Genotypic variation in an ecologically important parasite is associated with host species, lake and spore size

Shaw, Cheng-Kuang; Bilich, Rebecca; O’Brien, Bruce; Cáceres, Carla E.; Hall, Spencer R.; James, Timothy Y.; Duffy, Meghan A.

doi:10.1017/s0031182021000949

Cited by 13 publications

(26 citation statements)

References 70 publications

(100 reference statements)

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“…Daphnia are also frequently infected by several microbial parasite species [20], which can impact Daphnia population dynamics and have cascading impacts on food webs [21]. The yeast Metschnikowia bicuspidata (Ascomycota: Saccharomycetales) is a generalist parasite that is commonly found infecting many Daphnia species (as well as other Cladocerans) in nature [20,[22][23][24][25]. In stratified lakes in the Midwestern United States, infection by M. bicuspidata typically happens annually during late summer/early autumn and can reach up to 60% prevalence in some populations [26,27].…”

Section: Introductionmentioning

confidence: 99%

Temperature modifies trait-mediated infection outcomes in aDaphnia–fungal parasite system

Sun

Dziuba

Jaye

et al. 2023

Phil. Trans. R. Soc. B

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One major concern related to climate change is that elevated temperatures will drive increases in parasite outbreaks. Increasing temperature is known to alter host traits and host–parasite interactions, but we know relatively little about how these are connected mechanistically—that is, about how warmer temperatures impact the relationship between epidemiologically relevant host traits and infection outcomes. Here, we used a zooplankton–fungus ( Daphnia dentifera–Metschnikowia bicuspidata ) disease system to experimentally investigate how temperature impacted physical barriers to infection and cellular immune responses. We found that Daphnia reared at warmer temperatures had more robust physical barriers to infection but decreased cellular immune responses during the initial infection process. Infected hosts at warmer temperatures also suffered greater reductions in fecundity and lifespan. Furthermore, the relationship between a key trait—gut epithelium thickness, a physical barrier—and the likelihood of terminal infection reversed at warmer temperatures. Together, our results highlight the complex ways that temperatures can modulate host–parasite interactions and show that different defense components can have qualitatively different responses to warmer temperatures, highlighting the importance of considering key host traits when predicting disease dynamics in a warmer world. This article is part of the theme issue ‘Infectious disease ecology and evolution in a changing world’.

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Section: Introductionmentioning

confidence: 99%

Temperature modifies trait-mediated infection outcomes in aDaphnia–fungal parasite system

Sun

Dziuba

Jaye

et al. 2023

Phil. Trans. R. Soc. B

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“…The study is novel in exploring how risk of infection by Metschnikowia shaped immune traits. Because Metschnikowia does not show high levels of detectable genetic variation (Searle et al, 2015 ; Shaw et al, 2021 ), the risk Daphnia face should be proportional to the abundance of the pathogen in the environment. Some invertebrates with phenotypically plastic immune traits boost their immune responses when living in crowded conditions or in conditions that might lead to higher prevalence of disease (Reeson et al, 1998 ).…”

Section: Discussionmentioning

confidence: 99%

“…The repeated occurrence of genotypes across environmental conditions enables the partitioning of traits among genotypic and environmental sources of variation. Third, within populations of Daphnia dentifera , the Metschnikowia parasite has been observed to have limited detectable genetic variation, suggesting that genotype‐by‐genotype interactions are less important in this system than others (Searle et al, 2015 ; Shaw et al, 2021 ). Finally, the transparency of Daphnia allows researchers to visually assess infection and efficiently and effectively measure immune traits (Stewart Merrill et al, 2019 ; Stewart Merrill & Cáceres, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

Partitioning variance in immune traits in a zooplankton host—Fungal parasite system

