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1. The seed transcriptome of Rafflesia reveals horizontal gene transfer and convergent evolution: Implications for conserving the world's largest flower

   https://doi.org/10.1002/ppp3.10370  

   Molina, Jeanmaire ; Wicaksono, Adhityo ; Michael, Todd P. ; Kwak, Su‐Hwan ; Pedales, Ronniel D. ; Joly‐Lopez, Zoé ; Petrus, Semar ; Mamerto, Allen ; Tomek, Brian ; Ahmed, Sumaya ; et al ( April 2023 , PLANTS, PEOPLE, PLANET)

   Rafflesiais a genus of parasitic plants with the largest flowers in the world, unique to the threatened forest habitats of tropical Asia. Here, we report on genes that are active (the transcriptome) inRafflesiaseeds as part of a larger effort to understandRafflesia.Rafflesiahas never been grown successfully outside of its native range. Consequently, seed banking is not yet possible, precluding a critical management strategy for conservation. The study ofRafflesiaseed biology is a critical step to improve its cultivation, which will educate the public about unique species and the importance of conserving their habitats.

   Rafflesiais of great interest as one of the only two plants known to have completely lost its chloroplast genome.Rafflesiais a holoparasite and an endophyte that lives inside the tissues of its host, a tropical grape vine (Tetrastigma), emerging only to bloom—with the largest flower of any plant. Here, we report the firstRafflesiaseed transcriptome and compare it with those of other plants to deepen our understanding of its extraordinary life history.

   We assembled a transcriptome from RNA extracted from seeds of the Philippine endemicRafflesia speciosaand compared this with those of other plants, includingArabidopsis, parasitic plantsStrigaandCuscuta, and the mycoheterotrophic orchidAnoectochilus.

   Genetic and metabolic seed pathways inRafflesiawere generally similar to the other plant species. However, there were some notable exceptions. We found evidence of horizontal transfer of a gene potentially involved in circumventing host defenses. Moreover, we identified a possible convergence among parasitic plants becauseRafflesia,Striga, andCuscutashared important similarities. We were unable to find evidence of genes involved in mycorrhizal symbiosis, suggesting that mycoheterotrophy is unlikely to play a role inRafflesiaparasitism.

   To date, ex situ propagation ofRafflesiaby seed has been mostly unsuccessful. Our research is a bold step forward in understanding the fundamentals ofRafflesiaseed biology that will inform the continued propagation and seed‐banking efforts concerning this recalcitrant plant. We discuss our findings in the broader context of the conservation of a genus in peril.

    

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2. Parasitic flowering plant collections embody the extended specimen

   https://doi.org/10.1111/2041-210X.13866  

   Teixeira‐Costa, Luiza ; Heberling, J. Mason ; Wilson, Carol A. ; Davis, Charles C. ( April 2022 , Methods in Ecology and Evolution)

   The widespread digitization of natural history collections, combined with novel tools and approaches is revolutionizing biodiversity science. The ‘extended specimen’ concept advocates a more holistic approach in which a specimen is framed as a diverse stream of interconnected data. Herbarium specimens that by their very nature capture multispecies relationships, such as certain parasites, fungi and lichens, hold great potential to provide a broader and more integrative view of the ecology and evolution of symbiotic interactions. This particularly applies to parasite–host associations, which owing to their interconnectedness are especially vulnerable to global environmental change.

   Here, we present an overview of how parasitic flowering plants is represented in herbarium collections. We then discuss the variety of data that can be gathered from parasitic plant specimens, and how they can be used to understand global change impacts at multiple scales. Finally, we review best practices for sampling parasitic plants in the field, and subsequently preparing and digitizing these specimens.

   Plant parasitism has evolved 12 times within angiosperms, and similar to other plant taxa, herbarium collections represent the foundation for analysing key aspects of their ecology and evolution. Yet these collections hold far greater potential. Data and metadata obtained from parasitic plant specimens can inform analyses of co‐distribution patterns, changes in eco‐physiology and species plasticity spanning temporal and spatial scales, chemical ecology of tripartite interactions (e.g. host–parasite–herbivore), and molecular data critical for species conservation. Moreover, owing to the historic nature and sheer size of global herbarium collections, these data provide the spatiotemporal breadth essential for investigating organismal response to global change.

   Parasitic plant specimens are primed to serve as ideal examples of extended specimen concept and help motivate the next generation of creative and impactful collection‐based science. Continued digitization efforts and improved curatorial practices will contribute to opening these specimens to a broader audience, allowing integrative research spanning multiple domains and offering novel opportunities for education.

    

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3. Infectivity of the parasite Metschnikowia bicuspidata is decreased by time spent as a transmission spore, but exposure to phycotoxins in the water column has no effect

   https://doi.org/10.1111/fwb.14082  

   Sánchez, Kristel F. ; Zhong, Baili ; Agudelo, Jorge A. ; Duffy, Meghan A. ( April 2023 , Freshwater Biology)

   Transmission from one host to another is a crucial component of parasite fitness. For some aquatic parasites, transmission occurs via a free‐living stage that spends time in the water, awaiting an encounter with a new host. These parasite transmission stages can be impacted by biotic and abiotic factors that influence the parasite's ability to successfully infect or grow in a new host.

