PerspectiveMicrobiomes are integral to conservation of parasitic arthropods
Graphical abstract
Introduction
Though often overlooked, global parasite biodiversity is threatened by environmental change and declining host biodiversity (Gómez et al., 2012; Rocha et al., 2016; Carlson et al., 2017). Indeed, all species are hosts for parasitic organisms, supporting a remarkable diversity of parasitic species, and the loss of these parasite species from ecosystems may have unforeseen negative consequences (Gómez et al., 2012; Stringer and Linklater, 2014; Wood and Johnson, 2015; Dougherty et al., 2016). Climate change-induced habitat alteration alone is expected to cause a global loss of 5–10% of parasite diversity by 2070, with ectoparasites experiencing greater extinction risk than endoparasites (Carlson et al., 2017). Parasites with high host specificity, a complex life cycle, or narrow environmental preferences will be impacted most severely (Cizauskas et al., 2017). As arthropods comprise the majority of classified animal life on earth (Giribet and Edgecombe, 2012) and the majority of parasitic animals are arthropods (Weinstein and Kuris, 2016), extinction of parasitic arthropod species represents a significant threat to biodiversity.
Parasites are most commonly viewed as hurdles along the path towards conservation of free-living host species, rather than the target of conservation efforts themselves (Stringer and Linklater, 2014; Dougherty et al., 2016). However, increasing evidence shows that parasites contribute to healthy host immune response, host population regeneration, ecological network stability, and nutrient cycling (Gómez et al., 2012; Hatcher et al., 2012; Wood and Johnson, 2015; Dougherty et al., 2016). For example, in humans, infection with some helminth parasites modulates the immune response and eases the effects of autoimmune diseases, like Crohn's disease and multiple sclerosis (Summers et al., 2005; Correale and Farez, 2007; Maizels, 2019). Mussels parasitized by endoliths are better able to survive bouts of extreme heat stress than non-infected individuals (Zardi et al., 2016). The trematode Cryptocotyle lingua (Plagiorchiida; Heterophyidae) decreases grazing rate of the common periwinkle snail (Littorina littorea), allowing greater macroalgae abundance for other marine herbivores (Wood et al., 2007). While parasites by definition harm their hosts to varying degrees, the net effect on populations and communities can be beneficial through the ecological functions they contribute.
A community of organisms is more than what meets the eye. If we follow the concept of the holobiont, where an individual organism is actually a composite of itself and associated microbes, and extend it to the scale of communities, then a community is a reflection of the millions of microscopic interactions that occur between the macro and microorganisms occupying a shared space. Even the interactions between hosts and parasites in a community, which are seemingly governed by their own evolutionary associations, are impacted by microorganisms (Dheilly, 2014; Kemen, 2014; Dheilly et al., 2015). The role of parasitic arthropods as hosts of microbes, vectors of microbes, and drivers of free-living host–microbe interactions has not been examined in the context of parasite conservation. Microbes are necessary to the development, immune response, and reproduction of parasitic arthropods (Engel and Moran, 2013; Narasimhan and Fikrig, 2015; Contreras-Garduño et al., 2016) and must be considered an integral part of efforts to stem global biodiversity loss.
Here, we provide a brief review of the importance of microbes to parasitic arthropods and outline areas of future research necessary to preserving parasitic arthropod biodiversity. Weinstein and Kuris (2016) define a parasite as a consumer that feeds on a maximum of one host individual during at least one life stage. We build on this definition to also include organisms that obligately feed on a single host species, regardless of the number of individuals, during at least one life stage. This definition excludes some micropredators like mosquitoes and tsetse flies, but includes others like louse flies, bat flies, and fish mites. Our current knowledge is biased towards insect parasites in the Order Diptera and arachnid parasites in the Subclass Acari, the two clades that contain the majority of parasitic arthropods (Weinstein and Kuris, 2016) and are therefore the focus of this review. However, we encourage the scientific community to investigate the role of microbes in the biology and ecology of other parasitic arthropods (c.f. Agany et al., 2020).
Section snippets
Parasite microbiomes are central to parasite health and reproduction
The microbiome is composed of archaea, bacteria, fungi, protozoa, and viruses. The sources of microbes found within parasites are not completely known, but likely include the broader environmental microbiome, the host microbiome, and the microbiomes of other parasite individuals within the same population (Fig. 1A). Primary and secondary bacterial symbionts share close evolutionary histories with their hosts and are typically maternally inherited (Moran et al., 2008). These bacteria provision
The link between host and parasite microbiomes and parasitic arthropod conservation
We cannot fully address projected parasite biodiversity loss without accounting for the multidimensional nature of hosts, parasitic arthropods, and the microbes that mediate their interactions. Microbiome perturbations may effectively limit the suitable habitat for parasitic arthropods, putting them at greater risk of extinction in the face of environmental change. Suitable “habitat” for parasitic arthropods encompasses both the host and broader environment where the host lives. The link
Directions for future conservation efforts
Conservation strategies targeting free-living arthropod species are broadly used to improve agricultural and natural landscapes, and to prevent arthropod biodiversity loss (Lattin, 1993; Hartley et al., 2007; Gaspar et al., 2011; Sebek et al., 2016; Mader et al., 2017). For example, many species of butterflies and moths have had or continue to have their populations supplemented by captive breeding programs to counteract declines caused by climate change and habitat loss (Ngoka et al., 2007;
Conclusion
Parasitic arthropod microbiomes offer opportunities for future research with implications for community ecology and evolutionary biology, conservation of global biodiversity, and disease ecology of pathogens relevant to human health, livestock, crops, and wildlife. The microbiome mediates the development, health, and reproduction of parasitic arthropods as well as the interactions of parasitic arthropods with the outside world. Through this interdependence, microbiomes must be a primary
Declaration of competing interest
The authors have no conflicts to declare.
Acknowledgments
Thank you to Dr. Skylar Hopkins and Dr. Colin Carlson for organizing this special issue on parasite conservation and inviting us to participate. Thank you to Dr. Kayce Bell for recommending us to the organizers. Thank you to three reviewers whose insights greatly improved the manuscript. We acknowledge the use of PhyloPic silhouettes for Fig. 1, which were created by Matt Crook (Gammaproteobacteria; https://creativecommons.org/licenses/by/3.0/), Tracy Heath (Querqus), Anne-Caroline Heintz
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