skip to main content


Title: Phanerozoic parasitism and marine metazoan diversity: Dilution versus amplification
Growing evidence suggests that biodiversity mediates parasite prevalence. We have compiled the first global database on occurrences and prevalence of marine parasitism throughout the Phanerozoic and assess the relationship with biodiversity to test if there is support for amplification or dilution of parasitism at the macroevolutionary scale. Median prevalence values by era are 5% for the Paleozoic, 4% for the Mesozoic, and a significant increase to 10% for the Cenozoic. We calculated period-level shareholder quorum sub-sampled (SQS) estimates of mean sampled diversity, three-timer (3T) origination rates, and 3T extinction rates for the most abundant host clades in the Paleobiology Database to compare to both occurrences of parasitism and the more informative parasite prevalence values. Generalized linear models (GLMs) of parasite occurrences and SQS diversity measures support both the amplification (all taxa pooled, crinoids and blastoids, and molluscs) and dilution hypotheses (arthropods, cnidarians, and bivalves). GLMs of prevalence and SQS diversity measures support the amplification hypothesis (all taxa pooled and molluscs). Though likely scale-dependent, parasitism has increased through the Phanerozoic and clear patterns primarily support the amplification of parasitism with biodiversity in the history of life. This article is part of the theme issue ‘Infectious disease macroecology: parasite diversity and dynamics across the globe’.  more » « less
Award ID(s):
1650745
NSF-PAR ID:
10328115
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
Philosophical transactions
Volume:
376
ISSN:
1471-2970
Page Range / eLocation ID:
20200366
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Temperature increases due to climate change have affected the distribution and severity of diseases in natural systems, causing outbreaks that can destroy host populations. Host identity, diversity, and the associated microbiome can affect host responses to both infection and temperature, but little is known about how they could function as important mediators of disease in altered thermal environments. We conducted an 8‐week warming experiment to test the independent and interactive effects of warming, host genotypic identity, and host genotypic diversity on the prevalence and intensity of infections of seagrass (Zostera marina) by the wasting disease parasite (Labyrinthula zosterae). At elevated temperatures, we found that genotypically diverse host assemblages had reduced infection intensity, but not reduced prevalence, relative to less diverse assemblages. This dilution effect on parasite intensity was the result of both host composition effects as well as emergent properties of biodiversity. In contrast with the benefits of genotypic diversity under warming, diversity actually increased parasite intensity slightly in ambient temperatures. We found mixed support for the hypothesis that a growth–defense trade‐off contributed to elevated disease intensity under warming. Changes in the abundance (but not composition) of a few taxa in the host microbiome were correlated with genotype‐specific responses to wasting disease infections under warming, consistent with the emerging evidence linking changes in the host microbiome to the outcome of host–parasite interactions. This work emphasizes the context dependence of biodiversity–disease relationships and highlights the potential importance of interactions among biodiversity loss, climate change, and disease outbreaks in a key foundation species.

     
    more » « less
  2. Abstract

    Understanding of community assembly has been improved by phylogenetic and trait‐based approaches, yet there is little consensus regarding the relative importance of alternative mechanisms and few studies have been done at large geographic and phylogenetic scales. Here, we use phylogenetic and trait dispersion approaches to determine the relative contribution of limiting similarity and environmental filtering to community assembly of stream fishes at an intercontinental scale. We sampled stream fishes from five zoogeographic regions. Analysis of traits associated with habitat use, feeding, or both resulted in more occurrences of trait underdispersion than overdispersion regardless of spatial scale or species pool. Our results suggest that environmental filtering and, to a lesser extent, species interactions were important mechanisms of community assembly for fishes inhabiting small, low‐gradient streams in all five regions. However, a large proportion of the trait dispersion values were no different from random. This suggests that stochastic factors or opposing assembly mechanisms also influenced stream fish assemblages and their trait dispersion patterns. Local assemblages tended to have lower functional diversity in microhabitats with high water velocity, shallow water depth, and homogeneous substrates lacking structural complexity, lending support for the stress‐dominance hypothesis. A high prevalence of functional underdispersion coupled with phylogenetic underdispersion could reflect phylogenetic niche conservatism and/or stabilizing selection. These findings imply that environmental filtering of stream fish assemblages is not only deterministic, but also influences assemblage structure in a fairly consistent manner worldwide.

