first molecular record of Hepatozoon in these arthropods worldwide. Additionally, molecular variance analysis (AMOVA) showed that host identity, rather than geography, may drive genetic differentiation of the parasite in Chile. This study provides evidence of Hepatozoon DNA in vertebrates and BSAs that have not been reported previously. It also highlights the parasite’s high genetic diversity, which may be influenced by the identity of its vertebrate hosts. Additionally, the study identifies Hepatozoon as a potential pathogen in endangered wild mammals and emphasizes the role of wild canids in spreading Hepatozoon infections in the Americas. Finally, the study emphasizes the importance of integrating molecular and ecological approaches to better understand the transmission cycles of emerging parasites in poorly studied ecosystems.
Description
Tesis presentada para optar al grado de Doctor en Ciencias Veterinarias
Keywords
Fauna silvestre Enfermedades, Roedores Chile, Genética animal