   Here we tested whether time spent in the water column and/or exposure to common cyanobacterial toxins impacted parasite transmission stages. More specifically, we tested whether the infectivity, within host growth, and virulence of the fungal parasiteMetschnikowia bicuspidatachanged as a result of time spent in the water or from exposure to cyanotoxins in the water column. We exposed parasite transmission spores to different levels of one of two ecologically important cyanotoxins, microcystin‐LR and anatoxin‐a, and factorially manipulated the amount of time spores were incubated in water. We removed the toxins and used those same spores to infect one genotype of the common lake zooplanktonDaphnia dentifera.

   We found that cyanotoxins did not impact parasite fitness (infection prevalence and spore yield per infected host) or virulence (host lifetime reproduction and survivorship) at the tested concentrations (10 and 30 μg/L). However, we found that spending longer as a transmission spore decreased a spore's chances for successful infection: spores that were only incubated for 24 hr infected approximately 75% of exposed hosts, whereas spores incubated for 10 days infected less than 50% of exposed hosts.

   We also found a negative relationship between the final spore yield from infected hosts and the proportion of hosts that became infected. In treatments where spores spent longer in the water column prior to encountering a host, infection prevalence was lower (indicating lower per spore infectivity), but each infected host yielded more spores at the end of infection. We hypothesise that this pattern may result from intraspecific parasite competition within the host.

   Overall, these results suggest that transmission spores of this parasite are not strongly influenced by cyanotoxins in the water column, but that other aspects of spending time in the water strongly influence parasite fitness.

    

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4. A role for the local environment in driving species‐specific parasitism in a multi‐host parasite system

   https://doi.org/10.1111/fwb.13961  

   Hasik, Adam Z. ; Siepielski, Adam M. ( June 2022 , Freshwater Biology)

   The extent and magnitude of parasitism often vary among closely related host species and across populations within species. Determining the ecological basis for this species and population‐level variation in parasitism is critical for understanding infection dynamics in multi‐host–parasite systems. To investigate such ecological underpinnings of variation in parasitism, we studiedEnallagmadamselfly host species and their water mite (Arrenurusspp.) ectoparasites in lakes.

   We first evaluated how host identity and density could shape parasitism. To test the effects of con‐ and heterospecific host density on parasitism, we used a field experiment withEnallagma basidensandE. signatum. We found that parasitism did not vary with con‐ or heterospecific density and was determined by host identity alone, with no spillover effects.

   We also evaluated the potential role of local adaptation and resource availability in shaping parasitism. To do so, we usedE. signatumin a reciprocal transplant experiment crossed with a prey resource‐level manipulation. This experiment revealed that parasitism declined sharply for one host population in its non‐local lake, but not the other source population, with no effects of prey levels. This asymmetry implies that damselflies express enhanced defences against parasitism that are neither population‐specific nor dependent on resource abundance, or that mites developed heightened local host specificity.

   The results of multivariate modeling from an observational study generally supported these experimental findings: neither host density nor resource abundance strongly explained among‐population variation in parasitism. Instead, local abiotic conditions (pH) had the strongest relationship with parasitism, with minimal associations with predator density, temperature and a measure of immune function.

   Collectively, our findings suggest a crucial role for the local environment in shaping host–parasite interactions within multi‐host–parasite systems. More generally, these results show that research at the intersection of community ecology and disease ecology is critical for understanding host–parasite dynamics within natural communities.

    

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5. Beyond single host, single parasite interactions: Quantifying competence for complete multi‐host, multi‐parasite communities

   https://doi.org/10.1111/1365-2435.14068  

   Stewart Merrill, Tara E. ; Calhoun, Dana M. ; Johnson, Pieter T. J. ( May 2022 , Functional Ecology)

   Understanding parasite transmission in communities requires knowledge of each species' capacity to support transmission. This property, ‘competence’, is a critical currency for modelling transmission under community change and for testing diversity–disease theory. Despite the central role of competence in disease ecology, we lack a clear understanding of the factors that generate competence and drive its variation.

   We developed novel conceptual and quantitative approaches to systematically quantify competence for a multi‐host, multi‐parasite community. We applied our framework to an extensive dataset: five amphibian host species exposed to four parasitic trematode species across five ecologically realistic exposure doses. Together, this experimental design captured 20 host–parasite interactions while integrating important information on variation in parasite exposure. Using experimental infection assays, we measured multiple components of the infection process and combined them to produce competence estimates for each interaction.

   With directly estimated competence values, we asked which components of the infection process best explained variation in competence: barrier resistance (the initial fraction of administered parasites blocked from infecting a host), internal clearance (the fraction of established parasites lost over time) or pre‐transmission mortality (the probability of host death prior to transmission). We found that variation in competence among the 20 interactions was best explained by differences in barrier resistance and pre‐transmission mortality, underscoring the importance of host resistance and parasite pathogenicity in shaping competence.

   We also produced dose‐integrated estimates of competence that incorporated natural variation in exposure to address questions on the basis and extent of variation in competence. We found strong signals that host species identity shaped competence variation (as opposed to parasite species identity). While variation in infection outcomes across hosts, parasites, individuals and doses was considerable, individual heterogeneity was limited compared to among‐species differences. This finding highlights the robustness of our competence estimates and suggests that species‐level values may be strong predictors for community‐level transmission in natural systems.

   Competence emerges from distinct underlying processes and can have strong species‐level characteristics; thus, this property has great potential for linking mechanisms of infection to epidemiological patterns.

   Read the freePlain Language Summaryfor this article on the Journal blog.

    

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