     
    more » « less
  3. Abstract

    Diverse host communities commonly inhibit the spread of parasites at small scales. However, the generality of this effect remains controversial. Here, we present the analysis of 205 biodiversity–disease relationships on 67 parasite species to test whether biodiversity–disease relationships are generally nonlinear, moderated by spatial scale, and sensitive to underrepresentation in the literature. Our analysis of the published literature reveals that biodiversity–disease relationships are generally hump-shaped (i.e., nonlinear) and biodiversity generally inhibits disease at local scales, but this effect weakens as spatial scale increases. Spatial scale is, however, related to study design and parasite type, highlighting the need for additional multiscale research. Few studies are unrepresentative of communities at low diversity, but missing data at low diversity from field studies could result in underreporting of amplification effects. Experiments appear to underrepresent high-diversity communities, which could result in underreporting of dilution effects. Despite context dependence, biodiversity loss at local scales appears to increase disease, suggesting that at local scales, biodiversity loss could negatively impact human and wildlife populations.

     
    more » « less
  4. Abstract Aim

    Characterizing macroecological patterns in biodiversity is key to improve our understanding of community assembly. Global biodiversity for many taxa follows a latitudinal gradient, with increased diversity in tropical latitudes. Less is known about global parasite biodiversity, inhibiting our ability to predict how global change will impact parasitic disease emergence. Using distribution and phylogenetic data for 2,386 avian haemosporidian blood parasites (generaPlasmodium,HaemoproteusandLeucocytozoon), I assessed how contemporary and historical drivers influence the composition of parasite communities worldwide.

    Location

    Global.

    Time period

    Current.

    Major taxa studied

    Haemosporidian blood parasites.

    Methods

    Parasite distribution and cytochrome bsequence data were accessed from an open‐source database. Bayesian phylogenetic tree distributions were constructed for each parasite genus using two substitution models to capture uncertainty. Hierarchical regressions assessed effects of environmental variation, latitude and phylogenetic β‐diversity (βdiv; a proxy for phylogenetic uniqueness) on the diversity and asymmetry of parasite communities around the globe.

    Results

    I uncovered biodiversity hotspots and identified broad variation in global diversity patterns among parasite genera. Community diversity increased with increasing phylogenetic uniqueness for all three parasite genera; however, these diverse and unique regions did not consistently occur in the tropics. I found no evidence of a latitudinal diversity gradient, and support for a latitudinal gradient in community phylogenetic asymmetry was weak.

    Main conclusions

    Global variation in avian haemosporidian phylogenetic diversity does not reflect a latitudinal gradient. Instead, parasite biogeography may reflect fundamental differences in host‐switching tendencies or the timing of avian evolutionary radiations. Examining the interplay between shared evolutionary history and phylogenetic diversity can provide important insights into the drivers of parasite biodiversity at global scales.

     
    more » « less
  5. Vermeij, Geerat J. (Ed.)
    Rapid warming and sea-level rise are predicted to be major driving forces in shaping coastal ecosystems and their services in the next century. Though forecasts of the multiple and complex effects of temperature and sea-level rise on ecological interactions suggest negative impacts on parasite diversity, the effect of long term climate change on parasite dynamics is complex and unresolved. Digenean trematodes are complex life cycle parasites that can induce characteristic traces on their bivalve hosts and hold potential to infer parasite host-dynamics through time and space. Previous work has demonstrated a consistent association between sea level rise and increasing prevalence of trematode traces, but a number of fundamental questions remain unanswered about this paleoecological proxy. Here we examine the relationships of host size, shape, and functional morphology with parasite prevalence and abundance, how parasites are distributed across hosts, and how all of these relationships vary through time, using the bivalve Chamelea gallina from a Holocene shallow marine succession in the Po coastal plain. Trematode prevalence increased and decreased in association with the transition from a wave-influenced estuarine system to a wave-dominated deltaic setting. Prevalence and abundance of trematode pits are associated with large host body size, reflecting ontogenetic accumulation of parasites, but temporal trends in median host size do not explain prevalence trends. Ongoing work will test the roles of temperature, salinity, and nutrient availability on trematode parasitism. Parasitized bivalves in one sample were shallower burrowers than their non-parasitized counterparts, suggesting that hosts of trematodes can be more susceptible to their predators, though the effect is ephemeral. Like in living parasite-host systems, trematode-induced malformations are strongly aggregated among hosts, wherein most host individuals harbor very few parasites while a few hosts have many. We interpret trace aggregation to support the assumption that traces are a reliable proxy for trematode parasitism in the fossil record. 
    more » « less