Variation and trade-offs in life history traits of the protist parasite Monocystis perplexa (Apicomplexa) in its earthworm host Amynthas agrestis

The life history of a parasite describes its partitioning of assimilated resources into growth, reproduction, and transmission effort, and its precise timing of developmental events. The life cycle, in contrast, charts the sequence of morphological stages from feeding to the transmission forms. Phen...

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Main Authors: Erin L. Keller, Jos. J. Schall
Format: Article
Language:English
Published: PeerJ Inc. 2024-03-01
Series:PeerJ
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Online Access:https://peerj.com/articles/17161.pdf
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author Erin L. Keller
Jos. J. Schall
author_facet Erin L. Keller
Jos. J. Schall
author_sort Erin L. Keller
collection DOAJ
description The life history of a parasite describes its partitioning of assimilated resources into growth, reproduction, and transmission effort, and its precise timing of developmental events. The life cycle, in contrast, charts the sequence of morphological stages from feeding to the transmission forms. Phenotypic plasticity in life history traits can reveal how parasites confront variable environments within hosts. Within the protist phylum Apicomplexa major clades include the malaria parasites, coccidians, and most diverse, the gregarines (with likely millions of species). Studies on life history variation of gregarines are rare. Therefore, life history traits were examined for the gregarine Monocystis perplexa in its host, the invasive earthworm Amynthas agrestis at three sites in northern Vermont, United States of America. An important value of this system is the short life-span of the hosts, with only seven months from hatching to mass mortality; we were thus able to examine life history variation during the entire life cycle of both host and parasite. Earthworms were collected (N = 968 over 33 sample periods during one host season), then parasites of all life stages were counted, and sexual and transmission stages measured, for each earthworm. All traits varied substantially among individual earthworm hosts and across the sites. Across sites, timing of first appearance of infected earthworms, date when transmission stage (oocysts packed within gametocysts) appeared, date when number of both feeding (trophic) cells and gametocysts were at maximum, and date when 100% of earthworms were infected differed from 2–8 weeks, surprising variation for a short season available for parasite development. The maximal size of mating cells varied among hosts and across sites and this is reflected in the number of oocysts produced by the gametocyst. A negative trade-off was observed for the number of oocysts and their size. Several patterns were striking: (1) Prevalence reached 100% at all sites by mid season, only one to three weeks after parasites first appeared in the earthworms. (2) The number of parasites per host was large, reaching 300 × 103 cells in some hosts, and such high numbers were present even when parasites first appeared in the host. (3) At one site, few infected earthworms produced any oocysts. (4) The transmission rate to reach such high density of parasites in hosts needed to be very high for a microbe, from >0.33% to >34.3% across the three sites. Monocystis was one of the first protist parasites to have its life cycle described (early 19th century), but these results suggest the long-accepted life cycle of Monocystis could be incomplete, such that the parasites may be transmitted vertically (within the earthworm’s eggs) as well as horizontally (leading to 100% prevalence) and merogony (asexual replication) could be present, not recognized for Monocystis, leading to high parasitemia even very early in the host’s season.
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spelling doaj.art-492a78aaeb5842758e7a7edb610bdd002024-03-28T15:05:18ZengPeerJ Inc.PeerJ2167-83592024-03-0112e1716110.7717/peerj.17161Variation and trade-offs in life history traits of the protist parasite Monocystis perplexa (Apicomplexa) in its earthworm host Amynthas agrestisErin L. Keller0Jos. J. Schall1School of Biological Sciences, Washington State University, Pullman, WA, United States of AmericaDepartment of Biology, University of Vermont, Burlington, VT, United States of AmericaThe life history of a parasite describes its partitioning of assimilated resources into growth, reproduction, and transmission effort, and its precise timing of developmental events. The life cycle, in contrast, charts the sequence of morphological stages from feeding to the transmission forms. Phenotypic plasticity in life history traits can reveal how parasites confront variable environments within hosts. Within the protist phylum Apicomplexa major clades include the malaria parasites, coccidians, and most diverse, the gregarines (with likely millions of species). Studies on life history variation of gregarines are rare. Therefore, life history traits were examined for the gregarine Monocystis perplexa in its host, the invasive earthworm Amynthas agrestis at three sites in northern Vermont, United States of America. An important value of this system is the short life-span of the hosts, with only seven months from hatching to mass mortality; we were thus able to examine life history variation during the entire life cycle of both host and parasite. Earthworms were collected (N = 968 over 33 sample periods during one host season), then parasites of all life stages were counted, and sexual and transmission stages measured, for each earthworm. All traits varied substantially among individual earthworm hosts and across the sites. Across sites, timing of first appearance of infected earthworms, date when transmission stage (oocysts packed within gametocysts) appeared, date when number of both feeding (trophic) cells and gametocysts were at maximum, and date when 100% of earthworms were infected differed from 2–8 weeks, surprising variation for a short season available for parasite development. The maximal size of mating cells varied among hosts and across sites and this is reflected in the number of oocysts produced by the gametocyst. A negative trade-off was observed for the number of oocysts and their size. Several patterns were striking: (1) Prevalence reached 100% at all sites by mid season, only one to three weeks after parasites first appeared in the earthworms. (2) The number of parasites per host was large, reaching 300 × 103 cells in some hosts, and such high numbers were present even when parasites first appeared in the host. (3) At one site, few infected earthworms produced any oocysts. (4) The transmission rate to reach such high density of parasites in hosts needed to be very high for a microbe, from >0.33% to >34.3% across the three sites. Monocystis was one of the first protist parasites to have its life cycle described (early 19th century), but these results suggest the long-accepted life cycle of Monocystis could be incomplete, such that the parasites may be transmitted vertically (within the earthworm’s eggs) as well as horizontally (leading to 100% prevalence) and merogony (asexual replication) could be present, not recognized for Monocystis, leading to high parasitemia even very early in the host’s season.https://peerj.com/articles/17161.pdfEcologyLife History TraitsParasitologyProtistsGregarinesParasite of invasive earthworms
spellingShingle Erin L. Keller
Jos. J. Schall
Variation and trade-offs in life history traits of the protist parasite Monocystis perplexa (Apicomplexa) in its earthworm host Amynthas agrestis
PeerJ
Ecology
Life History Traits
Parasitology
Protists
Gregarines
Parasite of invasive earthworms
title Variation and trade-offs in life history traits of the protist parasite Monocystis perplexa (Apicomplexa) in its earthworm host Amynthas agrestis
title_full Variation and trade-offs in life history traits of the protist parasite Monocystis perplexa (Apicomplexa) in its earthworm host Amynthas agrestis
title_fullStr Variation and trade-offs in life history traits of the protist parasite Monocystis perplexa (Apicomplexa) in its earthworm host Amynthas agrestis
title_full_unstemmed Variation and trade-offs in life history traits of the protist parasite Monocystis perplexa (Apicomplexa) in its earthworm host Amynthas agrestis
title_short Variation and trade-offs in life history traits of the protist parasite Monocystis perplexa (Apicomplexa) in its earthworm host Amynthas agrestis
title_sort variation and trade offs in life history traits of the protist parasite monocystis perplexa apicomplexa in its earthworm host amynthas agrestis
topic Ecology
Life History Traits
Parasitology
Protists
Gregarines
Parasite of invasive earthworms
url https://peerj.com/articles/17161.pdf
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