{"title":"Genetic infrapopulation sizes in blood parasites: a pilot quantification of the bottleneck in louse fly vectors","authors":"Kai Fischer, Nayden Chakarov","doi":"10.3389/fevo.2024.1319829","DOIUrl":null,"url":null,"abstract":"IntroductionBottleneck events are crucial for the strength of genetic drift, selection and speed of evolution. They are believed to play a particularly prominent role for parasitic infrapopulations, inhabiting single host individuals, which are often established by very few parasite individuals during transmission. In vector-borne pathogens, the bottlenecking effects can even be serialized through repeated filtering of parasitic stages at different tissues and organs of the vector. Using qPCR we aimed to quantify the number of potentially transmittable sporozoites of the hemosporidian blood parasite <jats:italic>Haemoproteus columbae</jats:italic> in the specialized vector louse flies <jats:italic>Pseudolynchia canariensis</jats:italic> which transmit these parasites between house pigeon hosts <jats:italic>Columba livia</jats:italic>.ResultsBased on qPCR measurements of organ-derived DNA of individual louse flies, we estimate that the midgut of these vectors contains on average 20 parasites, the hindgut and other intestines ca. 50 parasites and the salivary glands ca. 5 parasite cells. Nearly one third of all vector individuals appeared to lack parasite DNA, despite having only infected hosts as blood meal sources. The magnitude of parasite numbers in midgut and salivary glands tended to correlate positively.DiscussionOur results indicate, potential severe bottlenecking of parasite populations during individual transmission events and a probable effect of individual vector immunity on this variable. However, this may be partly alleviated by the coloniality of house pigeons, the frequency of louse flies and their daily feeding events in most populations, leading to repeated transmission opportunities, decreased quasi-vertical transmission between parents and offspring and probable panmixia of <jats:italic>Haemoproteus columbae</jats:italic> lineages. Many of these mechanisms might not apply in other host-vector systems. We propose several additional molecular and microscopical tools to improve the accuracy of estimating parasite population sizes in vectors and call for more estimations in different vector species to better understand the co-evolution between malaria-like blood parasites and their avian and insect hosts.","PeriodicalId":12367,"journal":{"name":"Frontiers in Ecology and Evolution","volume":"28 1","pages":""},"PeriodicalIF":2.4000,"publicationDate":"2024-04-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Frontiers in Ecology and Evolution","FirstCategoryId":"93","ListUrlMain":"https://doi.org/10.3389/fevo.2024.1319829","RegionNum":3,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"ECOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
IntroductionBottleneck events are crucial for the strength of genetic drift, selection and speed of evolution. They are believed to play a particularly prominent role for parasitic infrapopulations, inhabiting single host individuals, which are often established by very few parasite individuals during transmission. In vector-borne pathogens, the bottlenecking effects can even be serialized through repeated filtering of parasitic stages at different tissues and organs of the vector. Using qPCR we aimed to quantify the number of potentially transmittable sporozoites of the hemosporidian blood parasite Haemoproteus columbae in the specialized vector louse flies Pseudolynchia canariensis which transmit these parasites between house pigeon hosts Columba livia.ResultsBased on qPCR measurements of organ-derived DNA of individual louse flies, we estimate that the midgut of these vectors contains on average 20 parasites, the hindgut and other intestines ca. 50 parasites and the salivary glands ca. 5 parasite cells. Nearly one third of all vector individuals appeared to lack parasite DNA, despite having only infected hosts as blood meal sources. The magnitude of parasite numbers in midgut and salivary glands tended to correlate positively.DiscussionOur results indicate, potential severe bottlenecking of parasite populations during individual transmission events and a probable effect of individual vector immunity on this variable. However, this may be partly alleviated by the coloniality of house pigeons, the frequency of louse flies and their daily feeding events in most populations, leading to repeated transmission opportunities, decreased quasi-vertical transmission between parents and offspring and probable panmixia of Haemoproteus columbae lineages. Many of these mechanisms might not apply in other host-vector systems. We propose several additional molecular and microscopical tools to improve the accuracy of estimating parasite population sizes in vectors and call for more estimations in different vector species to better understand the co-evolution between malaria-like blood parasites and their avian and insect hosts.
期刊介绍:
Frontiers in Ecology and Evolution publishes rigorously peer-reviewed research across fundamental and applied sciences, to provide ecological and evolutionary insights into our natural and anthropogenic world, and how it should best be managed. Field Chief Editor Mark A. Elgar at the University of Melbourne is supported by an outstanding Editorial Board of international researchers. This multidisciplinary open-access journal is at the forefront of disseminating and communicating scientific knowledge and impactful discoveries to researchers, academics and the public worldwide.
Eminent biologist and theist Theodosius Dobzhansky’s astute observation that “Nothing in biology makes sense except in the light of evolution” has arguably even broader relevance now than when it was first penned in The American Biology Teacher in 1973. One could similarly argue that not much in evolution makes sense without recourse to ecological concepts: understanding diversity — from microbial adaptations to species assemblages — requires insights from both ecological and evolutionary disciplines. Nowadays, technological developments from other fields allow us to address unprecedented ecological and evolutionary questions of astonishing detail, impressive breadth and compelling inference.
The specialty sections of Frontiers in Ecology and Evolution will publish, under a single platform, contemporary, rigorous research, reviews, opinions, and commentaries that cover the spectrum of ecological and evolutionary inquiry, both fundamental and applied. Articles are peer-reviewed according to the Frontiers review guidelines, which evaluate manuscripts on objective editorial criteria. Through this unique, Frontiers platform for open-access publishing and research networking, Frontiers in Ecology and Evolution aims to provide colleagues and the broader community with ecological and evolutionary insights into our natural and anthropogenic world, and how it might best be managed.