Westphal

Merrill

2022

Ecology and Evolution

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Host immune traits arise from both genetic and environmental sources of variation. When immune traits have a strong genetic basis, the presence and severity of disease in a population may influence the distribution of those traits. Our study addressed how two immune‐related traits (gut penetrability and the hemocyte response) are shaped by genetic and environmental sources of variation, and how the presence of a virulent disease altered the relative frequency of these traits in natural populations. Daphnia dentifera hosts were sampled from five Indiana lakes between June and December 2017 before and during epidemics of their fungal pathogen, Metschnikowia bicuspidata . Collected Daphnia were experimentally exposed to Metschnikowia and assayed for their gut penetrability, hemocyte response, and multi‐locus genotype. Mixed‐effects models were constructed to partition variance in immune traits between genetic and environmental sources. We then isolated the genetic sources to produce genotype‐specific estimates of immune traits for each multi‐locus genotype. Finally, we assessed the relative frequency and dynamics of genotypes during epidemics and asked whether genotypes with more robust immune responses increased in frequency during epidemics. Although genotype was an important source of variation for both gut penetrability and the hemocyte response, environmental factors (e.g., resource availability, Metschnikowia prevalence, and co‐infection) still explained a large portion of observed variation, suggesting a high degree of flexibility in Daphnia immune traits. Additionally, no significant associations were detected between a genotype's immune traits and its frequency in a population. Our study highlights the power of variance partitioning in understanding the factors driving variation in Daphnia traits and motivates further research on immunological flexibility and the ecological drivers of immune variation.

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“…The switch of host or infected tissue represent important driving factors for genetic differentiation, even novel speciation. Meanwhile, genetic variation of pathogens is possible associated with the virulence of pathogens which directly determine the infection consequences ( Eggert et al, 2021 ; Shaw et al, 2021 ). Therefore, insights into population genetics of some microsporidia species of economic importance will benefit for the control of microsporidiosis in aquaculture.…”

Section: Introductionmentioning

confidence: 99%

Intraspecific genetic diversity of the fish-infecting microsporidian parasite Pseudokabatana alburnus (Microsporidia)

Weng

Zhang²,

Xin³

et al. 2023

Front. Microbiol.

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Pseudokabatana alburnus is a xenoma-forming fish microsporidium, firstly described from the liver of the Culter alburnus from Poyang Lake in China. In the present study, P. alburnus was firstly reported from the ovary of 6 other East Asian minnows, including Squaliobarbus curriculus, Hemiculter leucisculus, Cultrichthys erythropterus, Pseudolaubuca engraulis, Toxabramis swinhonis, and Elopichthys bambusa. Genetic analysis revealed high sequence diversity in the ribosomal internal transcribed spacer region (ITS) and the largest subunit of RNA polymerase II (Rpb1) loci of P. alburnus isolated from different hosts and locations. The variation of Rpb1 mainly occurred in the 1,477–1737 bp regions. The presence of a wide variety of Rpb1 haplotypes within a single fish host, together with evidence of genetic recombination suggested that P. alburnus may have the intergenomic variation and sexual reproduction might be present in other hosts (possibly freshwater shrimp). Phylogenetic analysis and population genetic analysis showed that there was no geographical population divergence for P. alburnus. Homogeneity and high variability of ITS sequences indicates that ITS may be a suitable molecular marker to distinguish different P. alburnus isolates. Our data confirm the broad geographical distribution and host range of P. alburnus in the middle and lower reaches of the Yangtze River. Additionally, we emendated the genus Pseudokabatana to exclude the infection site, liver as one of the taxonomic criteria, and proposed that fish ovary was be the general infection site of P. alburnus.

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Genotypic variation in an ecologically important parasite is associated with host species, lake and spore size

Abstract: Abstract

Cited by 13 publications

References 70 publications

Temperature modifies trait-mediated infection outcomes in aDaphnia–fungal parasite system

Temperature modifies trait-mediated infection outcomes in aDaphnia–fungal parasite system

Partitioning variance in immune traits in a zooplankton host—Fungal parasite system

Intraspecific genetic diversity of the fish-infecting microsporidian parasite Pseudokabatana alburnus (Microsporidia)

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